indirect effects of a marine ecosystem engineer alter...
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INDIRECT EFFECTS OF A MARINE ECOSYSTEM ENGINEER ALTER THE ABUNDANCE AND DISTRIBUTION OF FOUNDATION CORAL SPECIES
By
JADA-SIMONE SHANTI WHITE
A DISSERTATION PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT
OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY
UNIVERSITY OF FLORIDA
2010
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© 2010 Jada-Simone Shanti White
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To all my Mother and my Sammy
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ACKNOWLEDGMENTS
First and foremost, I thank my Mother. She was my provider and my inspiration:
she taught me to value integrity and that contributing to knowledge and education was a
noble career path. My Grandmother, Sammy (Eileen) Ringold, also provided a positive
role model and broadened my horizons in various ways throughout my life. My Father,
William B. White, and other Grandparents, Ross D. Reeves, and Elmer and Nancy
White, offered support, inspiration, and encouragement throughout my life. My first
employer, Dr. John B. Roberts, and my first mentor in Field Ecology, Albin Bills, taught
me about graduate school and fostered my belief that, through science and education, I
could have a positive influence on the world. My amazing brothers, Jaaron, Tory, and
Tealson, as well as my dear chosen sisters, Cailyn, Kendee Rae, Jen Rose, and Erica
Lena, offered unconditional support and love; despite my, often ridiculous, travel
schedules. My wonderful nephews, Sage, Shilo, and Seth, and the rest of the beloved
children of our community, especially Ayden, Lauren, and Thomas, reminded me
through our snorkeling adventures that the youth have a yearning desire to know about
the natural world and that a life in pursuit of this knowledge was valuable and inspiring.
I am extremely grateful to Benjamin M. Bolker, Gustav Paulay, and members of
my supervisory committee, Karen Bjorndal, Bill Lindberg, Brian R. Silliman, and Colette
M. St. Mary, for their mentoring, support, and, especially, for providing exceptional
models for academic and professional conduct for me to glean from (in countless
ways!). Craig Osenberg taught me to value critical exchange, reinforced the strong
experimental design training I had gained at UCSB, and improved my writing
significantly, for which I will always be grateful (and no, I do not believe that the error
bars ever overlapped zero). Ben Bolker taught me to write using outlines, how to “be
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quantitative”, in particular, he improved both my accuracy at, and understanding of,
ecological inference, and, of course, he taught me how to program in R; while Gustav
Paulay corrected my natural history knowledge and improved my precision in species
identifications, writing, and scientific presentations. These skills were invaluable to my
success as a graduate student and will be treasured and passed on with pride. Karen
Bjorndal reinforced the importance of nutritional ecology and, through her work as
Director of the Archie Carr Sea Turtle Center and a seminar in Sea Turtle Biology,
exemplified the multi-faceted approach that is necessary do effective conservation
science. Bill Lindberg broadened my critical thinking skills, as well as my historical
knowledge of scientific philosophies. Brian Silliman’s enthusiasm was contagious and
he taught me to focus on the main story, first and foremost. Colette St. Mary exemplified
the linking theory with data that I had learned to strive toward as an undergraduate and
offered support and mentoring at critical times. The St. Mary-Osenberg-Bolker Lab
fostered a love of critical exchange and offered the fine polishing that I needed to grow;
while the Paulay lab supported my knowledge (and love) of natural history, including
tried and true species identification, collection, and curation skills, as well as cutting
edge approaches. Marta Wayne, was a powerful role model and offered crucial support
as the Faculty Advisor of our grass roots organization, Women in Science and
Engineering; she was also a dear friend. I am also grateful to the staff and members at
the Department of Biology, in particular Karen Patterson and Cathy Moore, for their
countless assistance through the years. Daniella Ceccarelli, Richard Aronson, and one
anonymous reviewer offered helpful comments on my second chapter and improved the
quality of the work immensely.
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I give mauruuru roa (large thanks) to Jimmy O’Donnell, Shelby Boyer, Emily
Vuxton, and Crystal Hartman. These students invested long hours in collecting both my,
and their own data, and contributed to our collective understanding of the system. I also
gained invaluable insight into the experience of advising through the process of
mentoring their senior honors theses and I will always be grateful they chose to work
with me. Shelby, in particular, was an exceptional research assistant (and dear friend)
through several field seasons and nearly a year in the field (collectively). She was hard
working, independent, honest, and caring, and I really appreciate her countless hours of
effort and, especially, her big smile at the end of every long day.
My roommates at Gump for many years, Nichole Price and Jennifer Lape, were
my dearest friends in Moorea and I will always love and cherish them for their
unconditional support. Erica Spotswood and David Hembry filled their void when they
graduated and moved to greener pastures, and I really appreciate our wonderful nights
on the hill. The other graduate students working at Gump contributed to my
development, as a scientist and as a person, in countless ways: Tom Adam, Gerick
Bergsma, Carol Chaffee, Adrien Delval, Anne Duplouy, Robin Elahi, Shane Geange,
Danny Green, Will Goldenheim, Nick Haring, Rebecca Habeeb, Emily Hornett, Joshua
Idjadi, Jenny Kahn, Kate (Hansen) Karaköylü, Maireid Maheighn, Nancy Muehllehner,
Jennie Oates, Abigail Poray, Hollie Putnam, Alice Rogers, Melissa Spitler, Hannah
Stewart, Adrian Stier, Stephanie Talmage, and Annie Yau. As did our regular visitors
from the R.V. Braveheart (they know who they are!). And, of course, my own graduate
student mentors from UCSB, Katie Arkema, Sarah Lester, Scott Hamilton, Ben
Ruttenberg, Andrew Rassweiler, Jamael Samhouri, Jeff Shima, Rick Wilder, Will White,
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and, especially, Andrew Thompson, who showed me the way through their good work
and offered support and encouragment, both prior to, and throughout my graduate
studies. I will always cherish the memories and I look forward to creating more at WSN,
ESA, and ICRS, or elsewhere in the Pacific!
Folks that cycled in and out of Gump sporadically were also instrumental,
especially the following, who volunteered countless hours and helped collect the data
that I needed: Dieldrich Bermudez, Lindsey Carr, Joseph Chipperfield, Sarah Gravem,
Amanda Roe, Melissa Schmitt, Will van Stippen, Michael Way, and, especially, Wesley
Davis. The East-West course, and the other courses that came through (UCLA and
Berkeley in particular) also offered many helping hands, diving buddies, fun distractions
(fish prints!), and fantastic role models (Rick Vance, Peggy Fong, Mark Steele, and
Claire Wormald, in particular), for which I am extremely grateful.
Other folks were part of the Gump family and offered wonderful support through
the years in many different ways. I offer my sincere mauruuru roa to the station Director,
Neil Davies, Managers, Hinano and Frank Murphy (and their nehenehe family: Teheire,
Tangaroa, Terava, Kohina, and Temakahu), and the amazing Gump staff: Valentine
Brotherson, Tony You-Sing, Irma and Jacques You-Sing, and all of the wonderful
nehenehe Gump children, especially, Melissa Schmitt, for always keeping the Gump
family spirit alive and smiling.
My undergraduate mentors, Russell Schmitt and Sally Holbrook, and the rest of
the LTER professors, offered a supportive and academically stimulating environment
throughout my graduate career. Of these, Andrew Brooks, Peter Edmunds, Ruth Gates,
and Hunter Lenihan (as well as his beautiful family: Olivette, Rea, Loana, and the rest of
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the extended family), were particularly instrumental in my development as a scientist
(and as a lover Tahitian food and dance, respectively). The LTER research technicians
Keith Seydel, Michael Murray, and Vincent Moriarty, were diving savvy, knowledgeable
about all things technical, and perhaps most importantly, they contributed to the fun!
Leslie and the rest of the McIlroy family (Tiare, Matt Jean, Prinz, Douglas, Ioane,
Moava, and Manukura) were my second family. They offered me shelter, food, love, and
affection (and, of course, fine instruments, keen problem-solving minds, and power
tools). Without their open house and hearts, I could not have stretched my research
funds and completed the magnitude of work undertaken. I only hope I can offer the
same support to them one day.
My experiences with C.R.I.O.B.E. and the University of Perpignan rounded my
scientific and cultural experiences in French Polynesia. In particular, René Galzin,
Serge Planes, Thierry Lison de Loma, and Yannick Chancerelle challenged me to think
(and speak) like the French! They also offered me amazing opportunities for personal
and professional growth through expeditions to France, the Marquesas, and the South
Tuamotus, for which I am extremely grateful, and I look forward to continuing our
productive collaboration as we publish the data we collected together. The CRIOBE
staff and graduate students were the most friendly and supportive folks imaginable and
offered the familial environment I missed, just as Gump was expanding at record
speeds. While, my French exchange companion, Adrien Delval (or mon petite monkey)
challenged me culturally in countless other ways and, through it all, was a wonderful
friend.
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Last, but certainly not least, my wonderful friends and colleagues at the University
of Florida provided a supportive and nurturing home for me, both during and between
my long trips abroad, for which I will always be grateful. My chosen family here spoiled
me rotten the first six year (Lisa, Donovan, Marina, James, Skye, D, Deena, Trace,
Trav, Thea, Brandon, Lisa K., Francois, Adrien, Mary, Andy, Shane, Ellie, and the rest
of the crew) and I ached for their companionship in the final year, after they had moved
to greener pastures. Luckily, I found Fay Ray, and fun friends old and new inspired me
in new directions and kept the fire of adventure and discovery alive. This offered a
wonderful reprieve from the norm of pretending to be locked in the Ivory Tower (like
Rapunzel!), writing my dissertation at an accelerated pace. All in all, the Department of
Biology was the ideal place for my graduate study and, although the years flew by, they
will never be forgotten.
Methods to remove Stegastes nigricans were approved by the University of Florida
(U.F.) Institutional Animal Care and Use Committee (Approval #: E-109: June 2005 –
July 2008). I gratefully acknowledge research funding from the following sources: NSF
Graduate Research Fellowship; U.F. Alumni Fellowship; French-American Cultural
Exchange Ocean Bridges Program; U.F.-Howard Hughes Medical Institute Group
Advantaged Training Of Research (G.A.T.O.R.) Mentorship Graduate Fellowship
Program; International Society for Reef Studies / The Ocean Conservancy Graduate
Fellowship in Coral Ecosystem Research; U.C. Berkeley’s Gump Station Pearl
Internship; and grants from the American Museum of Natural History’s Lerner-Gray
Fund for Marine Research; the American Society of Ichthyologists and Herpetologists
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Raney Fund; and ProjectAWARE (all to JSW), in addition to base funds from NSF
(OCE-0242312, to C.W. Osenberg, B.M. Bolker, C.M. St. Mary, and J.S. Shima).
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TABLE OF CONTENTS page
ACKNOWLEDGMENTS .................................................................................................. 4
LIST OF TABLES .......................................................................................................... 15
LIST OF FIGURES ........................................................................................................ 18
LIST OF OBJECTS ....................................................................................................... 20
LIST OF ABBREVIATIONS ........................................................................................... 21
CHAPTER
1 INTRODUCTION .................................................................................................... 24
Farmerfish as Ecosystem Engineers ...................................................................... 25 Study System .......................................................................................................... 28 Research Goals and Approach ............................................................................... 29
2 INDIRECT EFFECTS OF A KEY ECOSYSTEM ENGINEER ALTER SURVIVAL AND GROWTH OF FOUNDATION CORAL SPECIES........................................... 31
Introduction ............................................................................................................. 31 Methods .................................................................................................................. 33
Study System ................................................................................................... 33 Experimental Reefs .......................................................................................... 36 Farmerfish and Algal Removal Manipulations .................................................. 37 Coral Transplants and Caging Sub-Treatments ............................................... 37 Fish Surveys and Reef Composition ................................................................ 38 Termination of experiment ................................................................................ 39 Statistical Analyses .......................................................................................... 39
Results .................................................................................................................... 41 Treatment Efficacy ........................................................................................... 41
Fish removals ............................................................................................. 41 Turf removals ............................................................................................. 42
Field Surveys .................................................................................................... 42 Chase frequency ........................................................................................ 42 Density ....................................................................................................... 43 Microhabitat use ......................................................................................... 43 Foraging frequency .................................................................................... 43 Changes in reef composition ...................................................................... 44
Experimental Responses.................................................................................. 45 Frequency of predation .............................................................................. 45 Temporal change in coral mass ................................................................. 45 Frequency of algal overgrowth ................................................................... 46
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Discussion .............................................................................................................. 47 Conclusions and Implications ................................................................................. 51
3 INDIRECT EFFECTS OF STEGASTES NIGRICANS ON MASSIVE PORITES CORAL AND IMPLICATIONS FOR OTHER COMMUNITY MEMBERS ................. 56
Introduction ............................................................................................................. 56 Methods .................................................................................................................. 59
Paired Field Surveys ........................................................................................ 59 Transition Zone Field Experiment ..................................................................... 59
Treatment implementation ......................................................................... 60 Digital photographic analyses .................................................................... 61
Statistical Analyses .......................................................................................... 62 Paired field surveys .................................................................................... 62 Transition zone experiment ........................................................................ 62
Results .................................................................................................................... 63 Observational Results: Paired Surveys ............................................................ 63 Experimental Results: Porites-Turf Transition Zone ......................................... 63
Discussion .............................................................................................................. 64 Conclusions and Future Directions ......................................................................... 66
4 EFFECTS OF FARMERFISH AND CORAL PREDATORS ON THE POPULATION DYNAMICS OF BRANCHING CORALS IN A DISTURBED LAGOON SYSTEM ................................................................................................. 75
Introduction ............................................................................................................. 75 Evidence Farmerfish Engineer the Coral Community ....................................... 76 Diverse Life History Strategies ......................................................................... 77 Demographic Complexity ................................................................................. 78 Scaling Up ........................................................................................................ 79
Methods .................................................................................................................. 81 Study System ................................................................................................... 81 Experimental Reefs .......................................................................................... 82 Demographic Monitoring .................................................................................. 83 Life Table Response Experiment ..................................................................... 84 Statistical Analyses .......................................................................................... 84
Reef attributes ............................................................................................ 85 Mortality ..................................................................................................... 85 Change in size of corals ............................................................................. 87
Matrix Models ................................................................................................... 88 Recruitment and Fragmentation ....................................................................... 88
Results .................................................................................................................... 89 Life Table Response Experiment ..................................................................... 89
Acropora mortality ...................................................................................... 89 Pocillopora mortality ................................................................................... 90 Fragmentation ............................................................................................ 91 Change in coral size .................................................................................. 92
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Experimental change in Acropora size ....................................................... 92 Experimental change in Pocillopora size ................................................... 93
Matrix Models ................................................................................................... 94 Recruitment Patterns ........................................................................................ 94
Discussion .............................................................................................................. 94 Observed Community Response ...................................................................... 95 Differential Susceptibility to Predation .............................................................. 96 Recruitment Failure .......................................................................................... 99 Conclusions .................................................................................................... 100
5 CONCLUSIONS ................................................................................................... 112
Variable Outcomes of Farming Behaviors ............................................................ 113 Farmerfish Effect Varies with Community Structure ............................................. 114 Expanding the Grazing Continuum ....................................................................... 115 Evidence Based Upon Research in Moorea ......................................................... 117
APPENDIX
A SAMPLING METHODS AND RESULTS CONCERNING EXPERIMENTAL REEF CHARACTERISTICS PRIOR TO AND AFTER MANIPULATIONS ............ 124
Methods ................................................................................................................ 124 Results .................................................................................................................. 124
B TABLES AND FIGURES SUPPORTING THE EFFICACY OF REMOVAL TREATMENTS ..................................................................................................... 133
C EXPERIMENTAL METHODS, DETAILS, AND RESULTS FOR DAILY CHANGE IN CORAL MASS .................................................................................................. 140
Methods ................................................................................................................ 140 Results .................................................................................................................. 140
D RESULTS OF FULL MODELS TESTING THE FREQUENCY OF PREDATION AND OVERGROWTH ........................................................................................... 144
E RESULTS OF FULL MODELS TESTING THE TERRITORIAL EFFORT EXPENDED BY STEGASTES NIGRICANS AND RESPONSES BY IMPORTANT MOBILE FISHES (DENSITY, FORAGING, REEF USE) ................. 148
F DETAILED METHODOLOGY FOR LAB AND FIELD OBSERVATIONS OF COMPETITION BETWEEN PORITES AND ALGAL TURF .................................. 157
G EXPERIMENTAL REEFS BEFORE AND AFTER FARMERFISH REMOVALS ... 163
H POPULATION MEASURES FOR ACROPORA AND POCILLOPORA IN THE PRESENCE AND REMOVAL OF FARMERFISH ................................................. 173
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I TRANSITION MATRICES FOR ACROPORA AND POCILLOPORA IN THE PRESENCE AND REMOVAL OF FARMERFISH ................................................. 184
LIST OF REFERENCES ............................................................................................. 191
BIOGRAPHICAL SKETCH .......................................................................................... 206
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LIST OF TABLES
Table page 3-1 Transition-zone Experimental Treatments .......................................................... 68
4-1 General susceptibility of Acropora, Pocillopora, and Porites to natural disturbances. .................................................................................................... 101
4-2 Overall mortality patterns for all sizes of Acropora. .......................................... 102
4-3 Overall mortality patterns for all sizes of Pocillopora. ....................................... 103
4-4 Record of fragmentation of corals by period and treatment .............................. 104
4-5 Record of coral recruitment to reefs by period and treatment ........................... 105
4-6 Overall λ values for Pocillopora and Acropora. ................................................. 106
5-1 Summary of differences between foraging and farming coral reef fishes. ........ 122
A-1 Physical factors of all reefs before manipulations (GLM) .................................. 124
A-2 Composition of Stegastes Reefs before removals (GLM) ................................. 125
A-3 Comparisons of Stegastes and Porites reefs before removals (t-tests) ............ 126
A-4 Composition of Stegastes Reefs after removals (GLM) .................................... 127
B-1 Density of adult Stegastes nigricans (GLMM)................................................... 133
B-2 Contrasts for density of adult Stegastes nigricans (GLMM) .............................. 134
B-3 Density of adult Stegastes nigricans before removals (Χ2). .............................. 135
B-4 Density of adult Stegastes nigricans after removals (Χ2). ................................. 136
B-5 Mean mass of dried algal turf (GLM) ................................................................ 137
C-1 Daily coral growth (GLM) .................................................................................. 140
C-2 Tests of growth effect slices for each coral species (GLM). ............................. 141
C-3 Daily growth of caged individuals (GLM) .......................................................... 142
D-1 Predation frequency (Logisitic Regression). ..................................................... 144
D-2 Frequency of algal overgrowth (Logistic Regression) ....................................... 145
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D-3 Turf abundance and coral overgrowth (Linear Regression) .............................. 146
E-1 Chase frequency (GLMM) ................................................................................ 148
E-2 Contrasts of chase frequency (GLMM) ............................................................. 149
E-3 List of species documented for each target fish family ..................................... 150
E-4 Densities of target families of coral reef fishes (GLMM) ................................... 151
E-5 Contrasts of densities of target families of coral reef fishes (GLMM) ................ 152
E-6 Reef use by target families of coral reef fishes (GLMM) ................................... 153
E-7 Contrasts of reef use by target families of coral reef fishes (GLMM) ................ 154
E-8 Foraging frequency of target families of coral reef fishes (GLMM) ................... 155
E-9 Contrasts of foraging frequency of target families of reef fishes (GLMM) ......... 156
F-1 Test of average change in live Porites (LMM) .................................................. 157
F-2 Contrasts for change in live Porites (LMM) ....................................................... 158
F-3 Test of average change in bleaching front (LMM) ............................................ 159
G-1 Experimental reef characters BEFORE manipulations. .................................... 163
G-2 Differences in the average size of experimental reefs (LM) .............................. 164
G-3 Reef size model estimates (LM). ...................................................................... 165
G-4 Average density of Stegastes nigricans before removals (LMM). ..................... 166
G-5 Stegastes nigricans density estimates before removals (LMM) ........................ 167
G-6 Average density of Stegastes nigricans after removals (LMM) ......................... 168
G-7 Stegastes nigricans density estimates after removals (LMM) ........................... 169
H-1 Mortality frequency for Acropora & Pocillopora (GLMM, LRT). ......................... 173
H-2 Mortality frequency model estimates (GLMM). ................................................. 174
H-3 Follow-up mortality analyses for Acropora (GLMM, LRT) ................................. 175
H-4 Follow-up mortality analyses for Pocillopora (GLMM, LRT) .............................. 176
H-5 Differences in final size of Acropora and Pocillopora (LMM). ........................... 177
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H-6 Follow-up change in size analyses for Acropora (LMM) ................................... 178
H-7 Follow-up change in size analyses for Pocillopora (LMM) ................................ 179
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LIST OF FIGURES
Figure page 2-1 Mean frequency of coral predation ..................................................................... 53
2-2 Frequency of coral overgrowth ........................................................................... 54
2-3 Mean density, reef use, and foraging frequency of target fish families. .............. 55
3-1 Representative photos of reefs by type .............................................................. 69
3-2 Simplified schematic of transition zone quadrat design ...................................... 70
3-3 Paired reef surveys: Mean number and size of Stegastes nigricans. ................. 71
3-4 Paired reef surveys: Mean percent cover live massive Porites and algal turf ..... 72
3-5 Mean linear change in live massive coral tissue by treatment ............................ 73
3-6 Mean linear change in the amount of dead Porites tissue .................................. 74
4-1 Mortality rates of Acropora ............................................................................... 107
4-2 Mortality rates of Pocillopora ............................................................................ 108
4-3 Change in size (Delta) of Acropora as a function of previous maximum linear length ................................................................................................................ 109
4-4 Change in size (Delta) of Pocillopora as a function of previous maximum linear length ...................................................................................................... 110
4-5 Mean population decay rate of Acropora and Pocillopora (λ) ........................... 111
5-1 Schematic of Stegastes nigricans direct and indirect interactions .................... 123
A-1 Design schematic ............................................................................................. 128
A-2 Photographic example of experimental reefs ................................................... 129
A-3 Photographic example of experimental coral nubbins ...................................... 130
A-4 Mean reef composition before removals ........................................................... 131
A-5 Mean reef composition after removals .............................................................. 132
B-1 Mean number of adult Stegastes nigricans ...................................................... 138
B-2 Mean mass of dried algal turf ........................................................................... 139
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C-1 Mean daily coral growth rates ........................................................................... 143
D-1 Frequency of algal overgrowth for Pocillopora verrucosa ................................. 147
F-1 Paired reef surveys: Reef Size ......................................................................... 160
F-2 Example photo quadrats from a sample experimental reef .............................. 161
F-3 Schematic of line measurements for transition zone experiment...................... 162
G-1 Mean size of experimental reefs ....................................................................... 170
G-2 Mean density of Stegastes nigricans before removals ..................................... 171
G-3 Mean density of Stegastes nigricans at the termination of the experiment ....... 172
H-1 Raw mortality values for Acropora .................................................................... 180
H-2 Raw mortality values for Pocillopora ................................................................. 181
H-3 Representative photos of Acropora predation before and after removals of Stegastes nigricans. ......................................................................................... 182
H-4 Representative photos of Pocillopora predation before and after removals of Stegastes nigricans. ......................................................................................... 183
I-1 Schematic of size classes and types of transitions for Acropora and Pocillopora. ....................................................................................................... 184
I-2 Size structure transition matrix for Acropora on all reefs prior to experimental manipulations ................................................................................................... 185
I-3 Size structure transition matrix for Acropora following application of clove oil to experimental CONTROL reefs. ........................................................................ 186
I-4 Size structure transition matrix for Acropora following application of clove oil and removal of farmerfish. ................................................................................ 187
I-5 Size structure transition matrix for Pocillopora on all reefs prior to experimental manipulations. ............................................................................. 188
I-6 Size structure transition matrix for Pocillopora following application of clove oil to experimental CONTROL reefs. .................................................................... 189
I-7 Size structure transition matrix for Pocillopora following application of clove oil and removal of farmerfish. ........................................................................... 190
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LIST OF OBJECTS
Object page 3-1 Video of vermetid feeding (28.9 MB .avi) ............................................................ 64
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LIST OF ABBREVIATIONS
GBR Great Barrier Reef
GLMM Generalized Linear Mixed Model
LM Linear Model
LLM Linear Mixed Model
LRT Likelihood Ratio Test
PNG Papua New Guinea
Χ2 Chi Square Test Statistic
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Abstract of Dissertation Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Doctor of Philosophy
INDIRECT EFFECTS OF A MARINE ECOSYSTEM ENGINEER ALTER THE
ABUNDANCE AND DISTRIBUTION OF FOUNDATION CORAL SPECIES
By
Jada-Simone Shanti White
May 2010
Chair: Benjamin M. Bolker Cochair: Gustav Paulay Major: Zoology
Farmerfish engineer coral communities by facilitating algal turf and exerting
resource control through territorial defense: Within territories, these behaviors indirectly
(1) increase interactions between coral and farmed turf and (2) decrease interactions
with mobile grazers. A small-scale experiment indicated massive Porites were more
vulnerable to competition with turf, than were branching Acropora, encrusting
Montipora, or lobed Pocillopora. In contrast, the more delicate acroporids (Acropora and
Montipora), were more vulnerable to predation by mobile corallivores and grew and
survived better in the presence of S. nigricans defense. I used a more realistic
manipulation of turf, sediment, and sediment-consuming vermetid snails to document
the rate of massive Porites overgrowth by S. nigricans-associated turf. I addressed the
indirect effects of territoriality in a demographic context using size specific population
monitoring of two of the four genera, Acropora and Pocillopora, in the presence and
removal of S. nigricans. It appears the disturbance history has played a pivotal role in
the types of community changes observed: While S. nigricans usually colonizes
Acropora thickets, a series of disturbances virtually eliminated these habitats and
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farmerfish are found colonizing the dominant disturbance tolerant, but turf sensitive,
massive Porites. Taxa with a higher resistance to competition with turf can utilize dead
portions of these massive corals. This increase in substrate availability, when coupled
with lower mortality rates, has led to enhanced recovery of branching corals within
farmerfish territories. Corymbose Acropora are relegated to high flow, or cracks and
crevices, outside S. nigricans territories, suggesting grazing pressure is constraining
recovery in the absence of this ecosystem engineer. Pocillopora also enjoys lower
mortality inside S. nigricans territories, though susceptibility to losses by corallivorous
fishes was lower than those attributed to a periodic outbreak of the crown-o-thorn
seastar, Acanthaster planci. This system supports the idea that disturbance can alter
the engineering role: S. nigricans adversely affects branching Acropora in relatively
undisturbed habitats, but can offer a less stressful environment if predation pressure by
corallivores is high. These results suggest that corallivory may sometimes function as
an important regulatory process of coral community structure and warrants additional
research. In particular, whether the observed high predation rates are driven by
changes in top-down (e.g., trophic cascades induced by anthropogenic removal of top
predators), or bottom-up processes (e.g., changes in grazing pressure due to alterations
in coral and algal community structure following natural disturbances).
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CHAPTER 1 INTRODUCTION
Our understanding of what factors are driving the community structure of complex
systems, such as coral reefs, is often compromised by an inability to test factors
constraining the distribution of multiple taxa at relevant scales. Frequent disturbance
regimes (e.g., cyclones, bleaching events) prevent competitive exclusion and contribute
to the maintenance of high diversity on coral reefs (Connell 1978). These complex
communities are often considered to be non-equilibrium systems (Connell 1978) with
species abundance constrained by recruitment limitation (i.e., whether larvae can arrive,
Doherty 1981) and a competitive lottery (i.e., the first to arrive at a new habitat patch is
expected to have an advantage, Sale 1977, 1982). In these stochastic environments,
long-lived individuals have a greater potential to ‘store’ reproductive potential via
recruitment storage effects (Warner and Chesson 1985). Nonetheless, top down
processes can alter community composition, and herbivores, in particular, play a role in
mediating competition between fast-growing algae and slow-growing coral (Huston
1985; Sluka and Miller 2001). The foraging rate of herbivores creates a gradient of
competition between coral and algae from intense (e.g., in the absence of herbivory
following Diadema die-offs in overfished parts of the Caribbean and resulting coral
declines, e.g., Lessios et al. 1984) to absent (e.g., when grazing pressure is high
enough that there is little contact between filamentous or macroalgae and corals). As
predicted by theory (Connell 1978), the highest algal diversity has been reported at
intermediate foraging rates, because lower standing algal biomass reduces competition
for limited resources (Sammarco 1983; Hixon and Brostoff 1983,1996; Huston 1985).
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The likelihood for a community to be tightly linked, in which a change in the
abundance of one species affects others in a predictable way, is higher when a
keystone species (Paine 1969; Mills et al. 1993; Power et al. 1996) or ecosystem
engineer (Jones et al. 1994, 1997) is operating. Those species that create a predictable
change in the environment due to non-trophic modifications (e.g., dam building by the
beaver, Castor canadensis, Wright et al. 2002) have been termed keystone modifiers
(Mills et al. 1993) or ecosystem engineers (Jones et al. 1994,1997). Indeed, indirect
effects are gaining acceptance as an important driver of key demographic processes
(e.g., recruitment, Webster and Almany 2002), as well as larger-scale community
change (e.g. Dulvy et al. 2004). In addition to biotic disturbances, such as competition
and predation, natural physical disturbances also remove or kill organisms and alter
resource availability (e.g., Sousa 1979a, 1979b). The high diversity and stochastic
disturbance regimes characteristic of coral reefs (Connell 1978; Hughes 1989) offer an
opportunity to explore how resource control by key engineers (Boogert et al. 2006)
changes when community composition is altered by larger-scale natural disturbances.
Farmerfish as Ecosystem Engineers
Territorial damselfish occupy defined areas that they actively defend from
competitors and egg predators (reviewed in Ceccarelli et al. 2001). Within this diverse
group, only territorial algal “farmerfish” influence the benthic structure of coral reefs.
These farmerfish develop and maintain conspicuous filamentous algal mats (hereafter,
turf) through a variety of behaviors, including: substrate preparation via killing coral
(e.g., Kaufmann 1977; Wellington 1982); “weeding” by selectively removing unpalatable
algae (e.g., Hata and Kato 2003, 2004); fertilization through defecation (e.g., Klumpp
and Polunin 1989; but see Lison de Loma et al. 2000, Hata and Kato 2002); and
26
reducing herbivory through active defense (e.g., Hixon and Brostoff 1981). Species of
damselfish that farm turf are more aggressive than non-farming congeners and
effectively alter the spatial distribution of other (non-farming) pomacentrids through
territorial defense (Robertson 1996). Farmerfish aggressively defend against urchins
(e.g., Sammarco and Williams 1982), large herbivorous and corallivorous fishes (e.g.,
Hixon and Brostoff 1981), and potential egg predators (e.g, Haley and Müller 2002),
thereby reducing resource availability for those species.
The direct effects of farmerfish “farming” on benthic algal community structure
have been well documented, with respect to increases in algal biomass (Hata et al.
2002; Hata and Nishihira 2002), diversity (Hixon and Brostoff 1983, 1996), and
productivity (Klumpp et al. 1987). Given high algal abundance within territories, it is not
surprising that previous research has documented farmed turf can overgrow hermatypic
corals and coral spat (Vine 1974; Potts 1977; Lobel 1980; Sammarco and Carleton
1981).
Territorial behavior by farmerfish toward other species serves to directly reduce
access to defended reefs (i.e., resource control) and can indirectly benefit species that
use territories without eliciting this response. These “territory residents” may be
indirectly afforded protection due to the reduced frequency and intensity of visits from
grazers (e.g., Hixon and Brostoff 1986), competitors (e.g., Williams 1980, 1981) or
predators, including corallivores (e.g., Wellington 1982; Glynn and Colgan 1988).
Several authors have documented increased recruitment (Sammarco and Carleton
1981; Gleason 1996) and survivorship of corals within farmerfish territories (Sammarco
and Williams 1982, Wellington 1982, Glynn and Colgan 1988, Gleason 1994), resulting
27
in higher coral abundance (Wellington 1982; Glynn and Colgan 1988; Done et al. 1991;
Gleason 1994, 1996; Suefuji and van Woesik 2001). The underlying mechanism
appears to be an indirect positive effect of territorial behavior creating a spatial refuge
from mortality due to foraging by grazing herbivorous and corallivorous fishes (Gleason
1996, Wellington 1982) and invertebrates (urchins: Sammarco and Williams 1981, Done
et al. 1991, Gleason 1996; crown-of-thorns starfish: Glynn and Colgan 1988).
Thus, within algal systems, farmerfish have been shown to maintain higher
diversity by maintaining intermediate levels of (herbivorous) disturbance (Hixon and
Brostoff 1983, 1996). With respect to corals, the evidence is more equivocal as
farmerfish interact indirectly with corals along two opposing axes of already existing
interaction chains. By reducing access of herbivores to territories, farmerfish facilitate
algal abundance and increase competitive interactions between algae and corals.
Simultaneously, the reduction of grazing pressure by herbivores and corallivores may
indirectly benefit corals within territories. Therefore, farmerfish may indirectly affect coral
in two ways: (1) increased competition with farmed algal turf; and (2) decreased
predation by corallivores or incidental predation by grazing herbivores. Given the
indirect nature of these interactions, the importance of one mechanism over the other
could vary with community structure (i.e., the relative abundance of macroalgae, corals,
or grazers).
Previous research on the influence of farmerfish on corals has relied upon the
spatially confounded approach of comparing territories with non-territories. This
approach, while strongly indicative of a trend, does not eliminate potential effects of
natural variation in corallivore abundance or other physical factors, such as flow
28
(Osenberg et al. 2006). In contrast, I experimentally manipulated farmerfish and/ or turf
abundance to test whether differences are due to indirect effects of competition with
algae or protection via territorial defense.
Study System
In Moorea, French Polynesia, farmerfish territories account for approximately 5 –
45% of the back-reef hard-bottom environment (Done et al. 1991, Gleason 1994). The
pattern of higher abundance of branching Acropora and Pocillopora coral abundance
within dusky farmerfish, Stegastes nigricans, territories was first documented by Glynn
and Colgan (1988) who hypothesized that farmerfish protect resident corals from the
corallivorous echinoderm, Acanthaster planci. Done et al. (1991) reported a higher
recovery of some branching and rare corals inside farmerfish territories after a series of
disturbances. Gleason (1996) documented higher recruitment rates of pocilloporid
corals inside territories in comparison to nearby grazed, as well as macroalgae
(Turbinaria ornata) dominated reefs. The proposed mechanism is an indirect effect of
territorial behavior that results in decreased predation within territories. Further, at least
some species of coral appear to be negatively impacted in farmerfish territories (Done
et al. 1991). Massive Porites species dominate Moorea backreef (lagoon) coral
assemblage and, Porites coral heads within territories have significantly lower coral
cover than those outside territories (Glynn and Colgan 1988). This suggests that direct
(e.g., killing coral) or indirect effects of farming turf (e.g., coral-algal competition) may
reduce the abundance of at least Porites within territories. Thus, the relative effects of
farmerfish on coral assemblages remain poorly understood (reviewed in Ceccarelli et al.
2001), and the net effect could be positive or negative, depending on coral species.
29
Research Goals and Approach
For my dissertation research I sought to understand what processes were driving
the observed coral community structure in farmerfish territories and to identify
vulnerable demographic stages. I utilized a combination of observational studies, small-
scale experiments, and a life table response experiment to evaluate the effects of this
key ecosystem engineer on the dominant coral genera within Moorean lagoons. I
conducted the first experimental test of the direct and indirect effects of a farmerfish on
the growth and mortality of four coral taxa: Acropora striata, Montipora flowerii,
Pocillopora verrucosa, and Porites australiensis (Chapter 2). In summer 2004 and
spring 2005, I conducted paired reef surveys within Vaipahu lagoon to establish the
current patterns of habitat and community within S. nigricans territories (Chapter 3).
During the spring 2007, I evaluated how turf, sediment, and vermetid snails affect the
rate of massive Porites overgrowth by algal turf (Chapter 3). I experimentally evaluated
coral recruitment on reefs with S. nigricans naturally present, experimentally removed,
or naturally absent (January 2006). I also began monitoring populations of branching
Acropora and Pocillopora, as well as massive Porites, on reefs with S. nigricans to
measure demographic parameters for these species in the presence of this farmerfish
(July 2006). Simultaneously, my undergraduate assistant, Shelby E. Boyer, conducted
an experiment on the effects of the fish anesthetic clove oil on growth and survival of
representatives for the three target coral genera (Boyer et al. 2009). This work was
instrumental in testing possible confounding effects and improved the methodology for
subsequent removals of S. nigricans in July 2007, for a life table response experiment
to test the effects of territoriality on Acropora and Pocillopora (Chapter 4). Finally, I
30
explore the ramifications of this, and related, work by placing the observed interactions
within a larger theoretical context (Chapter 5).
31
CHAPTER 2 INDIRECT EFFECTS OF A KEY ECOSYSTEM ENGINEER ALTER SURVIVAL AND
GROWTH OF FOUNDATION CORAL SPECIES
Introduction
Understanding how organisms modify communities via indirect interactions is
particularly essential for strongly interactive species, i.e., species whose absence (or
removal) leads to significant changes in their communities (Soulé et al. 2003). Effects of
such keystone species on communities, often mediated through trophic interactions, are
disproportionate to their abundance (Paine 1966). Ecosystem engineers create,
maintain, or modify the physical environment through behavioral control of resources
(e.g., beavers) and also include foundation species (e.g., trees) that provide substrate
or habitat for other species through their form (Jones et al. 1994, 1997). Like keystone
species, key engineers exert resource control that is disproportionate to their
abundance, but non-trophic in nature, thereby stimulating drastic changes in community
structure (Boogert et al. 2006). While ecologists have long used manipulative
experiments to identify and understand the effects of keystone species, many studies of
ecosystem engineers and foundation species have been observational (but see
Bertness and Leonard 1997; Crain and Bertness 2005; Spooner and Vaugn 2006, for
examples of empirical studies).
Farmerfish are territorial damselfish (Pomacentridae) that can alter vast
expanses of the benthos via a combination of farming behaviors and territorial defense
(reviewed in Ceccarelli et al. 2001): Farming behaviors include substrate preparation
(including killing coral), weeding unpalatable algae, and fertilization through defecation.
Territorial defense also reduces foraging rates by limiting access of fishes and
32
invertebrates (Ceccarelli et al. 2001). Community change can be widespread and
profound, and include altering the depth zonation of corals (Panama: Wellington 1982)
and maximizing algal diversity (Hawaii: Hixon and Brostoff 1983, 1996).
The effects of farmerfish on algal communities are well documented: algal
abundance, productivity, and diversity are higher within territories (Ceccarelli et al.
2001). Algae are usually detrimental to coral health (Reviewed in McCook et al. 2001),
and early reports indicated that effects of farmerfish on coral were negative due to
enhanced algal overgrowth (Vine 1974, Potts 1977, Lobel 1980) and bioerosion (Risk
and Sammarco 1982). Some farmerfish bite polyps to expand their territories (Kaufman
1977). In addition, filamentous turf can trap sediment (Nugues and Robert 2003) or
indirectly promote harmful bacterial growth (Smith et al. 2006). However, other studies
have found higher coral abundance, recruitment or survival within territories, relative to
outside (Sammarco and Carleton 1981, Sammarco and Williams 1982, Glynn and
Colgan 1988, Done et al. 1991, Gleason 1994, Gleason 1996, Suefuji and van Woesik
2001). Thus, the impacts of farmerfish on algal turf are well-documented and positive,
but effects on coral are understudied and contradictory (Ceccarelli et al. 2001, see also
Jones et al. 2006).
Using patch reefs in Moorea, I transplanted corals and manipulated the presence
of turf and S. nigricans to investigate the direct effects of this farmerfish on turf
abundance and reef use by common herbivorous and corallivorous fishes, as well as
the indirect effects on growth and survival of four species of coral (Acropora striata,
Montipora floweri, Pocillopora verrucosa, and Porites cf. australiensis). Specifically, I
tested the following hypotheses:
33
• H1) Stegastes nigricans directly decrease coral survival and growth through predation.
• H2) Stegastes nigricans indirectly decrease coral survival and growth through increased competition with algae.
• H2A) Territorial defense by Stegastes nigricans decreases herbivore access.
• H2B) Decreased herbivore access increases algal turf abundance.
• H2C) Abundant turf decreases coral survival via overgrowth.
• H2D) Overgrowth by turf decreases coral growth.
• H3) Stegastes nigricans indirectly increase coral survival and growth, through decreased predation by other fish
• H3A) Territorial defense by Stegastes nigricans decreases corallivore access.
• H3B) Decreased corallivore access decreases coral predation.
• H3C) Lower predation allows higher coral growth.
• H4) Susceptibility to these direct and indirect effects will vary among coral
species, due to variation in life history traits.
Methods
Study System
My study was conducted June – July 2005 within the northeastern lagoon of
Moorea, French Polynesia (S 17º28’525-645, W 149º47’335-535). Moorea is
surrounded by shallow (usually 1-6 m deep) lagoons stretching 0.2 – 1.5 km offshore to
a barrier reef (Galzin and Pointier 1985). Within the back reef, the lagoon floor is a
mosaic of patch reefs and open substrate (e.g., sand, rubble, or pavement) with patch
reefs increasing in abundance and coalescing toward the reef crest. Due to a series of
disturbances in the 1980s (Done et al. 1991; Adjeroud et al. 2005), the underlying
structure of these patch reefs is primarily formed by disturbance-tolerant Porites corals
34
(primarily P. australiensis, P. lobata, and P. rus) (Berumen and Pratchett 2006). Prior to
these disturbances the lagoon was dominated by massive Porites, followed closely by
branching Acropora, with low cover of Montipora and Pocillopora (Bouchon 1985).
Berumen and Pratchett (2006) report that coral cover in the back reef of Moorea has
returned to previous levels, however, there has been a notable change in community
structure: Porites still dominate the reef flat, however, Pocillopora have increased
significantly in cover, relative to pre-disturbance levels, while Acropora and Montipora
have failed to recover except within Stegastes territories (Done et al. 1991, Mapstone et
al. 2007) and in areas with high flow (e.g., near the reef crest, White et al., unpubl.
data).
Branching corals (Acropora, Montipora and Pocillopora) are more susceptible to
periodic, large-scale, disturbances (e.g., storm damage, bleaching, crown-of-thorns
starfish outbreaks) relative to massive Porites (Bouchon 1985, Hughes et al. 1989,
Gleason 1993, Adjeroud et al. 2005, Berumen and Pratchett 2006, McClanahan et al.
2007). Branching corals are also more affected by small-scale perturbations, such as
corallivory by other echinoderms (e.g., sea urchins: Suefuji and van Woesik 2001;
pincushion stars: Rotjan and Lewis 2008) and fishes (e.g., Wellington et al. 1982, this
study), but they tend to grow rapidly relative to massive corals (Huston 1985) and are
generally considered better space competitors (Connell 1978). Given the high frequency
of disturbance, Porites continue to dominate the lagoons, despite their relatively slow
growth rates (Berumen and Pratchett 2006) and lower live coral within abundant Dusky
farmerfish (Stegastes nigricans) territories (Done et al. 1991, Chapter 3). When portions
35
of these massive corals die they provide substrate for other sessile organisms, such as
crustose coralline algae, algal turf, macroalgae, and other corals.
All four genera of coral tested are known to incur predation by coral reef fishes
(Reviewed by Rotjan and Lewis 2008). However, corallivorous fishes show distinct
preferences for Acropora and Pocillopora in the Indo-Pacific, while Montastrea and
Porites are the major prey species for corallivores in the Caribbean, due in part to
differences in abundances between the two regions (Reviewed in Cole et al. 2008). In
the eastern Pacific, benthic grazers with specialized dentition can ingest large portions
of coral skeleton (e.g pufferfish (Tetradontidae), large triggerfishes (Balistidae), and
parrotfish (Scaridae)), often preferring growing tips (Cole et al. 2008). Indeed, pufferfish
and parrotfishes reduced growth and survival of juvenile branching corals (Pocillopora)
through heavy grazing in Panama (Wellington 1982). In Moorea, pufferfish are in lower
abundance but the guineafowl puffer (Arothron meleagris) is observed to bite off large
chunks of branching corals (especially Acropora spp.): In contrast, relatively infrequent
observations of foraging on abundant massive corals (e.g., Porites australiensis) by A.
meleagris indicated damage is restricted to only the concave surfaces (White, pers.
obs.), and reinforces that differences in predator preference, skeleton morphology, and
skeletal density can alter susceptibility to predation.
In Moorea, highly aggressive Stegastes nigricans communally defend large
territories ranging from small isolated patch reefs with ~3 adults per m2 (this study) to
very large continuous territories several meters wide (Done et al. 1991). Communal
defense yields lush 1.0 – 3.0 cm long algal “turf” of fine rhodophytes composed mostly
of Polysiphonia spp. (Hata and Kato 2006). In this system, S. nigricans most commonly
36
colonizes dead portions of the dominant massive coral, Porites (Done et al. 1991), but
also inhabits all of the few remaining thickets of staghorn Acropora with a larger
congeneric farmerfish, S. lividus, at densities up to 30 damselfish (on average) per 5 m
(Mapstone et al. 2007). On average, the abundance of farmerfish, and the extent of
territories, is higher in the fringing reef and lower in the back reef (Galzin et al. In
preparation).
Experimental Reefs
I selected 32 Porites patch reefs colonized by S. nigricans within the back reef of
Aroa Lagoon. Using a 2 x 2 factorial field design, I removed S. nigricans and / or turf
algae prior to introducing coral transplants. As a positive control, I also transplanted
coral fragments to 8 (un-colonized) Porites reefs (naturally devoid of S. nigricans and
turf) that were interspersed among experimental reefs. This yielded a total of five
treatments (n=8 for all): (1) Stegastes present, Turf present, (2) Stegastes present, Turf
(locally) removed , (3) Stegastes removed, Turf present , (4) Stegastes removed, Turf
(locally) removed , (5) Stegastes absent, Turf absent (control or ‘Porites reefs’) (Figure
2-1A; Photos in Appendix A: Figure A-2).
Reefs were chosen based on similarity in size (mean ± 95% CI: 4.2 ± 0.3 m2),
depth (1.9 ± 0.1 m), average (0.7 ± 0.1 m) and maximum (1.1 ± 0.2 m) reef height, and
relative isolation from other patch reefs (2.2 ± 0.7 m; Appendix A: Table A-1). Prior to
manipulations, the 32 ‘Stegastes reefs’ did not differ significantly in gross community
composition and were comprised of a mix of farmed algal turf (overlaying dead coral;
58.5 ± 3.2%), reduced live massive Porites (26.2 ± 5.0%), and other corals (Acropora,
Montipora, Pocillopora; 8.96 ± 0.93%; Appendix A: Figure A-4, Table A-2). The 8 control
reefs did not differ significantly from manipulated reefs in cover of macroalgae or
37
combined dead coral and crustose coralline algae; however, live Porites was
significantly more abundant (89.0 ± 5.9%), and turf (1.35 ± 2.64%) and branching corals
(0.50 ± 0.64%) were less common (Appendix A: Figure A-4, Table A-3).
Farmerfish and Algal Removal Manipulations
To test the hypotheses that S. nigricans reduces reef access for important
herbivores (H2A) and corallivores (H3A), I removed S. nigricans prior to the experiment
using microspears and the fish anesthetic clove oil (Eugenol, City Chemicals, USA).
Because clove oil can increase coral bleaching and reduce growth (Boyer et al. 2009),
S. nigricans removal treatments were not maintained, although densities remained low,
likely due to isolation of the reefs. To test the hypothesis that turf decreases coral
survival (H2C) and growth (H2D), I removed turf with steel brushes until bare (dead) coral
substrate was exposed. I removed turf from twelve, 15cm x 15cm, similar patches
distributed around the reef (random sites for coral transplants), rather than removing all
turf from a given reef due to the large size of patch reefs and S. nigricans’
interdependence with turf. Throughout the experiment, I ensured there was no direct
contact between coral transplants and turf in removal treatments by scrubbing nubbin
bases with stiff plastic brushes every five days; however, the rest of the reef maintained
typical turf abundances.
Coral Transplants and Caging Sub-Treatments
To tease apart predation by S. nigricans (H1), versus transient corallivores (H3B),
I transplanted three coral transplants (hereafter, nubbins) of each species, with random
assignment to varying levels of protection (cage, control, and open) to each reef (Figure
2-1B). For each species tested (A. striata, M. floweri, P. verrucosa, and P. australiensis)
I collected 40, approximately thumb-sized, nubbins from three separate genets (large
38
colonies) to include, but not explicitly test, genetic variation (yielding 120 nubbins).
Nubbins were transported to the lab, mounted on Vexar (plastic mesh) using Z-spar™
compound (Splash-zone A788, Kopcoat, Pittsburgh, Pennsylvania, USA),
photographed, and weighed using the buoyant mass technique (Davies 1989). For each
species, I randomly assigned one nubbin (from a randomly selected genet) to a sub-
treatment (cage, control, or open), yielding 12 nubbins transplanted to each of the 40
experimental reefs (480 nubbins total). For the ‘turf removal’ treatments, I outplanted
nubbins to the middle of the scrubbed patch to avoid contact with turf. I constructed
cages and cage controls from Vexar with a mesh size of 3cm to reduce effects on flow
and light while still offering protection from most adult fishes, including S. nigricans.
Cages consisted of four sides and a top connected with plastic cable-ties, while cage
controls lacked two (opposite) sides to allow access while controlling for the effects of
reduced light or flow (Photos in Appendix A: Figure A-3). Cages and cage controls were
cleaned every 5 days throughout the experiment.
Fish Surveys and Reef Composition
To document whether reef use by other fishes varies with S. nigricans presence,
removal, and absence (H2A and H3A), one diver (JSW) conducted 5 min counts of fishes
occurring within 1 m of each experimental reef beginning 10 d before experimental
implementation and continuing every 5 days until the termination of the experiment 32
days later. Species identity, microhabitat used (e.g., sand, water column, turf, coral,
dead coral, etc.), and (binary) foraging status of each fish was recorded.
Simultaneously, the second diver (JOD) counted chases from S. nigricans and noted
the species chased. To test whether herbivore access alters turf abundance at the reef
39
scale (H2B), I re-assessed reef composition at the end of the experiment (see Appendix
A: Methods).
Termination of experiment
I collected and re-photographed 479 nubbins (1/480 was lost) 32 days after deployment.
To test whether corallivores increase coral mortality (H3B), photos were scored blindly
(without knowledge of treatment origin) using binary designations (present=1, absent=0)
for evidence of destructive predation (i.e., CaCO3 skeleton removed). Simultaneously,
to test whether turf increases coral mortality (H2C), photos were scored (1) if nubbins
were partially or fully overgrown by turf. After photographing, I removed sediment from
the base of the nubbin using a seawater squirt bottle and scraped all turf into a separate
beaker. To test whether herbivore access alters turf abundance at the nubbin scale
(H2B), I filtered the turf onto Millipore glass fiber filters, dried for 24 hours at 70 ºC, and
weighed with an analytical balance. After removing turf, I scrubbed off all remaining
encrusting organisms and buoyantly re-weighed each nubbin to test the effects of turf
(H2D) and corallivory (H3C) on coral growth (see Appendix C).
Statistical Analyses
I used a general linear model to test whether reef characters (e.g., size, depth, isolation,
benthic composition) varied among Treatment groupings prior to manipulations (SAS
PROC GLM, Appendix A: Figure A-1). I tested the efficacy of S. nigricans removals by
comparing adult abundances among treatments throughout the duration of the
experiment using a generalized linear mixed model (GLMM) with a Poisson error
distribution and log link and degrees of freedom estimated using the Kenward-Roger
approximation (Reviewed in Bolker et al. 2009): Treatment and Period (Before versus
After) were used as fixed effects and Day as a random effect to account for the lack of
40
independence among observations through time (SAS PROC GLIMMIX, Appendix B:
Tables B-1 and B-2). For mean response variables calculated once, i.e., algal mass
(H2B, nubbin-scale) and change in daily mass of nubbins (H2D), I used a linear mixed
model to test the fixed factors of coral Species, Treatment, Sub-treatment (cage,
control, and open) and all two- and three-way interactions, with Reef as a random effect
(SAS PROC MIXED, Appendix B: Tables B-3 and Appendix C: Table C-1 and C-2,
respectively). I tested for Treatment effects on growth for caged individuals of each
species (H3C) using Reef as a random effect (SAS PROC MIXED, Appendix C: Table C-
3). I used the same analysis, to determine whether there was a difference in the arcsine
square root transformed reef composition (i.e., % turf, etc.) prior to the start, and at the
termination of, experimental manipulations (H2B, reef-scale) (Appendix A: Tables A-2, A-
3, and A-4). I used logistic regression to compare the frequency of predation (H3B) and
overgrowth (H2C) of corals in the presence and absence of S. nigricans and turf, and in
relation to sub-treatment (SAS PROC LOGISTIC, Appendix B: Tables B-3 and B-5).
Because there were no significant differences between open and cage control sub-
treatments in any analyses, data are pooled for graphical presentation (only). As a
follow-up, I used linear regression to test for a linear relationship between (arc-sine
square root transformed) overgrowth frequency and the average algal abundance
experienced by each treatment-reef combination (Appendix D: Table D-3). I calculated
differences in the frequency of territorial chases, reef use, and foraging for each family
(H2A, H3A) after experimental removals using GLMMs. I used Reef Type (Stegastes
nigricans present, removed, absent) as a fixed effect and Day as a random effect to
account for lack of temporal independence (SAS PROC GLIMMIX, Binomial error
41
distribution, logit link function, Appendix E: Tables E-3, E-4, and E-5). For the density of
fishes in a given family, I used the same model with a Poisson error distribution and log
link (Appendix E: Tables E-2); however, because overdispersion was present (the
average Pearson residuals were significantly > 1.0) I used a quasi-binomial model
(Bolker et al. 2009). When appropriate, I applied Tukey’s HSD test or contrasts to make
relevant comparisons. For all analyses, I evaluated whether I were using the
appropriate distribution (e.g., binomial, normal, or Poisson) for each model using Q-Q
plots and Pearson residuals. For normal-based tests, I also used Levene’s test for
equality of variances. All analyses were performed using SAS version 9.13 (SAS
Institute Inc., Cary, NC, USA). I report mean ± 95% confidence intervals (1.96*S.E.) for
all values parenthetically.
Results
Treatment Efficacy
Fish removals
Stegastes nigricans average daily abundance was nearly 7 times higher in
presence, than in removal treatments, throughout the experiment. Both main effects
(Treatment and Before-After period) were significant (Appendix B: Table B-1) and re-
colonization remained at low levels in the removal treatments. Very few adult S.
nigricans were sighted on control reefs either before (n=0) or after (n=1) experimental
removals took place (Day 0) and absent reefs were omitted from analyses (Appendix B:
Figure B-1). I used Chi square contingency analyses to compare abundances among
reefs colonized by S. nigricans, before and after removals: Prior to removals, S.
nigricans were distributed approximately equally across treatments; as expected, there
were significant differences among treatments following the pulse removals and ~88%
42
of all adult Stegastes were observed on ‘Stegastes presence’ reefs (Appendix B: Table
B-2).
Turf removals
At the end of the experiment, the manipulated turf environment (i.e., turf biomass
around the base of nubbins) differed significantly among treatments (ANOVA,
F4,418=128.45, P<0.0001) but not among coral species (P = 0.50), nor was there a
treatment x coral species interaction (P = 0.81). On average, algal biomass on nubbins
within S. nigricans territories was 4.5 times higher than on reefs from which I removed
turf and 2.6 times higher than outside territories, i.e., control (Porites) reefs. The smaller
difference in the latter case is driven by a cage effect: algal abundance was 1.8 to 2.2
times higher when nubbins were caged rather than exposed (control and open sub-
treatments) on all reefs in which turf was not manually removed (Treatment x Sub-
Treatment: ANOVA, F2,418=29.31, P<0.0001). Thus, our removals were effective, but
differences in grazing protection (i.e., S. nigricans presence and cages) resulted in more
than the three intended levels of turf (Appendix B: Figure B-2).
Field Surveys
Chase frequency
On average, I observed more fishes chased from reefs (e.g., butterflyfishes
(Chaetodontidae), parrotfishes (Scaridae), and surgeonfishes (Acanthuridae)) when S.
nigricans was present (11% ± 0.02%) than when removed (1% ± 0.01%) or naturally
absent (<0.01% ± 0.0008%) (GLMM, Wald F2,597=5.15, P<0.006; P vs. R: t597=-2.15,
P=0.03; P vs. A: t597=-2.62, P=0.009, Appendix E: Table E-1). The few S. nigricans that
re-colonized reefs were responsible for the chases observed on ‘removal reefs’; juvenile
43
S. nigricans, which occupy an array of habitats and are less aggressive (Letourneur
2000), were responsible for the three chases observed on ‘naturally absent’ reefs.
Density
In general, the presence of S. nigricans did not influence the density of other focal
fishes surrounding patch reefs (plus 1 m perimeter) (see Appendix E: Table E-2 for
species list). However, surgeonfishes showed a significant difference in density among
reef types, with insubstantially higher densities on absent and removal reefs than reefs
with S. nigricans present (GLMM, Wald F2,193=3.81, P=0.02; A vs P: t193=2.13, P=0.03;
R vs P: t193=1.21, P=0.01; Figure 2-4, Appendix E: Table E-3).
Microhabitat use
Territorial behavior by S. nigricans influenced reef use of surgeonfishes,
parrotfishes, and corallivores: I observed greater use of the substrate or water column
surrounding the reef – rather than the actual reef – when S. nigricans was present, and
the opposite when removed (H2A ,H3A: t197≥2.50, P≤0.01 for all families; Appendix E:
Table E-4; Figure 2-4). In contrast, reef use did not differ between naturally absent
(control) reefs and reefs with S. nigricans present, except for surgeonfishes, which were
observed using control reefs more frequently than present reefs (Figure 2-4; A vs. P:
T197=3.78, P=0.0002).
Foraging frequency
The frequency of individuals observed foraging varied significantly with reef type
for butterflyfishes, surgeonfishes, and parrotfishes: For each of these families,
individuals were observed foraging more frequently on S. nigricans removal reefs
versus reefs with S. nigricans present and, sometimes, naturally absent reefs (Figure 2-
44
4). Roughly twice as many butterflyfishes, were observed foraging on reefs where S.
nigricans was removed, than when present (H3A: 28 ± 9% versus 10 ± 6%; GLMM, Wald
F2,197=6.01, P=0.002; t197=3.61, P<0.004). Similarly, I observed surgeonfishes foraging
twice as often when S. nigricans was removed, relative to present (H2A: 49 ± 10%
versus 24 ± 9%; GLMM, Wald F2,197=99.48, P<0.0001; P vs. R: t197=5.16, P<0.0001).
Parrotfishes exhibited a similar, slightly stronger, pattern, with roughly four times the
number of individuals observed foraging on reefs with farmerfish removed (74 ± 10%)
relative to present (17 ± 7%) (H2A: GLMM, Wald F2,197=20.15, P<0.0001; t197=12.17,
P<0.0001). There was no difference in foraging between reefs with S. nigricans
naturally present or absent for all families (Figure 2-4, THSD=1.13, P=0.40, Appendix E:
Table E-5) and the observed foraging patterns among treatments suggest an interplay
between reduced reef access (when S. nigricans is present) and differences in resource
quality and abundance and, thus, attractiveness (when S. nigricans is removed vs.
absent).
Changes in reef composition
At the end of the experiment, turf cover dropped by two thirds on reefs where S.
nigricans was removed (16.6 ± 7%) relative to reefs where S. nigricans remained (50.2
± 8%; H2B: ANOVA, F3,28=10.25, P<0.0001), thereby significantly increasing the amount
of bare substrate and crustose coralline algae (55 ± 7%; H2B: ANOVA, F3,28=40.25,
P<0.0001). The level of macroalgae was also significantly lower; however, the cover of
live Porites or branching corals did not differ among these treatments (Appendix A:
Figure A-2, Table A-4).
45
Experimental Responses
Frequency of predation
Corallivory of exposed nubbins occurred for the two acroporids, but not for the
other two corals tested (H3B): Exposed Acropora were ~100 times (11.2 to 1000) more
likely to incur predation on reefs where S. nigricans was removed or absent (Wald
χ2=16.44, P<0.0001). Similarly, exposed Montipora nubbins were ~ 27 times (3.9 to
200) less likely to incur predation in the presence of Stegastes (Wald χ2=11.09,
P=0.0009; Figure 2-2B). Cages provided an effective barrier to corallivory (save for a
few large individuals on removal and control reefs that were not completely protected by
cages (Figure 2-2) and there were no significant differences between control versus
open sub-treatments (Appendix D: Table D-1): Exposed Montipora and Acropora
nubbins were ~200 (26.3 to 1000) and ~300 times (35.7 to 1000), respectively, more
likely to suffer skeletal damage than caged nubbins (Logistic reg., Acropora: Wald
χ2=21.37, P<0.0001; Montipora: Wald χ2 = 20.37, P<0.0001). However, exposed
Pocillopora or Porites coral nubbins on the same reefs suffered no obvious damage.
Temporal change in coral mass
I attribute losses in coral mass to predation because I did not observe storm
surges, or other physical damage, during our short (32 d) study. Significant coral by S.
nigricans treatment (ANOVA, F12,418=1.76, P=0.05) and coral by caging sub-treatment
interactions (ANOVA, F6,418=4.78, P<0.0001) suggest that corals varied in their
susceptibility to decreased growth due to predation (H3C). Acropora and Montipora had
significantly reduced mass after 32 days when exposed (uncaged) on reefs where
Stegastes was removed or naturally absent (control reefs), but not when Stegastes was
present (Figure 2-2). There were no significant differences in mass among treatments or
46
sub-treatments for Porites, despite overgrowth, or for Pocillopora (Appendix C: Figure
C-1, Tables C-1 & C-2). When I assessed growth in the absence of predation (i.e.,
caged sub-treatment), there were no significant differences across treatments for any
coral species (H2D) (Appendix C: Table C-3). I observed significantly lower losses for
Acropora and Montipora in cages relative to control (THSD=3.65, P=0.0008) and exposed
(THSD=4.90, P<0.0001) sub-treatments (Figure 2-2 A & B) indicating cages functioned
as intended. The lack of significant differences between the control and open sub-
treatments (THSD=1.26, P=0.42) suggests that possible negative physical effects (e.g.,
reduced light and flow) of the cages can be disregarded.
I estimated the magnitude of skeletal loss due to predation as (Exposed – Caged)
/ Caged. This is a measure of corallivore consumption rates (exposed and control
nubbins) relative to the intrinsic growth rate of coral (caged nubbins). I compared loss
rates in the removal or absence, relative to the presence, of S. nigricans using ratios.
For Acropora, predation resulted in 4.3 or 5.0 times higher skeletal loss when S.
nigricans was removed or naturally absent, respectively, relative to when S. nigricans
was present (Figure 2-2A). Whereas, for Montipora, skeletal losses were 2.3 or 2.4
higher on reefs where S. nigricans was naturally absent or experimentally removed,
respectively, versus reefs with S. nigricans present. The low growth rate for Montipora
when exposed on Stegastes reefs (Figure 2-2B) contributes to this reduced ratio and
suggests that S. nigricans defense may be less effective for this species. Alternatively,
S. nigricans may actually contribute to the predation (see below).
Frequency of algal overgrowth
The frequency of algal overgrowth varied significantly among treatments for three
of the four corals tested (H2C): Porites nubbins were 3.4 times (1.4 to 8.4) more likely to
47
be overgrown in the presence of turf (Figure 2-3A, Logistic reg., Wald χ2 = 7.41, P =
0.007) and Acropora nubbins were 7.1 times (1.4 to 36) more likely to incur overgrowth
in the presence of turf (Wald χ2=5.47, P=0.02). However, the overall frequency of
overgrowth was generally twice as high for Porites than for Acropora (Figure 2-3A).
Montipora nubbins were 11.3 times (1.3 to 101.3) more likely to be overgrown in the
presence of S. nigricans (Figure 2-3A, Wald χ2=4.65, P=0.03), regardless of turf
manipulation (Appendix D: Table D-2). Interestingly, exposed (open and control)
Montipora nubbins were 3.4 times (1.0 to 11.4) more likely to be overgrown than were
caged nubbins (Figure 2-3A, Wald χ2=3.90, P=0.05), suggesting that Montipora may be
bitten by S. nigricans thus facilitating overgrowth, although I did not observe predation
directly. Overall, variation in algal abundance predicted a large amount of the variation
in overgrowth for Porites (Linear Reg., Adj. R2=0.53, P=0.001) and Acropora (Figure 2-
3B, Adj. R2=0.46, P=0.003), but not Montipora (Figure 2-3B, Adj. R2=0.14, P=0.10).
Pocillopora did not incur substantial overgrowth in any treatment (Appendix D: Figure D-
1, Tables D-2 and D-3).
Discussion
On Moorea patch reefs, territorial behavior by S. nigricans effectively reduces reef
access, and thus foraging opportunities, for common, facultative corallivores
(butterflyfishes) and herbivores (surgeonfishes and parrotfishes) (Figure 3). This
reduced corallivore access indirectly increased the survival and growth of Acropora and
Montipora (Figure 1), but no destructive predation or differences in growth were
observed for either Pocillopora or Porites. Similarly, reduced herbivore access in the
presence of S. nigricans indirectly increased turf abundance at both the reef (Appendix
48
A: Figure A-5) and nubbin scales (Appendix B: Figure B-2), with detrimental
consequences for three of the four coral species tested (Figure 2).
The high predation and associated skeletal loss in the absence and removal of S.
nigricans for Acropora striata and Montipora floweri (Figure 1), suggests that this key
engineer may be capable of indirectly facilitating growth and survival of these
disturbance-sensitive corals. Indeed, it is this territorial behavior that likely underlies the
observed higher recovery of some corals in the presence of Stegastes spp. following
the series of natural disturbances in the 1980s (Done et al. 1991, Gleason 1994,
Mapstone et al. 2007, Chapter 4, Galzin et al. In preparation). I was surprised not to
observe a similar response for Pocillopora (Appendix C: Figure C-1), as Gleason (1994)
previously documented reduced predation on juvenile fragments within S. nigricans
territories in Moorea. This inconsistency may be due to spatiotemporal variation in
corallivore distribution, as there are fundamental differences in the morphology, and
thus likely the susceptibility, of these corals to predation (Cole et al. 2008). Acroporids
are often thin and finely branching, with a fragile, spongy skeleton architecture, thus,
when accessible, can be cropped substantially by corallivores (Figure 1). In contrast,
Pocillopora forms thick lobe-like branches and has a dense skeleton that makes
destructive predation of large colonies only accessible for grazers with strong dentition
and musculature like that of Tetradontiforms, e.g. puffers (Wellington 1982) and
filefishes (Jayewardene et al. 2009). While these taxa were observed in the study
system, they are numerically rare and shy, and were never sampled despite our
intensive surveys. Additional research on destructive corallivores is needed to tease
apart variation in susceptibility, prey preferences, and frequency dependent predation.
49
Species also varied in their susceptibility to overgrowth by turf: Acroporids and
poritids incurred significantly more overgrowth in the presence of farmerfish and farmed
turf, but the overgrowth effect was 2 to 3 times larger for Porites, than for Acropora or
Montipora, respectively (Figure 2A). Thus, although these acroporids incur some
overgrowth, the relative risk of (at least partial) mortality is likely higher outside of
territories given the rate and magnitude of predation (Figure 1). For Porites, there is no
apparent benefit of S. nigricans. Because Porites spp. are currently the dominant reef-
builders within the lagoons of Moorea (Done et al. 1991, Berumen and Pratchett 2006),
overgrowth by Stegastes-induced turf may significantly increase the amount of
settlement space available for the other, more turf-tolerant taxa, like Pocillopora, which
did not incur significant overgrowth. In Moorea, ambient rates of overgrowth of Porites
by turf can be high, depending on biotic factors and season (White et al., unpubl. data),
thereby opening space for any colonists that can tolerate the turf. Indeed, recruitment of
Pocillopora has been shown to be higher within S. nigricans territories, relative to
heavily grazed or macro-algae dominated areas (Gleason 1996). In Moorea, the
reduction in post-settlement mortality, due to decreased predation in the presence of
territorial exclusion by S. nigricans, may be particularly important for life stages and taxa
that are vulnerable to grazing pressures (e.g., coral recruits and delicate acroporids).
Partial predation by farmerfish may weaken, and thus predispose, Montipora to
overgrowth. I observed higher overgrowth for exposed (vs. caged) individuals in the
presence of S. nigricans, regardless of turf treatment (Figure 2A). Given the lack of a
relationship with turf abundance (Figure 2B), our results hint that initial bites by S.
nigricans may predispose individuals to overgrowth, though additional manipulations,
50
with more frequent assessments of coral health, are necessary to tease apart these two
factors. Within the lagoons of Moorea, large colonies of Montipora and Acropora are
most commonly found within Stegastes’ territories, except in areas of very high water
flow (Galzin et al. In preparation), suggesting that (even Stegastes-facilitated) algal
competition is less of a threat than coral predation in this system.
Given that S. nigricans territories can cover 40% or more of the reef area on a
given Moorean back reef (Gleason 1996, Galzin et al. In preparation), these differential
responses can lead to marked changes in coral distributions. Pocillopora have
increased significantly in cover relative to pre-disturbance levels (Berumen and
Pratchett 2006), which is consistent with our observed low mortality in the presence of
both farmed turf and corallivores. In contrast, Acropora, which incurred high mortality via
predation in the removal and natural absence of S. nigricans, has failed to recover
(Berumen and Pratchett 2006). Previous authors have suggested this lack of recovery is
due to the frequency of disturbance (Berumen and Pratchett 2006). While this
undoubtedly plays an important role, it does not explain the higher abundance (Done et
al. 1991, Mapstone et al. 2007) and size of Acropora and other rare corals within
Stegastes territories relative to outside (Chapter 4, Galzin et al. In preparation).
Stegastes nigricans usually inhabit Acropora thickets (e.g., Indian Ocean: Lison
de Loma and Ballesteros 2002; Indo West Pacific: Jones et al. 2006; East Pacific:
Mapstone et al. 2007). The natural disturbances in the early 1980s led to a severe
reduction of these habitats in Moorea lagoons (Beruman and Pratchett 2006, Mapstone
et al. 2007) and mostly relegated farmerfish to dead portions of the remaining dominant
coral, Porites (Done et al. 1991, Chapter 3). Thus, the manner in which farmerfish act
51
as a key engineer appears to vary across environmental stress regimes: In relatively
pristine areas, farmerfish are a nuisance inhabitant of branching Acropora thickets
because they bite living tissue and induce algal overgrowth (e.g., Kaufman 1977). In
contrast, in areas with high grazing rates they can inhabit disturbance-tolerant massive
corals and territorially defend branching corals, thereby indirectly cultivating more turf-
tolerant corals that are sensitive to grazing outside territories (Wellington 1982, Suefuji
and van Woesik 2001, this study).
Nubbins provide a convenient way to control the distribution of coral in an
experimental setting; however, the degree to which their growth (Elahi and Edmunds
2006) and survival really reflect those of juvenile corals remains to be tested for most
taxa. I use nubbins as a relative test and acknowledge that a demographic
understanding is crucial for understanding the observed community change, with the
ultimate goal of predicting which life stages are most crucial for restoration due to
ontogenetic variation in vulnerability (Werner and Gilliam 1984). Additional long-term
experimental removals, using in situ size distributions of corals paired across territories,
are underway to scale up our measurements to the demographic level.
Conclusions and Implications
I suggest that Stegastes nigricans may act as a key engineer by indirectly
facilitating recovery of coral species that are otherwise sensitive to disturbances. While
the dominant massive Porites are less susceptible to disturbances than branching
corals (Berumen and Pratchett 2006), they are more vulnerable to competition with
farmed algal turf. Colonization of massive Porites (P. lobata, P. lutea,and P.
australiensis ) by S. nigricans decreases live coral cover (Done et al. 1991, White et al.,
In preparation, a) and can enhance substrate availability for many organisms, including
52
corals (Gleason 1996). Territorial defense can decrease predation for delicate
acroporids (Suefuji and van Woesik 2001, this study). The increased abundance (Done
et al. 1991, Shima et al. 2008) and size of branching corals within territories (Chapter 4,
Galzin et al. In preparation) may enhance habitat diversity, as these taxa can serve as
foundation species for crustaceans (e.g., Stewart et al. 2006), other damselfishes
(Holbrook et al. 2000), and early life stages of other reef fishes (Shima et al. 2008).
Bioerosion appears to alter the morphology of Porites patch reefs, creating complex
lobes of living coral surrounded by algal turf (Done et al. 1991). There is some evidence
that farmerfish require structural complexity (Wellington 1982), thus the facilitation of
branching corals may form an important feedback for farmerfish population growth and
corresponding community dynamics.
.
53
Figure 2-1. Mean frequency of coral predation. The average frequency of coral predation and corresponding average daily loss in skeletal mass (± 95% CI) was higher in the removal or absence of S. nigricans for A) Acropora striata and B) Montipora floweri. Treatment labels indicate the experimental level (PRESENT or REMOVED (–)) of Stegastes nigricans (Stegastes) crossed with farmed turf (Turf), and naturally ABSENT control reefs (Ø), yielding five unique treatment combinations. Bar color indicates whether nubbins were CAGED (black) or EXPOSED (cage control or open = gray). Pocillopora verrucosa and Porites australiensis did not incur any obvious predation (Appendix D: Table D1) or significant differences in daily growth among treatments or sub- treatments during the course of the experiment (Appendix C: Figure C1).
Figure 2-2. Frequency of coral overgrowth. A) Three of the four species tested, Porites australiensis, Montipora floweri, and Acropora striata, incurred significantly higher overgrowth when farmed turf was PRESENT, versus REMOVED or ABSENT (treatment designations match Figure 2-1, but order is altered to highlight the effect of interest). B) The average amount of algae present in a given treatment predicted 53% of the variation in overgrowth frequency for P. australiensis and 46% of the variation in overgrowth frequency for A. striata, but offered no significant predictive power for M. floweri (Linear Regression, algal mass was arc sine square root transformed to meet normality assumption, here I present raw data, Appendix D: Table D-3). Pocillopora verrucosa incurred very little overgrowth (~10% or less) in any treatment, regardless of turf abundance (Appendix D: Figure D1, Tables D2-D3).
55
Figure 2-3. Mean density, reef use, and foraging frequency of target fish families. A) Mean density of surgeonfishes (Acanthuridae), parrotfishes (Scaridae) and butterflyfishes (Chaetodontidae) (± 95% CI) among reefs with Stegastes nigricans PRESENT (dark gray bars), REMOVED (gray bars), or ABSENT (light gray bars). B) The mean proportion of fishes observed using the experimental reefs (vs. the water column and adjacent substrate; ± 95% CI), and C) the mean proportion of fishes foraging on experimental reefs (± 95% CI) was consistently higher on S. nigricans removal reefs for surgeonfishes, parrotfishes, and butterflyfishes (see Results, Appendix E: Tables E3-E5).
56
CHAPTER 3 INDIRECT EFFECTS OF STEGASTES NIGRICANS ON MASSIVE PORITES CORAL
AND IMPLICATIONS FOR OTHER COMMUNITY MEMBERS
Introduction
Trees (Ellison et al. 2005), plants (Alteri et al. 2007), coral (Bruno et al. 2003), and
algae (Eriksson et al. 2006) function as ecosystem engineers because they create,
modify, or maintain habitats for other species through their physical structure (Jones et
al. 1994). Consumers have been shown to mediate the distribution of habitat-forming
species across ecosystems (Grasslands: Chase et al. 2000; Oak Savanna: Ritchie et al.
1998; Rocky intertidal zone: Bertness et al. 2002, Bertness et al. 2004; Kelp forest
ecosystems: Halpern et al. 2006; Coral Reefs: Burkepile and Hay 2006) thereby
changing resource availability for other community members. Simultaneous with
foundational (e.g., Dayton 1972) and consumer-driven habitat modification (e.g., Power
1997), ecosystem engineers can further modify community structure through non-
trophic interactions (i.e., behaviors), to create patches with assemblages of organisms
that differ from unmodified surrounding habitats (e.g., dam building by beavers, Jones et
al. 1994, 1997). Engineering can have both positive and negative consequences for
species that inhabit the new or old habitat, respectively (Jones et al. 1997).
Some territorial damselfishes (Pomacentridae), known as “farmerfish”, engineer
the community structure of coral reefs by developing and maintaining conspicuous
filamentous algal mats (hereafter, turf) (reviewed by Ceccarelli et al. 2001). Farmerfish
of the genus Stegastes tend to farm dense, filamentous red algal turf, and Polysiphonia
species in particular, are the dominant algae within the territories of more than half the
Stegastes species investigated (Ceccarelli 2007). Of the common mechanisms of
competition between corals and algae, farmerfish-associated turf is most likely to
57
preempt settlement space, or overgrow, rather shading or abrading, corals (reviewed by
McCook et al. 2001). Filamentous turf can also reduce flow and increase rates of
sedimentation (Purcell 2000), and sediment trapped by turf can harm corals (Potts
1977, McCook et al. 2001, Nugues and Roberts 2003) or reduce recruitment within
areas occupied by turf (Birrell et al. 2005). In addition, there is some experimental
evidence that indirect contact between corals and turf may facilitate mortality via
bacteria-associated disease (Smith et al. 2006). Algal turf within territories can increase
the rate of overgrowth on coral (Potts 1977, Lobel 1980) and coral spat (Sammarco and
Carleton 1981). Farmerfish may also actively remove coral recruits or living coral tissue
to expand the size of territories (Kaufman 1977, Robertson et al. 1981) and
susceptibility to this damage can vary depending on coral morphology (Wellington
1982). When territories are established on dead coral, through whatever mechanism,
there is higher bioerosion due to increased densities of boring sponges and
sipunculans, presumably as a result of reduced grazing by other fishes within territories
(Risk and Sammarco 1982).
There is evidence that coral species vary in their susceptibility to overgrowth within
farmerfish territories (Sammarco and Williams 1982, Wellington 1982, Glynn and
Colgan 1988, Done et al. 1991, White and O’Donnell In press). For example, in a recent
experimental test, massive Porites australiensis incurred considerably higher frequency
of overgrowth with turf present, than other corals tested (Acropora striata, Montipora
flowerii, and Pocillopora verrucosa) (Chapter 2). Within Moorea lagoons today, the
common Pacific farmerfish, Stegastes nigricans, typically colonizes these dominant
massive Porites (Done et al. 1991, this study). When colonized, these reefs have an
58
altered morphology (Done et al. 1991, Figure 3-1), likely due to the eroding influence of
abundant boring invertebrates within territories (e.g., Risk and Sammarco 1982,
Sammarco and Risk 1990). Massive Porites colonies occupied by Stegastes nigricans
maintain higher abundances of filamentous turf (especially Polysiphonia spp.) and
sediment (Vuxton et al. In preparation). Dendropoma maxima, a conspicuous, tube-
dwelling vermetid snail (Vermetidae), commonly inhabits colonies of Porites in Moorea
lagoons (Peyrot-Clausade 1992). Vermetid snails cast a mucus web to filter feed
(Hughes and Lewis 1974). These mucus webs remove sediment (Kappner et al. 2000)
and can smother algae and reduce turf-associated sedimentation within S. nigricans
territories (pers. obs.). They also have been shown to decrease coral growth,
presumably because their mucus nets can also interfere with coral feeding and/or
respiration (Colgan 1985). Thus, vermetid snails may function as cryptic consumers and
mediate turf-Porites competition if they are near the zone of contact, by indirectly
lowering the sediment accumulation and, possibly, the rate of overgrowth by turf.
This study asked the following questions:
1. What is the abundance of turf and live coral on massive Porites patch reefs with adult Stegastes nigricans present and absent?
2. On Porites reefs colonized by Stegastes nigricans, is the rate of overgrowth by algal turf driven by the effects of turf, sediment, and/ or vermetid snails?
Previous research indicates massive Porites are particularly susceptible to
overgrowth by turf (Chapter 2). This design scales up from using coral fragments
(nubbins) to measuring rates of turf overgrowth at the live Porites-turf transition zone.
59
Methods
Paired Field Surveys
To answer the first question, I selected 24 pairs of massive Porites reefs
(colonized versus uncolonized by Stegastes nigricans, Figure 3-1), in Vaipahu lagoon
on the north shore of Moorea in April 2005. Paired reefs were similar in size (Appendix
F: Figure F1) and location (average distance between pairs, mean ± 95% C.I.: 7.9 ± 1.9
m), but differed in that ‘colonized’ reefs were defined as having adult Stegastes
nigricans present and consequently had obvious turf cover, whereas ‘uncolonized’
Porites reefs had no adult S. nigricans or associated turf. I measured the dimensions of
each reef, including footprint (maximum length and perpendicular width), average and
maximum height, and a rough estimate of reef volume (length x width x average height;
m3). In addition, I measured the composition each reef using fixed point contact, at 10
cm intervals, of 3 transects laid perpendicular to the longest reef axis. This yielded an
estimate of live massive coral (Porites) and farmed filamentous algal turf cover in the
presence and absence of farmerfish. For each reef, I also counted the number, and
estimated the size (within 5mm), of all S. nigricans.
Transition Zone Field Experiment
To answer the second question, I selected 9 massive Porites reefs interspersed
within Vaipahu lagoon that were colonized by Stegastes nigricans. Experimental reefs
contained at least four areas selected for quadrats, approximately equally spaced
around the reef, that met the following criteria: 1) vertical orientation; 2) relatively flat
surface to accommodate reference nails; 3) roughly equal cover of live coral and turf
algae; and 4) 2 – 3 vermetid snails in algae near or below base of quadrat and not in
contact with coral. This insured adequate coverage of mucus nets over algae within a
60
given quadrat, while eliminating impact of mucus nets on coral. On each of these
experimental reefs, 4 permanent photo quadrats were established, using 3 or 4
permanent markers (stainless steel nails) (Figure 3-2). Nails provided visual reference
for the 20 cm x 20 cm photoquadrat frame and allowed compensation for error
associated with photoquadrat placement (see Appendix F: Figure F-2 for representative
photographs).
I used experimental manipulations to decouple and explore the effects of turf,
sediment, and vermetid snails on the rate of turf overgrowth onto living massive Porites.
This yielded four treatments (one quadrat for each treatment) on each of 9 reefs:
+turf/+sediment/-vermetid snails; -turf/-sediment/-vermetid snails; +turf/-sediment/-
vermetid snails; +turf/+sediment/+vermetid snails (Table 3-1). Some quadrats were lost
because reefs crumbled and degrees of freedom were constrained accordingly
(Appendix F: Table F-1, Figure F-2). Treatments were randomly assigned, to control for
variation in flow around a given reef, and maintained daily.
Treatment implementation
For all but the vermetid snails present quadrat (Treatment 4, Table 3-1), vermetid
tubes and snails were removed with large nails. Although this removal only occurred at
the beginning, this can be considered a “press” treatment, because vermetid snails will
not settle and grow to sufficient sizes within the short (6 week) duration of the
experimental trial. For turf removal plots, all existing turf was initially removed with
stainless steel brushes to expose underlying dead coral substrata. Turf removal
treatments were then maintained by daily scrubbing with firm toothbrushes, taking care
not to abrade live coral. For sediment removal quadrats, sediment was removed daily
by gentle (manual) rubbing of turf to loosen sediment, combined with brief, directed flow
61
(with my hand). The other two treatments (ambient turf and sediment with and without
vermetid snails) were not manipulated post removal of vermetid snails (see Appendix F:
Figure F-2 for representative photographs of treatments after implementation).
Digital photographic analyses
The experiment was conducted during the austral summer (14 February – 30
March 2007). To measure the response to manipulations, photos were taken
immediately after treatment implementation (initial) and re-taken after 6 weeks (final).
Photos were analyzed using CPCe (Kohler and Gill 2006) and measurements made
were blind with respect to period (initial vs. final) and treatment (except for the turf and
sediment removal treatments, which were obvious), but not with regard to quadrat, as
paired lines required placement verification. For each photo, I recorded linear
measurements (n=4/ quadrat) from the edge of each quadrat to the boundary of turf,
and a second measurement from the edge of the quadrat to a distinct coral boundary
(i.e., a distinct lobe of living Porites) (see Appendix F, Figure F-3, for schematic of line
measurements). Thus, the zone of live Porites was defined by this latter measurement
(live coral plus turf or dead substrata, depending on treatment), minus the first
measurement (just turf or dead substrata). For each line, I also measured the size of
obvious dead tissue / exposed skeleton at the transition zone (i.e., the ‘zone of dead
tissue’, see inset in Figure 3-6, schematic in Appendix F: Table F-3). At the termination
of the experiment, I calculated the average linear change (final - initial) in the live coral
boundary zone for each quadrat (schematic in Appendix F: Table F-3). In the case of
change in live coral, a positive response indicates tissue growth, while a negative
response indicates tissue loss (overgrowth) (Appendix F: Table F-3). For the zone of
dead tissue, a positive change would indicate a larger zone of tissue damage (prior to
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overgrowth), and a negative change would suggest this loss of tissue was ameliorated
or that algae overgrew it.
Statistical Analyses
Paired field surveys
I performed a paired t-Test to verify that reefs did not vary in initial volume (length
x width x average height, m3; measurements were missing for one reef, thus paired
sample sizes were reduced accordingly). I also used paired t-Tests to evaluate whether
there was significantly higher abundance and size (in mm) of Stegastes nigricans on
colonized versus uncolonized Porites reefs. I examined the average difference in
Porites reef composition (i.e., % cover) in the presence and absence of adult S.
nigricans by first summing the cover of each category across the three transects for
each reef to reduce the degrees of freedom to the appropriate level (n=24). I then tested
the mean (arc sine square root transformed) proportion cover of each variable as a
function of ‘Reef Type’ (Porites reefs colonized by S. nigricans vs. uncolonized Porites
reefs; t.test, option=paired, R, v.2.9.2).
Transition zone experiment
I performed a linear mixed model to evaluate the linear change in live Porites
tissue by the fixed effect of Treatment (Table 3-1), with the random effects of quadrat
(n=4) nested within reef (n=9) (lme, R, v. 2.9.2, Appendix F: Table F3). This took into
account the unbalanced design and insured a conservative treatment denominator
degree of freedom of 21 (Pinheiro and Bates 2000, p. 91). I examined the residuals and
Q-Q plot. The change in live Porites data set was not perfectly normal; however, when I
tested the subset of the data set that satisfied this assumption the results did not
change (Appendix F: Table F1), and I report results from the full data set. In addition, I
63
evaluated the effects of interest using contrasts defined a priori (Table 3-1; Appendix F:
Table F2, Figure F-2). The same analysis was repeated for the change in the amount of
dead tissue between live Porites and algal turf (i.e., the ‘dead tissue zone’) (lme
(package: nlme), R, v. 2.9.2, Appendix F: Table F3).
Results
Observational Results: Paired Surveys
As defined above, ‘colonized’ reefs had adult Stegastes nigricans present,
whereas ‘uncolonized’ Porites reefs had no adult S. nigricans. Paired reefs did not differ
significantly in size (t=1.87, df=22, P>0.05; Appendix F: Figure F-1). Colonized Porites
reefs had 10 times more S. nigricans (across size classes) than uncolonized Porites
reefs (t=10.60, df=23, P<0.001, Figure 3-3). Of the 24 uncolonized Porites reefs
examined, juvenile S. nigricans were observed on 7 reefs. The sizes of S. nigricans
were substantially larger on colonized reefs (Figure 3-3, t=5.55, df=6, P=0.001). With
this difference in S. nigricans size and abundance (Figure 3-3), there was an associated
change in reef cover (Figure 3-1 and 3-4). On average, uncolonized Porites reefs had
nearly twice as much live Porites cover (80.5 ± 8.9%) than colonized reefs (42.9 ±
10.1%) (t-test, t=6.71, df=23, P<0.001). In contrast, these colonized reefs had roughly
25 times more filamentous algal turf (42.0 ± 8.2%) than uncolonized reefs (1.6 ± 3.0%)
(Figure 3-4; t-test, t=7.99, df=23, P<0.001). Each of the other cover categories (i.e.,
macroalgae, dead coral, crustose coralline algae, and other live corals) comprised on
average <5% of the total reef cover and were not further analyzed.
Experimental Results: Porites-Turf Transition Zone
The change in live Porites tissue varied significantly among treatments (Figure 3-
5; lme, F3,21=3.33, P=0.04, Appendix F: Table F-1). A profound loss of live Porites
64
occurred under ambient abundances of turf and sediment (and removal of vermetid
snails) (nearly 5 cm in 6 weeks, Figure 3-5). In contrast, loss of live Porites tissue was
lowest with sediment removal (Figure 3-4). Loss rates were also relatively low with
manual removal of turf or, as well as with ambient density of vermetid snails, which cast
a mucus web and inadvertently remove sediment from turf (see video of D. maxima
feeding, Object 3-1). As defined a priori (Table 3-1), there was not a significant ‘Turf
effect’ (t=1.04, df=21, P>0.05, Appendix F: Table F-2) or ‘Vermetid effect’ (t=1.04,
df=21, P>0.05, Appendix F: Table F-2); however, there was a significant effect of
‘Sediment’ (t=2.27, df=21, P=0.03, Appendix F: Table F-2). There was no significant
difference in the size of the dead zone among treatments (Figure 3-6; Appendix F:
Table F-3).
Object 3-1. Video of vermetid feeding (28.9 MB .avi)
Discussion
Stegastes nigricans farms filamentous algal turf through a series of behaviors,
including ‘weeding’ un-preferred algae (e.g., Hata and Kato 2002, 2006) and
invertebrates (e.g., snails: Lobel 1980; urchins: Williams 1981), as well as territorial
defense (reviewed by Ceccarelli et al. 2001). Massive Porites are the dominant
hermatypic coral in the Moorea lagoon today. Those occupied by S. nigricans have
roughly half as much live coral cover as ‘uncolonized’ Porites reefs, with a concomitant
increase in filamentous algal turf (Figures 3-1 and 3-3). With ambient levels of turf and
sediment (and removal of vermetid snails), the rate of overgrowth by algal turf was
nearly 5 centimeters in a six-week period (Figure 3-5). However, removal of sediment
(only) countered this overgrowth and live coral tissue significantly increased, with a
reciprocal loss of turf, within these quadrats (Figure 3-5). Among the competitive
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mechanisms used by algae, recent evidence suggests that the alga is not always the
direct agent of death, but rather the trigger. For example, the green, calcareous alga,
Halimeda opuntia, hosts a bacterium (Aurantimonas coralicida) that stimulates disease
(white plague type II) of the massive coral Montastraea faveolata, and thus facilitates its
overgrowth (Nugues et al. 2004). Similarly, Smith et al. (2006) suggested that the
release of Dissolved Organic Carbon by algae could enhance microbial abundance and
adversely affect corals. Potentially an increased availability of nutrients or food (such as
Particulate Organic Carbon in sediment) may induce a bloom in the bacterial community
that can either lead to pathogenic infection of corals or cause coral tissue loss due to
physiological stress such as hypoxia as bacteria consume available oxygen (Kline et al.
2006; Kuntz et al. 2005). Indeed, recent analyses suggest there is a 60% reduction in
Dissolved Oxygen at the interface between farmerfish turf and coral tissue, with
associated loss of coral tissue (Barott et al. 2009) as was observed in the Moorea
system (see inset in Figure 3.6).
Farmerfish may facilitate settlement, growth, and survival of some mobile
organisms through habitat modification (Ceccarelli et al. 2001). Dense algal turf on the
lobes of massive corals may facilitate a rugose morphology, in the place of less
complex mounds (Figure 3-1, Done et al. 1991), because there are higher densities of
internal bioeroders within territories (reviewed in Ceccarelli et al. 2001). Increased
bioerosion weakens the structure of a reef (Risk and Sammaro 1982; Huston 1985) and
increases its structural complexity (Figure 3-1, Done et al. 1991). The turf itself also
adds structure, with some Polysiphonia (e.g., P. sertulosa) maintaining average lengths
of 15 mm (pers. obs.). This added complexity facilitates the buildup of higher densities
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of small invertebrates than adjacent, more barren, areas (Klumpp et al. 1988), and, with
the higher abundance of algal turf, may augment the food supply for other territory
residents. For example, Green (1992, 1998) noted higher abundance of juvenile labrids
and scarids within damselfish territories. Within S. nigricans territories in Moorea, it is
common to find massive Porites colonies that have undergone partial mortality and are
covered with turf, with live coral limited to the top of the lobes (Figures 3-1 and 3-2).
These territories have disproportionately higher densities of juvenile fish than adjacent
live coral habitat and juvenile wrasses, Thalassoma hardwicke, experience weaker
density dependence (Shima et al. 2008), suggesting an indirect positive effect of the
habitat modification.
Conclusions and Future Directions
Massive Porites are the dominant hermatypic corals within the lagoons of
Moorea (Beruman and Pratchett 2006). Their ability to settle to rubble on an otherwise
sandy surface (Idjadi and Edmunds 2003) offers a great resource to other taxa that
require hard bottom for settlement. Vermetid snails are the most conspicuous sessile
fauna on Porites (followed by the serpulid, Spirobranchus giganteus, O’Donnell and
White, In preparation, White et al. In preparation-b). Sessile vermetid snails consume
sediment and entrapped particles at a nearly constant rate (Kappner et al 2000) and this
sediment consumption may indirectly reduce the rate of Porites overgrowth by turf
within S. nigricans territories (Figure 3-5). Although, Coles and Strathmann (1973)
reported no fish feeding on vermetid snail mucus, I have observed adult S. nigricans
steal (and eat) the mucus webs from large vermetid snails (Dendropoma maxima) within
their territories. Indeed, S. nigricans is considered to be at least a partial detritivore
(Wilson and Bellwood 1997), thus these sessile snails, which can arrest the
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development of the farmed turf front, may compete with S. nigricans for food resources.
Additional research is necessary to understand how physical drivers that influence
sediment levels (e.g., flow), affect the rate of overgrowth of S. nigricans-associated turf
over massive Porites, as well as whether microbial drivers are responsible for the loss
of live Porites in the presence of turf and sediment. Ongoing research seeks to quantify
whether vermetid snails are depressed within S. nigricans territories (C.D. Hartman,
senior honors thesis) by evaluating the change in abundance and size of vermetid
snails through time using photographs of recruitment tiles outplanted on reefs with S.
nigricans naturally absent, present, and experimentally removed (Hartman et al. In
preparation).
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Table 3-1. Transition-zone Experimental Treatments
Treatment Vermetid
snails Turf Sediment a priori Contrasts of Interest
1 (Control) − + + 2 − − − 2 and 3: Turf effect 3 − + − 1 and 3: Sediment effect 4 + + + 1 and 4: Vermetid effect
Notes: Summary of manipulations to lower (turf) portion of each randomly assigned experimental quadrat on a given reef (N=9). All quadrats originally contained 2-3 vermetid snails within the turf portion. Vermetid snails were removed from all quadrats except treatment 4 (vermetid snails, turf, and sediment present).
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Figure 3-1. Representative photos of reefs by type. Top panel: Healthy live ‘uncolonized’ Porites reef. Bottom panel: Porites reef ‘colonized’ by the dusky farmerfish, Stegastes nigricans (note the silhouette of a S. nigricans in the top right corner, as well as several other visible individuals).
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Figure 3-2. Simplified schematic of transition zone quadrat design. For each experimental reef, four quadrats were placed on a vertical relief, with live Porites occupying the top half, and farmed algal turf occupying the bottom half, of each quadrat. For each quadrat, stainless steel nails were used to mark the photo-quadrats and verify quadrat placement during subsequent digital measurements using CPCe (Kohler and Gill 2006). For representative photos of actual quadrats and a schematic of linear measurements, see Appendix F: Figure F-2 and Figure F-3).
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Figure 3-3. Paired reef surveys: Mean number and size of Stegastes nigricans. Reef type refers to Porites reefs ‘colonized’ by adult Stegastes nigricans versus ‘uncolonized’ Porites reefs (n=24 pairs or reefs, mean ± 95% CI). Top panel: Mean number of all S. nigricans (across size classes) was higher on colonized, than uncolonized, Porites reefs (paired t-test, t=10.60, df=23, P<0.001). Bottom panel: Only juvenile S. nigricans were encountered on 7 of the 24 uncolonized Porites reefs and, as expected, when compared to their paired colonized reef, the mean size of S. nigricans was smaller (paired t-test, t=5.55, df=6, P=0.001).
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Figure 3-4. Paired reef surveys: Mean percent cover live massive Porites and algal turf. For photos and descriptions of ‘Reef Type’ see Figures 3-1 and Figure 3-3. Top panel: There was significantly higher cover of live massive Porites coral on uncolonized, relative to colonized, Porites reefs (n=24 pairs or reefs, mean ± 95% C; paired t-test, t=6.71, df=23, P<0.001). Bottom panel: Percent cover of farmed algal turf was significantly higher on Porites reefs colonized by S. nigricans, versus uncolonized Porites reefs, (paired t-test, t=7.99, df=23, P<0.001).
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Figure 3-5. Mean linear change in live massive coral tissue by treatment. The average rate of linear change in live Porites tissue within Stegastes nigricans territories during a 6-week period in the austral summer 2007(14 Feb – 30 Mar 2007) varied according to treatment (mean ± s.e; LMM, F3,21=3.33, P=0.04; see Table 3-1 for description of treatments and contrasts). Of these, only sediment removal treatments were significantly less overgrown than the treatment with both turf and sediment present (i.e., a sediment effect; Table 3-1; t-test, t=2.27, df=21, *P=0.03; Appendix F, Tables F1 and F2).
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Figure 3-6. Mean linear change in the amount of dead Porites tissue. Inset illustrates a
large dead tissue zone in which the live coral and algal turf are separated by approximately 1 cm. There was no significant difference in the average rate of change of dead Porites tissue at the transition zone between healthy Porites and farmed turf within Stegastes nigricans territories according to treatment during a 6 week period in the austral summer 2007 (14 Feb – 30 Mar 2007; mean ± s.e.; LMM, F3,21=0.26, P=0.86; Appendix F, Table F-3; see Table 3-1 for descriptions of treatments and contrasts).
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CHAPTER 4 EFFECTS OF FARMERFISH AND CORAL PREDATORS ON THE POPULATION
DYNAMICS OF BRANCHING CORALS IN A DISTURBED LAGOON SYSTEM
Introduction
Coral reefs are declining worldwide due to natural and anthropogenic disturbances
(Bruno and Selig 2007, Knowlton and Jackson 2008). Recovery varies both within and
among systems, and ecologists are struggling to understand the mechanisms that
constrain resilience (i.e., recovery to the previous state) (e.g., Bellwood et al. 2004).
Efforts to understand variable recovery are complicated because, as with most marine
invertebrates, corals have complex life cycles (e.g., Hughes and Jackson 1980; Hughes
1984). Most ecologists use small-scale experiments to draw inference on mechanisms
limiting recovery (e.g., Burkepile and Hay 2006). Alternatively, monitoring programs
seek to demonstrate the community-wide importance of top-down and bottom-up
mechanisms on coral health (e.g., Mora 2008) or uncover large-scale variation driving
differential coral recovery (e.g., Connell et al. 1997; Hughes and Connell 1999). While
both of these approaches are important and useful, neither considers the implicit
complexity of coral population dynamics. One very successful strategy is the
combination of small-scale experiments with larger-scale monitoring, and associated
population modelling, to scale-up our understanding of processes constraining
resilience (e.g., Edmunds 2005). These, however, are rare and, to my knowledge, this is
the first experiment to measure population rates of interest (recruitment, growth, and
survival) for in situ size classes of corals, both before and after experimental
manipulations.
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Evidence Farmerfish Engineer the Coral Community
Farmerfish represent an important component of the coral reef fish community and
can account for nearly half of the total fish abundance (e.g., La Reunion Island,
Letourneur et al. 1997), with their territories covering more than 50% of shallow reef
tracts at some sites (Panama: Wellington 1982; Great Barrier Reef (GBR): Sammarco
and Williams 1982; GBR/Papua New Guinea (PNG): Klumpp et al. 1987). These site-
attached damselfish (Pomacentridae) can act as ecosystem engineers (sensu Jones et
al. 1994) and alter the benthic environment using a combination of farming behaviors,
which enhance algal turf, and territorial defense against herbivores and coral predators
(corallivores) (reviewed in Ceccarelli et al. 2001; see also Chapter 2). Coral species can
respond differently to the indirect effects of these algae-farmers (Wellington 1982,
Chapters 2 and 3). Increased biomass (Hata and Nishihira 2002; Hata et al. 2002) and
productivity (Klumpp et al. 1987) of farmed algal turf within farmerfish territories can
overgrow or increase sedimentation on corals (Vine 1974, Potts 1977) and increase
(Risk and Sammarco 1982) or decrease bioerosion, depending on fish grazing
(Sammarco et al. 1986). Territorial behavior can create spatial refuge from predation by
foraging coral-eating (corallivorous) fishes (Wellington 1982; Gleason 1996; White and
O’Donnell In press) or echinoderms (urchins: Sammarco and Williams 1982, Suefuji and
van Woesik 2001; crown-of-thorns seastar: Glynn and Colgan 1988). While it is well-
accepted that grazing herbivorous fishes (Bak and Engel 1979) and urchins (Sammarco
and Williams 1982) can reduce survivorship of juvenile corals, few studies have
examined whether corallivores can alter the distribution and abundance of larger size
classes of corals (Randall 1974; Hixon 1997), and additional research is warranted
(Rotjan and Lewis 2008).
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In the lagoons of Moorea, vulnerable corals have recovered faster in the presence
of the dusky farmerfish, Stegastes nigricans, with greater abundance, size, and diversity
of corals within territories (Done et al. 1991; Gleason 1994; Gleason 1996; Shima et al.
2006, 2008; Galzin et al., In preparation). Small-scale manipulations utilizing coral
fragments indicated that Acropora suffer considerably less predation in the presence
(versus removal or natural absence) of S. nigricans (Chapter 2). However, this pattern
did not hold for Pocillopora, a now very common coral within the lagoons (Berumen and
Pratchett 2006) that was previously reported to incur less predation within S. nigricans
territories, relative to highly grazed or macroalgae dominated patches (Gleason 1994).
Clearly, measuring interactions with coral fragments does not give us a clear indication
of the true per capita effects on corals, nor whether sensitivity varies with size. Thus, a
demographic framework is necessary to tease apart whether higher recruitment or
reduced mortality for juvenile and/or adult stages (either independently or in
combination) could be responsible for the observed differential abundances within
territories.
Diverse Life History Strategies
A complication to understanding community resilience is incorporating the diverse
life history strategies of various taxa (Hughes and Tanner 2000), as this variation drives
whether a population declines, experiences local extinction, or recovers following
disturbance (e.g., Hughes 1989). The skeletal morphology of a given taxon largely
determines whether individuals are susceptible to breakage (fragmentation), predation
and associated loss of linear extension (shrinkage), or mortality due to natural
disturbances (e.g., storms). In general, massive Porites are slow growing, but hearty,
due to dense skeletal formation and boulder-like colonies that are not amenable to
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breakage (Hughes 1989). In contrast, fragile branching Acropora generally have less
dense skeletal structure and are more susceptible to natural disturbances (Woodley et
al. 1981, Hughes 1989, Knowlton et al. 1988), except competition, because their
associated rapid growth enhances overgrowth and shading of other corals (Connell
1978, Connell et al. 2004).
The coral reefs of Moorea have been subjected to a series of natural disturbances,
since the 1980s, including cyclones, bleaching events, and outbreaks of predatory
crown-of-thorn seastar, Acanthaster planci (Adjeroud et al. 2005). The dominant coral
genera of Moorean reefs differ in their susceptibility to these disturbances (Table 4-1).
By 2003, on the north side of Moorea, the mean coral cover in the back reef had
returned to near pre-disturbance (1979) levels (~45% coral cover), but with altered
community composition (Berumen and Pratchett 2006). Massive Porites spp. were little
affected by the disturbances, but branching Pocillopora spp., which were historically at
low densities in this system (Bouchon 1985), have now surpassed once dominant
Acropora spp. (Berumen and Pratchett 2006). Acropora are ‘sensitive’ to disturbances
(e.g., Woodley et al. 1981, Hughes 1989, Adjeroud et al. 2005), while Pocillopora can
be considered to be ‘weedy’, in that they can recover more quickly following a
perturbation (e.g., McClanahan et al. 2007). I monitored these two genera
simultaneously to elucidate why Pocillopora have been observed to recover from
disturbances better than historically dominant Acropora within lagoons of Moorea,
French Polynesia (Done et al. 1991, Berumen and Pratchett 2006).
Demographic Complexity
As long-lived organisms, corals are more sensitive to increases in mortality rates
for established individuals, than changes due to fluctuation in recruitment, whereas
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short-lived taxa are generally recruitment-limited (Hughes 1990). Indeed, large colonies
may preserve abundances via the storage effect (Warner and Chesson 1985), though
asexual reproduction (i.e., fragmentation) is likely only important for branching corals
whose morphology is amenable to fragmentation and re-attachment (or solitary fungiids,
which bud) (Veron 2000). Asexual reproduction by fragmentation is common for
dominant taxa in both the Caribbean and the Indo-West Pacific (Highsmith 1982).
Further, the size and number of fragments depends on initial size and morphology of a
given coral colony, and both factors contribute heavily to the expected contribution of
fragments to population growth (Highsmith 1982). Taxa that brood larvae (e.g.,
Pocillopora) also likely contribute to the next generation faster (i.e., their population
structure is more ‘closed’) than the typical strategy of broadcast spawning (e.g.,
Acropora), especially at low densities following a disturbance (Knowlton 2001). Because
corals are modular organisms, after recruitment to an adult population, they do not only
progress sequentially through size classes. Corals can shrink, loop (i.e., stay in the
same size class), fuse (with identical genets), or fragment (Hughes 1984), and these
processes combine to decouple size-age correlations (Hughes and Jackson 1980).
Smaller corals usually have faster growth rates, but are more likely to be killed than
larger corals (Connell 1973) and, to further complicate matters, this relationship can
vary with tissue age (i.e., fragments grow slower than ‘true’ juveniles, Elahi and
Edmunds 2007a, or younger tissue, Elahi and Edmunds 2007b).
Scaling Up
Most experimentation is limited to small coral fragments, due to both logistical and
ethical concerns: This may give misleading results, because fragments may or may not
behave like the life stage they are intended to represent (e.g., Elahi and Edmunds
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2007a,b). More importantly, the ability to generalize within a population (across size
classes) is limited. One possible approach is combining observed natural gradients in
distribution (e.g., like those associated with keystone species or ecosystem engineers,
Soulé et al. 2003), with careful experimentation to tease apart mechanisms driving the
observed community structure. The main objective of this research was to scale-up our
understanding of the demographic processes underlying the observed higher
abundances of branching corals within S. nigricans territories, as well as possible
drivers of the observed lower recovery of Acropora versus Pocillopora within the lagoon.
Understanding the relative vulnerability of different size classes to mortality can inform
management practices (e.g., Crouse et al. 1987), including restoration efforts, and
identify data critical to refining our understanding of processes limiting coral recovery. In
particular, I sought to answer the following questions:
1. Does the presence of Stegastes nigricans increase the survival, growth, or recruitment of Acropora or Pocillopora?
2. Does the strength of this interaction vary with coral size? If so, what sizes of coral are most protected from predation by Stegastes nigricans territoriality?
3. Do these differences lead to a lower rate of population decay (λ) for Acropora and/ or Pocillopora when Stegastes nigricans is present?
I documented the mortality and growth rates of in situ populations of Acropora and
Pocillopora within Stegastes nigricans’ territories between 2006 and 2007. This
provided a baseline of branching coral population dynamics (including the rate of
population decay, or λ) in the presence of S. nigricans. I then removed S. nigricans from
half of the experimental reefs and documented the change in key demographic
parameters for both control reefs, and reefs with S. nigricans removed between 2007
and 2008 (i.e., a life table response experiment). In addition, I measured fragmentation
81
and recruitment of Acropora and Pocillopora to experimental reefs throughout both
monitoring periods to incorporate the dynamic aspect of these open populations. While
following individuals through time allows calculation of the population decay (λ),
fecundity is essentially decoupled from the local population and a measure of input to
an ‘open’ population (i.e., recruitment and fragmentation) is necessary to complete our
demographic understanding using matrix models (e.g., Hughes 1984, 1990).
Methods
Study System
Moorea is a high volcanic island located in the Society Archipelago, approximately
14.5 kilometers from Tahiti. It has a well-developed barrier reef along most of the island
perimeter. Much of the lagoon is shallow (1-2 m). Lagoon bottoms are dominated by
sand and rubble inshore, with patch reefs ranging from relatively isolated in the backreef
to nearly continuous near the reef crest on a foundation of hardened pavement. These
patch reefs are predominately built by massive Porites corals, which have lower
susceptibility to the natural disturbances observed in this system (Adjeroud et al. 2005,
Penin et al. 2007, Berumen and Pratchett 2006).
In Moorea, the dusky farmerfish, Stegastes nigricans, communally defends large
territories of thick filamentous turf (mostly Polysiphonia and Corallophila spp., Vuxton et
al. In preparation). Around less disturbed islands, S. nigricans typically inhabit
arborescent Acropora thickets (e.g., Indian Ocean (Reunion): Lison de Loma and
Ballesteros 2002; Indo West Pacific (PNG): Jones et al. 2006; Taiwan: Jan et al. 2003;
French Polynesia: Mapstone et al. 2007). These habitats were virtually eliminated in
Moorea (Berumen and Pratchett 2006, Mapstone et al. 2007), and S. nigricans also
colonizes the dominant massive Porites (Done et al. 1991). Porites reefs with adult S.
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nigricans territories have significantly reduced live coral cover, than un-colonized reefs
(Chapter 3), and altered coral morphology (Done et al. 1991). When portions of these
massive corals die, they become substrate for other sessile organisms, including
crustose coralline algae, filamentous and macro- algae, and various corals, including
smaller massive, encrusting, branching, and plate-forming species (Done et al. 1991,
Gleason 1996, Galzin et al. In preparation). In Moorea lagoons, territory sizes can reach
several meters across (Done et al. 1991), with fish densities of up to 80 per square
meter (Gleason 1996).
Experimental Reefs
Matched pairs of control and experimental reefs were haphazardly distributed
within northeastern Aroa lagoon. Prior to beginning the study, I chose experimental
reefs using the following search image: large massive Porites patch reefs, colonized by
Stegastes nigricans, with ample branching Acropora (which are numerically rare in this
area relative to Pocillopora). Further, relatively isolated reefs were selected, to reduce
the likelihood of re-colonization following pulse removals of S. nigricans. Whenever I
found a suitable candidate reef, I searched the nearby area for another reef of similar
size, isolation, coral community structure (e.g., size distibutions of Acropora and
Pocillopora), and density of S. nigricans (Appendix G: Table G-1). For each reef, I
measured the reef footprint (maximum length x perpendicular width), reef height
(maximum and average), the water depth to lagoon floor, and distance to the three
nearest patch reefs, as a rough estimate of isolation. In addition, I estimated the habitat
composition of each reef by laying three transects perpendicular to the longest axis and
documenting the dominant cover under each 0.10 cm interval. Bottom cover categories
were combined as appropriate to form the following categories: live coral (identified to
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genus), filamentous algal turf, macroalgae (identified to genus, except cyanobacteria),
and dead coral and crustose coralline algae. Estimates of reef composition were made
once, at the beginning of the study; however, I estimated the number and size of all S.
nigricans throughout sampling (July 2006, April 2007, July 2007, April 2008).
Between March and July 2007, strong storms collapsed or overturned several
reefs, smashing delicate branching corals and reducing the sample size of large marked
colonies, in particular. In July, I added four additional reefs to compensate for large
colonies lost during the storms. The search protocol for these reefs was the same as
that described above; however, I chose reef pairs that were either very large, or that
contained high densities of branching corals, in order to meet the goal of increasing the
sample size of marked branching corals (Appendix G: Table G-1).
Demographic Monitoring
Between June 2006 and April 2008, I tagged and repeatedly measured and
photographed almost 700 individual corals from the genera Acropora (N=221) and
Pocillopora (N=458) during complete biannual censuses of 16 isolated S. nigricans
territories (terminating in July 2006, April 2007, July 2007, and April 2008). Individuals
were tagged using round aluminum Forestry tags affixed to the reef using nails and Z-
sparTM (a two-part epoxy: Splash-zone A788, Kopcoat, Pittsburgh, Pennsylvania, USA).
During each census, each individual was measured (linear length, width, and height of
average branch) and photographed. If an individual was partially overgrown by turf, I
noted an estimate of the percent of the skeleton covered by turf, and the presence (=1)
or absence (=0) of bleaching, obvious (skeletal) predation, or complete mortality.
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Life Table Response Experiment
Experimental reefs were selected in pairs based on reef size, location, abundance
of adult S. nigricans, and branching coral abundance. One reef from each pair was
randomly assigned to have S. nigricans removed (Appendix G: Table G-1). I removed
Stegastes using clove oil, a common fish anesthetic, after the July 2007 census. A
previous study indicated that high concentrations of clove oil could increase bleaching
and reduce growth for both Acropora and Pocillopora (Boyer et al. 2009). Therefore, I
used a low concentration of clove oil (7% in seawater), recorded the number of bottles
applied to a given removal reef, and applied the same amount to the control (‘Present’)
reefs to eliminate potential confounding effects (but on control reefs S. nigricans
individuals were allowed to recover, rather than being removed). Throughout the
experiment, any new Acopora or Pocillopora recruits were also marked, measured, and
photographed during each census.
Statistical Analyses
For all analyses, ‘Treatment’ refers to reefs with Stegastes nigricans naturally
PRESENT or experimentally REMOVED. ‘Period’ distinguishes between the 2006-07
observational period BEFORE removals occurred, versus the 2007-08 EXPERIMENTAL
period. We expect no differences between treatments in the ‘Period’ before removals
because there were no manipulations during that time; instead, this period controls for
(and quantifies) possible pre-existing differences among reefs. ‘Reef size’ isolates
differences due to differences in the size of experimental reefs (Appendix G: Table G-1).
For coral responses, ‘Previous Size’ is a continuous covariate testing whether the size
of a coral colony at the previous time step influences the likelihood of mortality or the
magnitude of change in size. In addition, I tested the interactions that were relevant for
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each response variable / subset of the data, as reported below. In general, the main
inference of interest is the ‘Treatment’ x ‘Period’ interaction, and I eliminated (only) non-
significant higher-order interactions (Zuur et al. 2009, P. 127) to respect the marginality
of lower-order terms (Nelder 1998). For all tests that assume that the error is normally
distributed, I assessed normality using Q-Q plots and evaluated equality of variance
using Levene’s test. For mortality estimates, which assume a binomial error distribution,
I assessed model fit graphically.
Reef attributes
I tested to be sure differences in the size of reefs (m2) were attributable to ‘Reef Pair’,
rather than ‘Treatment’ (i.e., that my blocking was effective), using a linear model
(Linear Model (LM), lm, R v. 2.9.2, Appendix G: Tables G-2 and G-3, Figure G-1). I
used a similar model, but with the added random effect of ‘Pair’, to assess differences in
the abundance of Stegastes nigricans BEFORE treatment implementation, while
accounting for variation associated with reef size (July 2006, April 2007, July 2007;
Appendix G: Table G-4 and G-5, Figure G-2). I used the same model to assess the
efficacy of removals after the EXPERIMENTAL period (i.e., whether reefs differed by
Treatment, rather than ‘Pair’ after removals) (April 2008; Appendix G: Table G-6 and G-
7, Figure G-3).
Mortality
Prior to assessing mortality, I restricted the data set to exclude fragmented
colonies and their progeny (i.e., single colonies that split into two or more smaller
colonies), as this would skew estimation of the size specific mortality rate (e.g., Hughes
1984). I assessed the frequency of mortality as a function of ‘Treatment’, ‘Period’,
‘Previous size’, and all of their two- and three-way interactions, as well as, an additive
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effect of ‘Reef size’. The full model was: Mortality ~ Treatment + Period + Previous Size
+Reef size + Treatment*Period + Previous Size*Period + Period*Previous Size +
Treatment*Period*Previous Size + σPAIR + σREEF, where σ designate random effects of
‘Pair’ (N=8) and ‘Reef’ (N=16) (Acropora, N=192; Pocillopora, N=381, Appendix H:
Table H-3 and H-4, Figures 4-1 and 4-2). In addition, I performed follow-up analyses for
relevant subsets of the data. For each genus (i.e., Acropora and Pocillopora,
independently), I examined the ‘BEFORE’ data in isolation to test whether mortality
differed among treatments or reefs prior to actual treatment implementation. For this
analysis, ‘Period’ was not relevant and the model was constrained accordingly. Thus,
the model for this data subset included ‘Treatment’, ‘Previous Size’, their interaction,
‘Reef Size’, and random effects of ‘Pair’ (N=6) and ‘Reef’ (N=12) (Acropora, N=66;
Pocillopora, N=134, Table H-5 and H6, Figures 4-1 and 4-2, respectively). In addition, I
examined the ‘PRESENT’ only reefs (across both periods), to test whether the mortality
rate varied between years within S. nigricans territories. For this test, ‘Treatment’ was
not relevant and the model included only ‘Period’, ‘Previous Size’, their interaction, ‘Reef
Size’, and the random effect of ‘Reef’ (N=16) (Acropora, N=94; Pocillopora, N=206;
Tables H-5 and H6, respectively). The random effect of ‘Pair’ was also omitted from this
model, as it is redundant without the reefs associated with the other treatment. Both of
these tests using reduced data sets provide verification of the experimental design and
evaluate the baseline mortality rates in the PRESENCE of S. nigricans; however, neither
evaluates the main inference of interest (the ‘Treatment’ x ‘Period’ interaction). For all
mortality models, I used a Generalized Linear Mixed Model (GLMM) (binomial
distribution, logit link) fit with the Laplace approximation (glmer, lme4 package, R v
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2.9.2). I performed Likelihood Ratio Tests (LRT) of the models defined a priori to isolate
which experimental variables best-predicted variation in the frequency of mortality for
the entire data set, as well as for relevant subsets of the data.
Change in size of corals
I followed the change in size of all corals, but excluded from analyses those
colonies that experienced complete mortality. Live areas (only) were measured for
colonies that underwent partial mortality. I also removed fragmented colonies from the
data set, as these skew the rate of negative growth in an artificial manner. Instead, I
report the sum and mean size of resulting fragmented colonies, as well as the average
number and size of fragmented daughter colonies, by ‘Treatment’ and ‘Period’ in Table
4-2.
I used a Linear Mixed Model (LMM) defined a priori to isolate which experimental
variables significantly affect the change in size of colonies (Δ Size = Size – Previous
Size) among and within reefs. For both Acropora (N=123) and Pocillopora (N=272), the
full model tested was: Change in Size ~ Treatment + Period + Previous Size + Reef size
+ Treatment*Period + Previous Size*Period + Period*Previous Size +
Treatment*Period*Previous Size + σPAIR (σREEF), where σ designate random effects of
Reef (N=16) and Pair (N=8) (Appendix H: Table H-7; Figure 4-3 and 4-4, respectively). I
also performed similar additional analyses, where I constrained the dataset to the
before period and present treatment only, using the same models reported for mortality
frequency above, but using LMMs to examine change in size (lme, nlme package, R v
2.9.2; Appendix H: Table H-8 and H-9; Figure 4-3 and 4-4). Because variability was not
constant between periods, I added a term to specify constant variance within (but not
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between) periods to all models that included ‘Period’ as a term (weights=varident
(form=~1|Period), lme, nlme package, R v 2.9.2).
Matrix Models
I compared size-specific demographic rates (e.g., survival, growth, and transition
rates – including looping (or stasis), shrinkage, fragmentation, and mortality, sensu
Hughes 1990) on reefs where S. nigricans is naturally present and experimentally
removed. Due to differences in sample sizes, the size classes estimated varied by
taxon, with one more size class for Pocillopora than for Acropora (Appendix I: Figure I-
1). As is standard for matrix population models, I computed the dominant eigenvalue of
the matrix (λ). Because corals have open populations, λ cannot be interpreted in the
usual way as an intrinsic population growth rate; instead, it is essentially a measure of
population decay and is expected to be less than 1.0 (i.e., recruits were not included in
this portion of the analysis). An estimated value of λ greater than 1.0 suggests that
fragmentation alone can maintain a growing population, with zero recruitment of new
genets from larvae (Hughes and Tanner 2000). I report the mean population decay (λ)
and 95% confidence intervals as an alternative summary of the previously described
continuous processes (see Appendix I: Tables I-2 through I-7 for transition matrices).
This approach integrates the effects of the (possibly size-dependent) changes in growth
and mortality between treatments and years into a summary measure of the effects on
overall population demography (Figure 4-5).
Recruitment and Fragmentation
Given the low rates of both fragmentation (Table 4-2) and recruitment (Table 4-3)
to experimental reefs, I refrained from formal testing and instead reported the raw
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counts, and mean size with 95 % Confidence Intervals (1.96 * standard error), and
made basic comparisons as outlined briefly below.
Results
Life Table Response Experiment
Acropora mortality
The effect of Stegastes nigricans ‘Treatment’ varied by experimental ‘Period’ for
Acropora (Figure 4-1), with mortality rates considerably higher on reefs where S.
nigricans were REMOVED (i.e., there was a significant ‘Treatment’ by ‘Period interaction’;
LRT, Χ2=11.51, df=1, P =0.0007; Appendix H: Tables H-1 & H-2). In the BEFORE period,
total mortality was low (7 - 15% across all size classes and both ‘Treatments’, Table 4-
2) and the model estimated that very small individuals (1.0 cm) incurred mortality at
relatively low levels (~ 10-30% on average) across experimental reefs (from both
treatments) (Figure 4-1). The estimated average mortality probability for Acropora was
higher on reefs in which Stegastes nigricans was REMOVED (~75 - 90%), relative to those
with S. nigricans PRESENT (~0-45%) (Figure 4-1).
In particular, the vulnerability of larger Acropora varied with the presence of S.
nigricans (‘Treatment’ by ‘Previous Size’ interaction; LRT, Χ2=4.74, df=1, P =0.03;
Appendix H: Table H-1). During the BEFORE period, large colonies (> ~12 cm previous
maximum length) all escaped mortality, although there were very few such colonies and
the estimates of mortality were uncertain (Figure 4-1). In contrast, mortality of large
colonies was 100% on reefs in which S. nigricans was REMOVED during the
EXPERIMENTAL period, when the sample size was also larger (Figure 4-1). Thus, in the
EXPERIMENTAL period total mortality of Acropora (across size classes) was nearly 5 times
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higher in removal (75%) relative to control/present (17%) reefs (Table 4-2; Appendix H:
Figure H-1).
The Acropora data from the BEFORE period showed no significant effect of
‘Treatment’ (LRT, Χ2=1.23, df=1, P =0.26) or any other factor tested (Appendix H: Table
H-3), confirming that mortality rates did not differ among reefs assigned to alternate
treatments prior to S. nigricans manipulations (Figure 4-1, Table 4-2). When the data
were constrained to examine the mortality probability of Acropora on reefs with S.
nigricans PRESENT only, there was a significant effect of ‘Previous size’ (LRT, Χ2=24.36,
df=1, P <0.0001), but the effect of 'Period' was not significant (nor were any other
factors, Appendix H: Table H-3). This suggests mortality pressure varied little across
years for Acropora (15% and 17%, respectively; Table 4-2). Despite an apparent size
refuge from predation in the presence of S. nigricans (Figure 4-1), corals may suffer
overgrowth by turf, causing individuals to shrink (see Change in Coral Size) or fragment
(see Fragmentation).
Pocillopora mortality
The results for Pocillopora were similar to those for Acropora, in that the effects of
Stegastes nigricans territorial defense varied between the BEFORE and EXPERIMENTAL
periods (‘Treatment’ by ‘Period’ interaction; LRT, Χ2=17.54, df=1, P <0.0001; Appendix
H: Tables H-1 and H-2). Across size classes, total mortality was approximately 3 times
higher on reefs with S. nigricans REMOVED (59%) versus PRESENT (17%) (Table 4-3).
The predicted mortality probability was higher for small individuals of Pocillopora (1 cm)
on reefs where S. nigricans was REMOVED relative to PRESENT during the EXPERIMENTAL
period (~75% and 30%, respectively; Figure 4-2). These differences were similar in
magnitude to the differences observed for Acropora (Figure 4-1). In contrast to the
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patterns observed for Acropora, removal of S. nigricans did not significantly affect the
mortality rates for larger Pocillopora and there was no significant interaction between
‘Previous size’ and ‘Treatment’ (Appendix H: Table H-1). There is, however, some
evidence that the mortality rates for Pocillopora were generally higher during the
EXPERIMENTAL period, including slightly higher mortality in the presence of S. nigricans
(i.e., total mortality increased from 6% to17%, Table 4-3). Thus, although there appear
to be higher overall mortality rates for Pocillopora in the EXPERIMENTAL period,
regardless of S. nigricans defense (Table 4-3), there were no differences between
periods when the data were constrained to the PRESENT treatment (Figure 4-2; Appendix
H: Table H-4). However, as for Acropora, larger corals have a lower probability of
mortality for Pocillopora when S. nigricans is PRESENT (Figure 4-2; ‘Previous size’, LRT,
Χ2=58.22, df=1, P<0.001; no effect of other factors tested, Appendix H: Table H-4). The
overall mortality rates of Pocillopora were low across reefs in the BEFORE period (6% -
12%, Table 4-3). When the data were constrained to examine the effects of S. nigricans
in the BEFORE period, there was no effect of ‘Treatment’ (LRT, Χ2=2.05, df=1, P=0.15) or
any other factor, reinforcing that the experimental design was also valid for Pocillopora
(Appendix H: Table H-4).
Fragmentation
I did not observe any fragmentation of Acropora on reefs with Stegastes nigricans
experimentally REMOVED. The five Acropora that fragmented were all located on reefs
with S. nigricans PRESENT and were of similar, relatively large size, with resulting
daughter colonies also of similar size (Table 4-4). The initial cause was presumably
predation, or some other stress, and fragmentation was maintained because turf
overgrowth segregated the fragments (pers. obs).
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No Pocillopora colonies fragmented during the BEFORE period across experimental
reefs (Table 4-4), despite the considerably larger number of colonies monitored (Table
4-3). Following the S. nigricans removals, six times more individuals fragmented on
removal (n=6) than control (n=1) reefs (Table 4-4).
Change in coral size
As with mortality, the experimental design was validated in that there was not a
significant effect of ‘Treatment’ on change in coral size when the data were constrained
to examine only the BEFORE period for both corals (Appendix H: Table H-5). Change in
size did vary as a function of ‘Previous size’ for both Acropora (LLM, F1,42=6.81, P=0.01)
and Pocillopora for this data subset (LLM, F1,106=9.33, P=0.003; Appendix H: Tables H-
6 and H-7, respectively). There was a decline in change in size with an increase in
previous size for both corals in the BEFORE period (Figures 4-3 and 4-4) and this may be
related to the strong storms during that time. Larger individuals can also be more
susceptible to fragmentation (Table 4-1) or mortality (Figures 4-1 and 4-2) and both
fragmented and dead individuals were excluded from these analyses (for details please
see Statistical Analyses).
Experimental change in Acropora size
In Moorea today, Acropora generally have very few large representatives in the
lagoon due to their slow recovery from earlier natural disturbances (Berumen and
Pratchett 2006). For this relatively delicate branching coral, the change in size-
dependent growth in the PRESENCE and REMOVAL of Stegastes nigricans diverged, as
expected, between the BEFORE versus EXPERIMENTAL periods. That is, the ‘Treatment’ by
‘Period’ by ‘Previous size’ interaction was significant for the full data set (LLM,
F1,100=18.61, P<0.0001; Appendix H: Table H-5). In the EXPERIMENTAL period, the
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trajectory of change in size as a function of previous size changed dramatically for both
treatments for Acropora. In the REMOVED treatment, only a few large individuals were
included in the analysis due to the high mortality rates (Figure 4-1). Those individuals
that survived (and did not fragment, Table 4-4) suffered considerable shrinkage (Figure
4-3).
When I examined the change in size of Acropora using data from the PRESENT
treatment in isolation, there was a significant ‘Period’ by ‘Previous Size’ interaction
(LLM, F1,67=13.48, P=0.0005; Appendix H: Table H-6). This suggests growth rates were
higher for Acropora within S. nigricans territories during the EXPERIMENTAL period (Figure
4-3). Although growth rates were lower in the before period, potentially due to a higher
storm frequency, the impact of S. nigricans removal was substantially higher than the
temporal variation in their presence (Figure 4-3).
Experimental change in Pocillopora size
Sample sizes of Pocillopora were more than twice that of Acropora, thereby
increasing confidence in growth estimates. Size-dependent growth varied according to
experimental period (‘Period’ effect, LLM, F1,250=4.85, P=0.03) and previous size (LMM,
F1,250=8.12, P=0.004). In this case, there was a slight decrease in change of size as a
function of previous size across both treatments, and considerably higher variation in
the EXPERIMENTAL period, versus the BEFORE period (Figure 4-4, Appendix H: Table H-5),
despite an almost doubling of the sample size. When I examined growth rates for
Pocillopora in the presence of S. nigricans (across both periods), there was a significant
effect of both ‘Previous Size’ (LMM, F1,162=11.00, P=0.001) and ‘Period’ (LMM,
F1,162=5.31, P=0.02). The small negative effect of previous size was consistent for both
constrained data sets (BEFORE period and S. nigricans PRESENT, Appendix H: Table H-
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7). This offers additional evidence that the design was valid. The significant effect of
‘Period’ when S. nigricans was present (Appendix H: Table H-7), as well as the higher
variation (despite higher sample sizes), does raise concerns about processes
constraining growth during the EXPERIMENTAL period.
Matrix Models
Matrix models corroborated that among reefs, on average, the rate of population
decline (λ) was slower in the presence of Stegastes nigricans, and increased, for both
Acropora and Pocillopora, when S. nigricans were removed (Figure 4-5). Further, there
was no significant difference in λ (+/- 95% C.I., see Table 4-6) between the two periods
for reefs with Stegastes nigricans present, despite changes in abiotic (storm) and biotic
(Acanthaster planci presence) factors (For transition matrices see Appendix I: Figures I-
2 to I-7).
Recruitment Patterns
Recruitment to experimental reefs was very low for Acropora regardless of ‘Period’
or ‘Treatment’ (Table 4-3). For Pocillopora, recruitment was similarly low for both
Treatments in the BEFORE period. In the EXPERIMENTAL period recruitment was
approximately ten times higher than in the BEFORE period for both reef treatments.
Discussion
I compared growth and survival of two recovering branching coral genera
(Acropora and Pocillopora) within S. nigricans territories versus reefs with S. nigricans
removed, and compared differences in key demographic rates to highlight factors
contributing to their differential recovery. Survival and growth of Acropora were
substantially higher inside S. nigricans territories across sizes. Mortality was low for
small sizes of Acropora and zero for larger individuals (> 15 cm) in the presence of
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Stegastes nigricans (Figure 4-1, Appendix H: Figure H-1). During the EXPERIMENTAL
period, juvenile Acropora suffered ~3 times higher mortality and nearly all (12/13 or
92%) of the large corals died on reefs with S. nigricans REMOVED (Figure 4-1).
Pocillopora also incurred less mortality in the presence of S. nigricans (Figure 4-2). For
both corals, there were no differences between treatments in the BEFORE period, which
confirms reefs did not differ prior to manipulations (see Results, Appendix H). For
Pocillopora, there were no differences between periods when I restricted the analyses
to only reefs with S. nigricans present. However, there was evidence the growth
trajectory varied between these periods for Acropora (Figure 4-3), potentially a
consequence of storm damage during the observational (BEFORE) period. Overall,
Acropora, and large individuals in particular, enjoyed reduced mortality, and higher
growth rates, in the presence of S. nigricans, despite the preponderance of turf.
Examination of the mean population decay rate (λ) corroborates these patterns and
both Acropora and Pocillopora experienced steep declines in λ with the removal of S.
nigricans (Figure 4-5).
Observed Community Response
In Moorea, Stegastes nigricans territories can occupy up to 45% of the back-reef
environment (Done et al. 1991; Gleason 1994). Following a series of disturbances in the
1980s on, disturbance-tolerant massive Porites were less affected and became the
dominant hermatypic coral in this system (Bouchon 1985; Berumen and Pratchett
2006), as has been observed at other disturbed sites in the West Pacific (Guam: Colgan
1987) and Indian Ocean (McClanahan et al. 2007). In addition, Pocillopora, which was
relatively rare in the system prior to these disturbances (Bouchon 1985), recovered
better, and is now more abundant than the once dominant Acropora (Berumen and
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Pratchett 2006). While Pocillopora is also more abundant within S. nigricans territories
than outside (Glynn and Colgan 1988; Done et al. 1991; Shima et al. 2008), the pattern
is not nearly as striking as for Acropora, which is rarely found today outside S. nigricans
territories in the backreef, except in areas of particularly high water flow (Galzin et al. In
preparation), or in the few existing aborescent Acropora thickets, which are colonized by
both S. lividus and S. nigricans (Mapstone et al. 2007). This differential recovery is likely
due to either (1) variation in post-settlement mortality, or (2) differential recruitment
processes. The first is plausible because Pocillopora is protected by tightly branching
morphology and a relatively dense skeleton, and was observed to be less affected by
fish predation (Chapter 2) than Acropora, which has a more fragile, spongy skeleton
(Veron 2000). Similarly, recruitment processes could contribute because the life history
strategies of these two genera differ substantially. Acropora is a broadcast spawner,
releasing relatively small ova in hermaphroditic bundles, development takes a couple of
weeks and cannot be extended as larvae do not feed and lack zooxanthellae (e.g.,
Hughes et al. 2002). In contrast, Pocillopora broods to the planula stage, releasing
large larvae that are competent to settle, but that also can delay settlement for months
because they harbor zooxanthellae, and are often asexually produced (e.g., Stoddart
1983; Hughes et al. 2002). While I did observe higher recruitment across experimental
reef types for this taxon in the EXPERIMENTAL period (Table 4-5), recruitment processes
are notoriously variable and longer-term measurements are required to make any
inference.
Differential Susceptibility to Predation
It is clear that, of the common genera in Moorea, Acropora is the most susceptible
to natural disturbances (Table 4-1). It appears they are also more susceptible to
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predators, given they experience a drastic loss when S. nigricans, and their associated
territorial defense, is removed (Figure 4-1). Within this system, the main coral predators
for Acropora include polyp-feeding butterflyfishes (Chaetodontidae), as well as skeletal
excavators, including triggerfishes (Balistidae) and pufferfishes (Tetradontidae) (pers.
obs.). S. nigricans reduces foraging rates of herbivores, including surgeonfish
(Acanthuridae) and parrotfish (Scaridae), as well as butterflyfishes (Chapter 2).
However, the corallivorous fishes that can inflict the damage observed (triggerfishes
and pufferfishes) are less common and considerably more shy than butterflyfishes and
thus their impact on corals in damselfish territories is difficult to quantify. Nevertheless, I
have observed S. nigricans successfully defend against these coral predators (e.g.,
Arothron meleagris and A. hispidus (Tetradontidae); Balistipus undulatus and Melicthys
vidua (Balistidae)), though several bites may be taken before the intrusion is
successfully thwarted. Thus, fish predation on coral can occur within territories, but at a
considerably reduced rate (See Appendix H for representative photos of predation
observed during each period: Figure H-3).
Pocillopora, on the other hand, is mostly fed upon by butterflyfishes, which do not
inflict skeletal damage (reviewed in Cole et al. 2008; Rotjan and Lewis 2008). Gleason
(1994) reported skeletal loss due to fish predation for juvenile Pocillopora. However,
when corallivores were presented with Acropora, Montipora, Pocillopora, and Porites
simultaneously on reefs with S. nigricans removed or naturally absent, only the delicate
acroporids incurred observable (i.e. skeletal) damage (Chapter 2). This lends further
credence that Pocillopora is less susceptible than Acropora to predation. For both taxa,
coral spat and small juveniles can also incur predation via non-discriminate foraging by
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herbivores (e.g., parrotfishes and surgeonfishes: Randall 1974, Bak and Engel 1979).
As these fish are also excluded by S. nigricans (Chapter 2), this type of predation is also
expected to be lower within territories.
Acropora and Pocillopora are also vulnerable to predation by the corallivorous
crown-of-thorns seastar, Acanthaster planci, although P. eydouxi, the most robust
Pocillopora species, is effectively protected by large crustacean exo-symbionts (C.S.
McKeon, pers. comm.), while other Pocillopora are protected less effectively (Glynn
1985). However, P. eydouxi was not included in analyses due to their rarity in the
lagoon. During 2008, an Acanthaster outbreak was underway in Moorea and we
observed several individuals within the lagoon near experimental reefs. Previous
research suggests that S. nigricans can defend against Acanthaster (Glynn and Colgan
1988); however, I did observe feeding by Acanthaster on some reefs with S. nigricans.
Further, the type of partial mortality incurred by Pocillopora on experimental reefs was
consistent with Acanthaster feeding mode (i.e., no skeleton loss, oval death zone of
appropriate size; See Appendix H for representative photos of predation observed
during each period: Figure H-4).
Both Acropora and Pocillopora are preferred food for Acanthaster (e.g, Saipan:
Goreau et al. 1972; Panama: Glynn et al. 1972, Porter 1972; and Hawaii: Chess et al.
1972), and preference appears to increase with prey availability (e.g., see Porter 1972
and Goreau et al. 1972). Pocillopora is more than twice as abundant as Pocillopora
(Tables 4-2 and 2-3) and attains larger sizes within territories (Figures 4-3 and 4-4). The
type of predation (Appendix H: Figure H-4), higher mortality, and variation in negative
growth experienced by Pocillopora during the experimental period is consistent with
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predation by Acanthaster. Whereas, both small and especially larger size classes of
Acropora were protected by S. nigricans defense consistently across both periods
(Figure 4-1). The differential predation pressure by Acanthaster may have been driven
by differences in prey availability (i.e., Pocillopora were larger and more abundant, thus
were targeted more frequently). If Acanthaster had not been present in the system, we
may not have seen the same degree of mortality on large Pocillopora.
Recruitment Failure
Acropora experienced very low levels of both asexual (Fragmentation, Table 4-2)
and sexual (Recruitment, Table 4-3) recruitment to experimental reefs. In combination
with the observed distribution of only small and denuded Acropora outside of territories
(unpubl. data), this suggests Acropora are highly susceptible to predation, and
associated population declines (Figure 4-5), in the absence of S. nigricans defense.
For Pocillopora, both fragmentation and recruitment were very low in the before
period (Table 4-2 and 4-3). During the experimental period, fragmentation (via partial
predation) increased substantially on reefs in which S. nigricans were removed, but not
where present. Interestingly, rates of ambient recruitment to both reefs increased
dramatically for Pocillopora in the experimental period, suggesting larval supply was
likely higher (given the poor survival of larger size classes on removal reefs, a reduction
of post-settlement mortality is not as likely of an explanation). Given Pocillopora brood,
reduced planktonic dispersal may also increase the probability those few individuals that
do survive may better contribute to the next generation (Knowlton 2001). However,
long-term recruitment studies are necessary before any inference can be made.
It seems Pocillopora has the advantage over Acropora of a stronger skeleton that
minimizes susceptibility to skeleton-damaging predation, though their susceptibility to
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predation by Acanthaster can be high without S. nigricans defense (Figure 4-2). In
Moorea, the intense predation pressure is likely the most important selective pressure,
as persistence of large colonies is expected to have the biggest impact on population
dynamics for long-lived, sessile species (Tanner and Hughes 2000) and future research
is warranted to tease apart the possible drivers of this high predation pressure.
Conclusions
A central goal in ecology is to understand the mechanisms underlying the
distribution and abundance of organisms well enough to predict population-level effects
of perturbations. The use of manipulative removals of a key engineer can identify the
mechanisms underlying documented community changes and provide a solid
foundation for understanding impacts within a community context (e.g., Paine 1969).
We can move toward a more predictive framework for non-trophic interactions (e.g.,
ecosystem engineers, mutualisms, etc.) by merging the interaction strength framework
commonly used in consumer-resource interactions (e.g., Paine 1992; Wootton 1997;
Berlow et al. 2005) and population-level measurements obtained using a Before-After-
Control-Impact design (Osenberg et al. 2006) within a Life table Response Experiment
framework (Caswell 2001). By comparing corals that vary in both disturbance-sensitivity
and recovery rates, it is possible to isolate factors that constrain community resilience.
This mechanistic understanding facilitates explorations of what processes are driving
the observed changes in community structure (Chapter 5).
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Table 4-1. General susceptibility of Acropora, Pocillopora, and Porites to natural
disturbances. Natural Disturbance
Documented (Relative) Susceptibility References
Acropora Pocillopora Porites Storm damage High Intermediate Low 1 Bleaching events High Intermediate Low 2 Acanthaster planci predation High Intermediate -
High* Low 3, 4
Destructive predation (fishes) High Intermediate Low 5
Overgrowth by algal turf Intermediate Low High 5 Notes: Natural disturbance is extended to include predation and competition with Stegastes nigricans-associated algal turf. References are not exhaustive but exemplary: 1Hughes 1989; 2Gleason 1993, 3Porter 1972, 4Goreau et al. 1972, 5White and O’Donnell In press. *This generalization excludes Pocillopora eyudouxi and depends upon whether colonies have large crustacean guards present (e.g., Glynn 1985, Pratchett 2001); In addition, preference appears to increase with prey availability (e.g., see Porter 1972 and Goreau et al. 1972).
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Table 4-2. Overall mortality patterns for all sizes of Acropora. Before Experimental Stegastes nigricans NMortality NTotal Rate NMortality NTotal Rate PRESENT 5 33 0.15 11 64 0.17 REMOVED 2 31 0.07 52 69 0.75 Notes: Measurements were repeated ‘Before’ manipulations (2006-2007) and during the ‘Experimental’ period (2007-2008) on reefs with Stegastes nigricans ‘Present’ and those from which S. nigricans were ‘Removed’. Please note that no S. nigricans were removed in the BEFORE period and, in this context, ‘Removed’ refers to reefs on which S. nigricans were scheduled to be removed during the EXPERIMENTAL period.
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Table 4-3. Overall mortality patterns for all sizes of Pocillopora. Before Experimental Stegastes nigricans NMortality NTotal Rate NMortality NTotal Rate PRESENT 4 71 0.06 23 137 0.17 REMOVED 8 68 0.12 68 116 0.59 Notes: Measurements were repeated ‘Before’ manipulations (2006-2007) and during the ‘Experimental’ period (2007-2008) on reefs with Stegastes nigricans ‘Present’ and those from which S. nigricans were ‘Removed’ (as in Table 4-2).
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Table 4-4. Record of fragmentation of corals by period and treatment Coral Period Stegastes
nigricans Num. of Ind. Fragmented
Mean Size of Ind. (cm)
Mean Num of Fragments (Total)
Mean Frag. Size
Acropora Before Present 0 NA (0) NA “Removed” 2 14.05 ± 4.18 3.0 ± 0.0 (6) 2.63 ± 2.45
Experimental Present 3 13.40 ± 7.34 4.3 ± 7.9 (13) 2.65 ± 3.12 Removed 0 NA (0) NA
Pocillopora Before Present 0 NA (0) NA “Removed” 0 NA (0) NA
Experimental Present 1 12.30 ± 0.00 2.0 ± 0.0 (2) 5.30 ± 4.16 Removed 6 14.05 ± 26.93 2.2 ± 0.8 (13) 3.66 ± 4.30
Notes: The number and mean size of Acropora or Pocillopora individuals that fragmented by ‘Period’ and ‘Stegastes nigricans’ treatment. In addition, I report the mean number of fragments (as well as the total number of fragments) and the mean size of fragments. For all mean values, 95% confidence intervals are reported as ± 1.96 * standard error. Please note that no S. nigricans were removed in the BEFORE period and, in this context, “Removed” refers to reefs on which S. nigricans were scheduled to be removed during the EXPERIMENTAL period.
105
Table 4-5. Record of coral recruitment to reefs by period and treatment Coral Period Stegastes
nigricans Num. of Recruits Mean Size of
Recruits (cm) Acropora Before Present 3 2.90 ± 0.36
“Removed” 0 NA Experimental Present 4 3.48 ± 1.0
Removed 2 4.30 ± 0.24 Pocillopora Before Present 2 1.90 ± 0.03
“Removed” 0 NA Experimental Present 30 2.24 ± 0.36
Removed 25 2.09 ± 0.36 Notes: The total number, and mean size, of Acropora or Pocillopora individuals that recruited to experimental reefs by ‘Period’ and ‘Stegastes nigricans’ treatment. For all mean values, 95% confidence intervals are reported as ± 1.96 * standard error. Please note that no S. nigricans were removed in the BEFORE period and, in this context, “Removed” refers to reefs on which S. nigricans were scheduled to be removed during the EXPERIMENTAL period.
106
Table 4-6. Overall λ values for Pocillopora and Acropora. Pocillopora Acropora
Stegastes nigricans Mean λ
min max Mean λ
min max
Before (Present) 0.96 0.89 0.99 1.03 0.86 1.20
Present 0.98 0.81 1.07 0.84 0.71 0.99
Removed 0.59 0.43 0.75 0.35 0.07 0.51
Notes: Matrice analyses were performed on all colonies for all reefs ‘Before’ manipulations (2006-2007, i.e., with Stegastes nigricans Present) and during the ‘Experimental’ period (2007-2008) on reefs with Stegastes nigricans ‘Present’ and those from which S. nigricans were ‘Removed’ (as in Table 4-2).
107
Figure 4-1. Mortality rates of Acropora. Mean mortality probability as a function of
previous maximum linear length (cm) during the ‘Before’ (2006-2007) and ‘Experimental’ (2007-2008) periods, between which clove oil was applied to reefs and the Dusky farmerfish, Stegastes nigricans, was allowed to recover (‘Present’, purple) or ‘Removed’ (gray) from half of each pair of experimental reefs. Points are jittered to reduce overlap and represent mortality, (=1) or survival (=0). The effect of S. nigricans ‘Treatment’ varied by experimental ‘Period’ for Acropora, with mortality rates considerably higher on reefs where S. nigricans were REMOVED (i.e., there was a significant ‘Treatment’ by ‘Period interaction’; LRT, Χ2=11.51, df=1, P =0.0007). In particular, the vulnerability of larger Acropora varied with the presence of S. nigricans (‘Treatment’ by ‘Previous Size’ interaction; LRT, Χ2=4.74, df=1, P =0.03; Appendix H: Tables H-1 & H-2).
108
Figure 4-2. Mortality rates of Pocillopora. Mean mortality probability as a function of
previous maximum linear length (cm) during the ‘Before’ (2006-2007) and ‘Experimental’ (2007-2008) periods, between which clove oil was applied to reefs and the Dusky Farmerfish, Stegastes nigricans, was allowed to recover (‘Present’, blue) or ‘Removed’ (gray) from half of each pair of experimental reefs. Points are “jittered” to reduce overlap and represent mortality, (=1) or survival (=0). The effects of S. nigricans on mortality varied between the BEFORE and EXPERIMENTAL periods, with higher mortality on reefs where S. nigricans were REMOVED (‘Treatment’ by ‘Period’ interaction; LRT, Χ2=17.54, df=1, P <0.0001; Appendix H: Tables H-1 and H-2).
109
Figure 4-3. Change in size (Delta) of Acropora as a function of previous maximum linear
length (cm) during the ‘Before’ (∆=Size2007-Size2006) and ‘Experimental’ (∆=Size2008-Size2007) periods, between which clove oil was applied to reefs and the Dusky Farmerfish, Stegastes nigricans, was allowed to recover (‘Present’, purple) or ‘Removed’ (gray) from half of each pair of experimental reefs. For Acropora, the change in size-dependent growth (of survivors) in the PRESENCE and REMOVAL of S. nigricans diverged, as expected, between the BEFORE versus EXPERIMENTAL periods, with considerably lower growth (higher shrinkage) when S. nigricans was REMOVED (i.e., the ‘Treatment’ by ‘Period’ by ‘Previous size’ interaction was significant for the full data set; LLM, F1,100=18.61, P<0.0001; Appendix H: Table H-5)
110
Figure 4-4. Change in size (Delta) of Pocillopora as a function of previous maximum
linear length (cm) during the ‘Before’ (∆=Size2007-Size2006) and ‘Experimental’ (∆=Size2008-Size2007) periods, between which clove oil was applied to reefs and the Dusky Farmerfish, Stegastes nigricans, was allowed to recover (‘Present’, blue) or ‘Removed’ (gray) from half of each pair of experimental reefs. For Pocillopora, size-dependent growth (of survivors) varied according to experimental period (‘Period’ effect, LLM, F1,250=4.85, P=0.03) and previous size (LMM, F1,250=8.12, P=0.004; Appendix H: Table H-5).
111
Figure 4-5. Mean population decay rate of Acropora and Pocillopora (λ ± 95% C.I.)
before manipulations (all reefs combined), as well as in the presence (control) and removal of the farmerfish, Stegastes nigricans.
CHAPTER 5 CONCLUSIONS
Coral reefs are declining worldwide due to natural and anthropogenic disturbances
(Bellwood et al. 2004, Hoegh-Guldberg et al. 2007). Stressors include terrigenous
runoff, nutrient pollution, overextraction by humans, and higher abiotic stress induced by
global change (Knowlton and Jackson 2008). Resilience and recovery rates vary, and
ecologists seek to understand the mechanisms influencing these processes. High cover
of macroalgae is an especially important proximate cause of coral decline, as it can
inhibit coral recruitment and survival (reviewed in McCook et al. 2001). Thus,
herbivorous fishes and urchins (which can suppress algal biomass via grazing) have
long carried a reputation for indirectly maintaining the abundance and diversity of reef-
building corals (Hixon 1997, Hughes et al. 2007). Although herbivory is well accepted as
a dominant process structuring coral reefs, it is important to differentiate two broad
behavioral groups of herbivorous coral reef fishes: mobile “foragers” versus site-
attached “farmerfish” (Ceccarelli et al. 2005) (Table 5-1). Foragers are generally larger,
herbivorous fishes that forage typically in loose single-or mixed-species schools over
relatively large home ranges (e.g., parrotfishes (Scaridae), surgeonfishes
(Acanthuridae), and rabbitfishes (Siganidae), Ceccarelli et al. 2005). Farmerfish are
smaller, highly territorial damselfish that cultivate preferred turf algae via active farming
and defense behaviors in restricted areas (Ceccarelli et al. 2001, 2005).
Farmerfish and foragers overlap in distribution but impact benthic communities in
fundamentally different ways (Ceccarelli et al. 2005). While all territorial damselfish
occupy defined areas which they actively defend from competitors and egg predators
(e.g., Ebersole 1977), only territorial algal “farmers” engineer the benthic structure of
coral reefs (reviewed in Ceccarelli et al. 2001). These farmerfish develop and maintain
conspicuous filamentous algal mats (i.e., turf) through a variety of behavioral
adaptations, including substratum preparation (killing coral and removing sediment),
“weeding” (selectively removing unpalatable algae), fertilizing (through defecation), and
reducing herbivory through active defense (Ceccarelli et al. 2001). The benthic algal
biomass (Hixon and Brostoff 1981, Hata and Nishihiri 2002, Hata et al. 2002), diversity
(Hixon and Brostoff 1983, 1996; Sammarco 1983), and productivity (Klumpp et al. 1987,
Lison de Loma and Ballesteros 2002) of filamentous algal turfs are higher within
farmerfish territories than in non-defended areas. With farmerfish removals, foraging
rates of mobile foragers increase in these gardens and turf cover declines rapidly
(Ceccarelli et al. 2001, Chapter 2), suggesting that territorial behavior is a key
determinant of the efficacy of benthic engineering. In contrast, experimental removals of
mobile foragers effectively enhances the abundance of fleshy and filamentous algae
(e.g., Lewis 1986, Hughes et al. 2007). Further, different species of foragers appear to
target specific taxa of algae (Mantyka and Bellwood 2007), and mixed assemblages are
more effective at maintaining low algal cover and promoting coral (Burkepile and Hay
2008).
Variable Outcomes of Farming Behaviors
In some Pacific reefs, there is a paradoxical pattern of higher recovery of
branching corals within algal farms of territorial damselfish (Panama: Wellington 1982;
Japan: Suefuji and van Woesik; Great Barrier Reef (GBR): Sammarco and Carleton
1981, Sammarco and Williams 1982; Moorea: French Polynesia: Done et al. 1991,
Gleason 1994; Tahiti, French Polynesia: Glynn and Colgan 1988). Generally, when
farmerfish inhabit arborescent branching corals of the genus Acropora, the corals suffer
from farming behaviors (e.g., biting coral tips to increase territory size) and associated
increased algal abundance (e.g., Kaufman 1977, Potts 1977, Knowlton et al.1988). After
a series of disturbances in Moorea, French Polynesia, the mortality risk for branching
Acropora and Pocillopora corals (via direct or incidental predation) was higher outside
territories than the mortality risk associated with algal overgrowth within territories
(Chapters 2 and 4). This pattern was also observed of Acropora in Okinawa, Japan,
following a bleaching event (Suefuji and van Woesik 2001). In Panama, coral zonation,
was reportedly controlled by another farmerfish (Eupomacentrus acapulcoensis) via
protection of Pocillopora (Wellington 1982). This indirect positive facilitation is opposite
to the typical (negative) interaction, in which live coral is reduced (and algae are
cultivated) (Ceccarelli et al. 2001). Indeed, in these same systems, there was a
detrimental impact on the other dominant hermatypic coral (Pavona in Panama:
Wellington 1982; Porites in Tahiti: Glynn and Colgan 1988, and Moorea: Done et al.
1991, Chapter 3; however there was no mention of other taxa in the short ‘Reef Site’
from Okinawa; Suefuji and van Woesik 2001). These patterns suggest that changes in
community structure, due to natural or anthropogenic disturbance, may change the
strength and direction of farmerfish engineering impacts. Further, species may respond
differently, due to variation in population dynamics and life history traits.
Farmerfish Effect Varies with Community Structure
Roughly half of all herbivorous damselfish farm algal turf (tallied from Ceccarelli et
al. 2001). These farmerfish function as ecosystem engineers (Jones et al. 1994),
although their roles apparently shift depending on community structure. In areas with
high coral cover and diversity (i.e., low disturbance sites), farmerfish are a nuisance
community member for the fast-growing arborescent Acropora because they reduce live
coral (e.g., Kaufman 1977, Potts 1977, Knowlton et al. 1988, Lison de Loma and
Ballesteros 2002). This could benefit other corals, in that their competitors are adversely
affected. In some disturbed communities, reefs have shifted from acroporid-dominated
(Acropora and Montipora) to a community structure dominated by disturbance-tolerant,
or fast-recovering ‘weedy’, coral species (e.g., Indian Ocean: McClanahan et al. 2007;
Moorea: Berumen and Pratchett 2006), due to differential susceptibility (Huston 1985),
thereby shifting the size and direction of the farmerfish effect. Colonization by farmerfish
negatively affects large corals that are amenable to turf-farming, e.g., Pavona and
Porites, by reducing cover of live coral (Wellington 1982, Done et al. 1991, Chapter 3).
However, some branching coral taxa may be necessary because they offer important
habitat structure for farmerfish, though this has only been tested explicitly in Panama
(Wellington 1982). The increased abundance of branching corals in these systems is
presumably due to a higher grazing rate outside territories (Panama: Pocillopora is
protected from pufferfishes, Wellington 1982; Okinawa: Acropora is protected from
urchin grazing, Suefuji and van Woesik 2001; Moorea, Acropora (Chapter 2 and 4) is
protected from corallivorous fishes, while Pocillopora is also protected from Acanthaster
planci (Chapter 4).
Expanding the Grazing Continuum
Recent studies across archipelagos indicate that changes in benthic reef
community structure can be clearly associated with changes in the composition and
trophic structure of coral reef fishes in both the Caribbean (Mora 2008) and the Pacific
(Friedlander and DeMartini 2002, Dulvy et al. 2004, DeMartini et al 2008, Sandin et al.
2008). Coral health is lower with lower biomass of top predators and corresponding
higher biomass of herbivorous fishes (Sandin et al. 2008). Similarly, the biomass of
farmerfish is higher in fished islands (DeMartini et al. 2008) and is negatively correlated
with predator biomass across U.S. reefs (Zgliczynski and Sandin, unpublished data). In
addition to cultivating algae, farmerfish effectively deter territory use by urchins
(Sammarco and Williams 1982, Mapstone et al. 2007) and large herbivorous and
corallivorous fishes (Ebersole 1977, Wellington 1982, Chapter 2). Thus, farmerfish
indirectly alter the magnitude and frequency of interactions for other community
members. For example, corals must contend with higher abundances of algal turf, but
enjoy reduced interactions with foraging herbivores and corallivores. Thus, large-scale
changes in fish community structure may predictably alter the magnitude and direction
of farmerfish engineering (i.e., the outcome of their engineering behaviors) on benthic
composition. That is, in the absence of high predation pressures, the high algal
abundance is expected to have a net negative effect; whereas, in the presence of high
corallivory or incidental predation on coral spat, turf-tolerant taxa may benefit from the
indirect protection of territorial defense (i.e., a net positive effect).
The observed differences in fish community structure highlights that different
processes can structure benthic communities. A recent meta-analysis of 54 field
experiments suggests grazers are the key determinant of algal abundance in nutrient
poor tropical systems and that the effects of nutrient enrichment are enhanced with
losses of herbivores (Burkepile and Hay 2006). Given variation in time since beginning
of fishing, grazing as a driver of community structure likely exists along a longer
continuum than previously considered. For example, in the Caribbean, marine protected
areas enhance the biomass of parrotfishes and increase grazing rates relative to
unprotected areas (Mumby et al. 2006) thereby indirectly facilitating higher coral
recruitment (Mumby et al. 2007). This is a classic example of an essentially grazer-
limited system, where ecologists expect herbivores to maintain coral dominance by
reducing algal biomass (e.g., Hay 1981; Hughes 1994; McCook 1996, 1999; Hughes et
al. 2007). Grazing by reef fishes is largely un-accepted as a process limiting coral
recovery, despite early reports (Darwin 1842, p. 14) and subsequent documented
changes in reef fish trophic structure (i.e., removal of piscivorous predators) that would
favor a prey release of coral predators and herbivores (e.g., Sandin et al. 2008).
Alternatively, high disturbance frequency may augment algal turf food resources (e.g.,
bleaching events, Gleason 1993), thereby supplementing herbivorous populations
(Hixon 1997) or facilitating differences in diet for facultative corallivores (e.g., Guzman
and Robertson 1989). However, there is evidence mounting that coral predation can
play an important regulatory role for coral community structure within Caribbean reefs,
including Belize (Littler et al. 1989) and the Florida Keys (Miller and Hay 1998); as well
as central Pacific coral reef communities: Hawaii (Frydl 1979, Jawardene et al. 2009),
Panama (Wellington 1982), Moorea, French Polynesia (White and O’Donnell, in press),
and outer zones of the Great Barrier Reef (Hoey and Bellwood 2008). Given farmerfish
can effectively exclude most other grazing fishes (Brawley and Adey 1977, Wellington
1982, Letourneur 2000, Chapter 2), increases in their abundance will further
concentrate foraging outside of territories (Steneck and Sala 2005).
Evidence Based Upon Research in Moorea
Darwin (1842) reports second hand (citing Mr Couthouy, p. 128-131) that at Tahiti
and Moorea (Eimeo) the space between reef and the shore has been nearly filled up by
the extension of those coral reefs (madrepores with tops of branches exposed =
Acropora), which within most barrier reefs merely fringe the land. Indeed, later reports
by Crossland (1928) corroborates that, historically, the most abundant reef-builders in
Tahiti and Moorea were corymbose Acropora, branching species of Pocillopora, and
Porites (though he notes Porites were ‘less important than conspicuous’, P. 722). As
late as 1979, Bouchon (1985) reports both Acropora and Porites dominated the reef flat
within Moorea lagoons, whereas, the fringing reef was already dominated by only
Porites. Since that time, coral reefs in French Polynesia suffered a series of natural
disturbances since the 1980s, including cyclones, bleaching events, and crown-of-thorn
seastar, Acanthaster planci, outbreaks (Berumen and Pratchett 2006). Within these
lagoons, the recovery of corals varies with the presence of a common territorial
farmerfish, Stegastes nigricans. There is lower cover of disturbance-tolerant massive
corals (Chapter 3), but higher abundances of recovering branching corals within
territories (Gleason 1994,1996; Done et al. 1991). Recent tests confirmed that corals
respond differently to S. nigricans presence: massive Porites experienced higher
mortality due to competition with turf, while branching Acropora and Montipora survived
and grew better in the presence of farmerfish due to corallivore and grazer exclusion
(Chapter 2).
Impacts will likely vary among life stages depending on vulnerability to competition
or predation / grazing impact, e.g., larger corals generally grow more slowly (depending
upon how you measure growth) and incur less mortality than smaller corals (Hughes
1990). Indeed, within given taxa different size classes can vary in their response. For
example, previous research suggests recruitment of branching Pocillopora is higher
within territories (Gleason 1994, 1996). However, a recent test found no evidence of a
farmerfish effect for the juvenile size class (Chapter 2). In addition, important
demographic rates may vary spatiotemporally, due to spatial or temporal differences in
physical (e.g., temperature, flow) or biological factors (e.g., corallivory or algal growth
rates). For example, in a test of the rate of turf overgrowth for massive Porites, the rate
varied dramatically within a given colony (~ 0 vs. 5 cm overgrowth in a six week period)
(Chapter 2, Figure 5-1). Overgrowth was lowest with manual sediment removal, and
highest under normal turf-associated sediment loads, i.e., in the absence of vermetid
snails, (Dendropoma spp.), which cast a mucus web and inadvertently remove sediment
from turf. This suggests that sediment is an important driver and that these
invertebrates may contribute to spatio-temporal variation in this rate of overgrowth by
indirectly reducing mortality associated with algal competition (Chapter 2).
Clearly, the snapshot approach of measuring interactions in one time and place
gives us little understanding of the true per capita effects on corals. To scale-up these
previously isolated mechanisms to the population level, I combined demographic field
surveys, experimental removals, and mathematical modeling. This isolated the
processes underlying higher growth and survival of two recovering branching coral
genera (Acropora and Pocillopora) within S. nigricans territories relative to outside. As
Pocillopora has recovered better than once dominant Acropora (Berumen and Pratchett
2006), comparing differences in key demographic rates may highlight factors limiting
recovery. Indeed, both Pocillopora and Acropora suffered significantly higher mortality
after the removal of Stegastes nigricans (Chapter 4). However, the effect was stronger
for Acropora, and only this taxa also suffered lower growth after removals (Chapter 4).
Whereas, Pocillopora suffered high mortality after removal of farmerfish, but also
suffered lower growth during the experimental period in the presence of farmerfish, and
it is likely both of these effects were driven by the presence of the crown-of-thorn
seastar (COTS) in the system, rather than corallivorous fishes. For example, when
nubbins of Pocillopora verrucosa and the more delicate acroporids (Acropora striata and
Montipora flowerii) were presented to corallivorous fishes on the same experimental
reefs, only the delicate acroporids suffered a reduction in skeletal mass due to predation
(Chapter 2, in 2005, prior to the COTS outbreak). This higher mortality and shrinkage
suggests the delicate skeletal structure is constraining recovery of Acropora in this high
grazing environment (Figure 5-1), while Pocillopora, with a dense lobed skeletal
structure, can tolerate the high grazing pressure (or is not preferred by corallivores) and
has a higher current distribution relative to historic records (Berumen and Pratchett
2006). By comparing coral species that vary in disturbance-sensitivity and recovery
rates in the presence and removal of the territorial farmerfish S. nigricans, I identified
that high grazing pressure on coral colonies may be constraining community resilience.
Thus, taxa with a higher resistance to competition with turf can utilize dead
substrata made available by farmerfish gardening. This increase in substrate
availability, when coupled with lower mortality rates, has led to enhanced recovery of
branching corals within farmerfish territories. Within the lagoon, in areas outside of
farmerfish territories, branching corals are relegated to high flow, or cracks and
crevices, suggesting grazing pressure is constraining recovery in the absence of this
ecosystem engineer. This system supports the idea that disturbance can alter the
engineering role. S. nigricans adversely affects branching corals in relatively
undisturbed habitats, but can offer a less stressful environment when there is a shift in
the community structure of grazing populations. Of course, this pattern is not expected
for all farmerfish species, as they may vary in their engineering impact. Good predictors
of engineering capacity (or magnitude of effect sizes) are: 1) large size and aggressive
territorial defense, 2) communal or shared defense, and 3) resulting large territory sizes.
Ideally, future research will take the ecological history into account and advocate a
precautionary, adaptive approach to management (e.g., Doak et al. 2008).
Table 5-1. Summary of differences between foraging and farming coral reef fishes. Character Foragers Farmers
Home range Varies; 10 to 100’s m square1,2 Small; 0-3 m square1,2
Diet Variable; Functional Redundancy1,3,4
Filamentous reds2
Size Larger (Post-Juvenile = 15-70 cm) 1,4
Smaller ( Post-Juvenile: 5-30 cm) 1,4
Reproduction Broadcast Spawners 1,4 Demersal Egg Layers 1,4
Lifespan Long? (20-40 years)1,4 Long (~20 years)1,4
Dominant Families
Acanthuridae (Surgeonfishes), Scaridae (Parrotfishes), & Siganidae (Rabbitfishes)
Pomacentridae (Damselfishes)
References: 1Randall 2005, 2Ceccarelli et al. 2001, 3Burkepile and Hay 2008, 4www.fishbase.org
Figure 5-1. Schematic of Stegastes nigricans direct and indirect interactions. Direct
(solid arrows) and indirect (dashed arrows) effects of the dusky farmerfish (Stegastes nigricans) documented on the north shore of Moorea, French Polynesia (Chapters 2, 3, and 4). The size of the arrow indicates the relative magnitude of the response: Net effects of farmerfish range from negative (grey) to positive (black) for massive Porites and branching Acropora coral, respectively, which is opposite their relative susceptibility to natural disturbances, such as predation, bleaching events, storm damage, or Crown-of-Thorn Seastar (COTS) break-outs.
APPENDIX A SAMPLING METHODS AND RESULTS CONCERNING EXPERIMENTAL REEF
CHARACTERISTICS PRIOR TO AND AFTER MANIPULATIONS
Methods
I identified and marked 32 reefs colonized by Stegastes nigricans (Figure A-2) and
8 interspersed reefs naturally devoid of S. nigricans and associated turf (i.e., healthy
Porites reefs, Figure A-2). Prior to any manipulations, I measured the density of S.
nigricans and physical characteristics of each reef, including: footprint (maximum length
and perpendicular width, cm), average and maximum heights (cm), water depth (cm),
distance to the three nearest neighbors (cm), and percent composition (using fixed point
contact, at 10 cm intervals, of 3 transects perpendicular to the longest reef axis). For
reef composition, corals living upon the reefs belonging to Acropora, Montipora, or
Pocillopora were combined into one category (Branching corals). Similarly, I combined
dead coral and crustose coralline algae into one category. Macroalgae were in very low
abundance on any reef type and I combined the following genera: Dictyota, Halimeda,
Turbinaria, and unidentified cyanobacteria.
Results
Table A-1. Physical factors of all reefs before manipulations (GLM) Physical Reef Characteristic Variable F value df Pr > F
Reef size (length x width) Treatment 0.49 4, 39 0.74 Depth to sand Treatment 1.94 4, 39 0.13 Average Height Treatment 1.19 4, 39 0.33 Maximum Height Treatment 1.24 4, 39 0.31 Reef isolation (avg. dist. to 3 nearest reefs)
Treatment 2.38 4, 39 0.07
Notes: Differences in average physical characteristics among experimental reefs prior to manipulations (PROC GLM, SAS 9.13). Mean values (± 95%CI) are reported in the Experimental Reefs section.
Table A-2. Composition of Stegastes Reefs before removals (GLM)
Benthic Category Variable F value df Pr > F Algal Turf Treatment (before) 1.03 3, 28 0.39 Porites spp. Treatment (before) 1.60 3, 28 0.21 Branching Corals Treatment (before) 0.17 3, 28 0.92 DeadCoral/ CrustoseCorallineAlgae
Treatment (before) 0.89 3, 28 0.46
Macroalgae Treatment (before) 0.77 3, 28 0.52 Notes: Differences in average (arc sine square root) benthic composition among Stegastes nigricans reefs prior to manipulations (PROC GLM, SAS 9.13). Benthic categories were arcsine squareroot transformed prior to analyses. The positive control reefs (i.e., those naturally devoid of Stegastes and Turf = Porites reefs) were not included as I expected differences due to the higher coral cover and absence of turf (Appendix A: Table A-3 and Figure A-2).
Table A-3. Comparisons of Stegastes and Porites reefs before removals (t-tests)
Benthic Category Variable t df Pr > t Algal Turf Reef Type 9.76 38 <0.0001 Porites spp. Reef Type 15.63 38 <0.0001 Branching Corals Reef Type 3.21 38 <0.003 DeadCoral/ CrustoseCorallineAlgae
Reef Type 1.27 38 0.21
Macroalgae Reef Type 0.51 38 0.61 Notes: Differences in average (arc sine square root) benthic composition betIen experimental and control reefs prior to manipulations (PROC TTEST, SAS 9.13) (Figure A-4). Reef type refers to reefs colonized by Stegastes nigricans (prior to any manipulations) versus control reefs (uncolonized by S. nigricans = Porites reefs). Benthic categories were arcsine square-root transformed. Sample sizes are not equal, but assumptions of normality and equal variance were met.
Table A-4. Composition of Stegastes Reefs after removals (GLM)
Benthic Category Variable F value df Pr > F Algal Turf Treatment (after) 10.25 3, 28 0.0001 Porites spp. Treatment (after) 1.61 3, 28 0.21 Branching Corals Treatment (after) 0.47 3, 28 0.71 DeadCoral/ CrustoseCorallineAlgae Treatment (after) 40.25 3, 28 <0.0001 Macroalgae Treatment (after) 3.17 3, 28 0.04 Notes: Differences in average (arc sine square root) benthic composition among Stegastes nigricans reefs after experimental manipulations (PROC GLM, SAS 9.13). Benthic categories were arcsine squareroot transformed prior to analyses. The positive control reefs (i.e., those naturally devoid of Stegastes and Turf = Porites reefs) were not compared in this analysis as I was testing the effects of the removal treatments and initial differences were already established (Table A-3 and Figures A-4 and A-5).
Figure A-1. Design schematic. A) Factorial manipulation of Stegastes nigricans and algal turf presence and removal on 32 colonized reefs. Naturally absent Porites reefs served as a positive control (N=8 for all treatments). B) For each of the 40 experimental reefs, we outplanted one of each sub-treatment (cage, cage control, and open) for each species (Acropora striata, Montipora floweri, Pocillopora verrucosa, and Porites australiensis) yielding 480 experimental nubbins total.
Figure A-2. Photographic example of experimental reefs. A) ‘Stegastes reef’ (N=32). B) ‘Porites reef’ (N=8). Nubbins were outplanted randomly by species and sub-treatment (orange flags).
Figure A-3. Photographic example of experimental coral nubbins. Each square represents the species x sub-treatments combinations that were outplanted to EACH experimental reef type (N=12 nubbins / reef).
Before Manipulations
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f Com
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Turf Porites Branching Corals Dead Coral and CCA Macroalgae
Figure A-4. Mean reef composition before removals. Mean percent benthic cover of
reefs (± 95% CI) by treatment prior to experimental manipulations (see Appendix A: Tables A2 & A3).
After Manipulations
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Turf Porites Branching Corals Dead Coral and CCA Macroalgae
Figure A-5. Mean reef composition after removals. Mean percent benthic cover of
experimental and control reefs (± 95% CI) one month after experimental manipulations (see Appendix A: Table A-4).
APPENDIX B TABLES AND FIGURES SUPPORTING THE EFFICACY OF REMOVAL
TREATMENTS
Table B-1. Density of adult Stegastes nigricans (GLMM) Effect F value df Pr > F
Treatment 45.91 4,314 <0.0001 Period 74.26 1,324 <0.0001 Notes: Differences in the average density of Stegastes nigricans among reefs throughout the experiment by fixed effects of ‘Treatment’ and ‘Period’ (before or after removals), and Day as a random effect as well as relevant contrasts within each main effect (PROC GLIMMIX, Poisson error distribution, SAS 9.13).
Table B-2. Contrasts for density of adult Stegastes nigricans (GLMM) Contrasts Estimate Range t value df Pr > t
Present vs Removed 7.3 5.3-9.9 12.56 314 <0.0001 Before vs After 0.5 0.5-0.6 -8.62 314 <0.001 Notes: Differences in the average density of Stegastes nigricans among reefs throughout the experiment by fixed effects of ‘Treatment’ and ‘Period’ (before or after removals), and Day as a random effect as well as relevant contrasts within each main effect (PROC GLIMMIX, Poisson error distribution, SAS 9.13).
Table B-3. Density of adult Stegastes nigricans before removals (Χ2).
Variable N X2 df P > X2 Stegastes densities BEFORE removals 667 0.84 3 0.84
Treatment
Count
Percent
Cumulative Count
Cumulative Percent
1 (Stegastes +/ Turf +) 172 25.8 172 25.8 2 (Stegastes +, Turf −) 159 23.8 331 49.6 3 (Stegastes −, Turf +) 163 24.4 494 74.1 4 (Stegastes −, Turf −) 173 25.9 667 100.0 5 (Stegastes , Turf )* 0 NA NA NA Notes: Chi square contingency analyses compare densities of adult Stegastes nigricans on treatment reefs ‘Before’ and ‘After’ removals (PROC FREQ, SAS 9.13).*Treatment 5 was not tested because cumulative counts across reefs and sampling observations were extremely low (0 and 1 in the before and after periods, respectively).
Table B-4. Density of adult Stegastes nigricans after removals (Χ2).
Variable N X2 df P > X2 Stegastes densities AFTER removals
1075 625.74 3 <0.0001
Treatment
Count
Percent
Cumulative Count
Cumulative Percent
1 (Stegastes +/ Turf +) 522 48.6 522 48.6 2 (Stegastes +, Turf −) 419 39.0 941 87.5 3 (Stegastes −, Turf +) 72 6.7 1013 94.2 4 (Stegastes −, Turf −) 62 5.8 1075 100.0 5 (Stegastes , Turf )* 1 NA NA NA Notes: Chi square contingency analyses compare densities of adult Stegastes nigricans on treatment reefs ‘Before’ and ‘After’ removals (PROC FREQ, SAS 9.13).*Treatment 5 was not tested because cumulative counts across reefs and sampling observations were extremely low (0 and 1 in the before and after periods, respectively).
Table B-5. Mean mass of dried algal turf (GLM)
Effect F value df Pr > F Coral 0.79 3, 418 0.50 Treatment 128.45 4, 418 <0.0001 Sub-Treatment 29.31 2, 418 <0.0001 Coral x Treatment 0.64 12, 418 0.81 Coral x Sub-Treatment 0.79 6, 418 0.58 Treatment x Sub-Treatment 7.21 8, 418 <0.0001 Coral x Treatment x Sub-Treatment 0.90 24, 418 0.60 Notes: Differences in mean mass of dried algal turf scraped from nubbins across coral species, treatments, sub-treatments, and all interactions (PROC GLM, SAS 9.13).
Figure B-1. Mean number of adult Stegastes nigricans (± 95 % C.I.). Removals
occurred at Day 0. Squares represent reefs with S. nigricans present while circles represent reefs with S. nigricans removed (or naturally absent). Symbol color designates the level of turf in each treatment: ambient (black), partially removed (grey), and naturally absent (light grey).
Figure B-2. Mean mass of dried algal turf (± 95 % C.I.). Algae was scraped from
the bases of nubbins at the termination of the experiment. Treatments included Stegastes nigricans present or removed, crossed with farmed algal turf present or removed and natural absent Porites reefs as a positive contol. On each reef, nubbins were placed in a full cage (black), partial cage (control=grey) or open (without cage=beige). Given the lack of differences among coral taxa tested (Appendix B: Table B3) we pooled these data to ease graphical presentation.
APPENDIX C EXPERIMENTAL METHODS, DETAILS, AND RESULTS FOR DAILY CHANGE IN
CORAL MASS
Methods
We used the buoyant mass technique (Davies 1989) to quantify the change in
skeletal mass of nubbins. At the termination of the experiment, we quantified surface
area of nubbins using the dye-dipping method (Hoegh-Guldburg 1988). The high
predation frequency in exposed and cage control sub-treatments (see Results)
restricted our use of this procedure to caged nubbins. The procedure was repeated
twice for each nubbin and the average of these values was then converted to surface
area based on a linear calibration curve (r2 = 0.99) derived from cylinders of known
surface area. We tested for an effect of surface on the calculated change in dry mass
for each species of caged nubbins and found insignificant or extremely weak
relationships. As a result, we have omitted surface area from our growth estimates and
instead report daily growth as the change in mass over the course of the experiment
(MassFinal – MassInitial / 32 days) by treatment.
Results
Table C-1. Daily coral growth (GLM) Variable F value df Pr > F
Coral 14.87 3, 418 <0.0001 Treatment 2.92 4, 418 0.02 Sub-Treatment 12.97 2, 418 <0.0001 Coral * Treatment 1.76 12, 418 0.05 Coral * Sub-Treatment 4.78 6, 418 <0.0001 Treatment * Sub-Treatment 1.79 8, 418 0.08 Coral * Treatment * Sub-Treatment 0.96 24, 418 0.52 Notes: Variation in skeletal growth/ loss among corals, treatments, sub-treatments, and all interactions (PROC GLM, SAS 9.13).
Table C-2. Tests of growth effect slices for each coral species (GLM). Effect Species F value df Pr > F
Coral * TTT* SUBTTT Acropora striata 3.26 14, 417 <0.0001 Coral * TTT* SUBTTT Montipora flowerii 3.63 14, 417 <0.001 Coral * TTT* SUBTTT Pocillopora verrucosa 0.88 14, 417 0.58 Coral * TTT* SUBTTT Porites australiensis 1.18 14, 417 0.28 Notes: Where TTT = Treatment and SUBTTT = Sub-Treatment (PROC GLM, SAS 9.13).
Table C-3. Daily growth of caged individuals (GLM)
Effect Species F value df Pr > F Treatment Acropora striata 0.48 4, 35 0.75 Treatment Montipora flowerii 0.58 4, 35 0.68 Treatment Pocillopora verrucosa 0.89 4, 35 0.48 Treatment Porites australiensis 0.90 4, 35 0.48 Notes: Variation in skeletal growth or loss in CAGED individuals (only) among experimental treatments by species (PROC MIXED, SAS 9.13).
Figure C-1. Mean daily coral growth rates (± 95% CI). A) Pocillopora verrucosa . B)
Porites australiensis. The average daily change in mass for each species is illustrated as a function of experimental treatment for Caged (black) versus Exposed (grey = Control + Open) nubbins.
APPENDIX D RESULTS OF FULL MODELS TESTING THE FREQUENCY OF PREDATION
AND OVERGROWTH
Table D-1. Predation frequency (Logisitic Regression). Taxon Variable Estimate ±S.E. Wald Χ2 df Pr > Χ2
Acropora striata
Stegastes -4.68 1.15 16.44 1 <0.0001 Stegastes − 0.037 1.07 0.0012 1 0.97 Turf -1.20 0.82 2.12 1 0.15 Caging -4.58 0.99 21.37 1 <0.0001 Exposure 1.25 0.86 2.11 1 0.15
Montipora flowerii
Stegastes -3.30 0.99 11.09 1 0.0009 Stegastes − -0.18 0.99 0.03 1 0.86 Turf -1.78 0.70 6.44 1 0.01 Caging -4.33 0.96 20.37 1 <0.0001 Exposure 0.97 0.64 2.26 1 0.13
Notes: Results of logistic regression isolating which experimental variables best predicted variation in predation frequency among and within reefs (PROC LOGISTIC, SAS 9.13). Pocillopora verrucosa and Porites australiensis each incurred zero skeletal predation across all treatments and sub-treatments and no analyses were performed.We used binomial (1 or 0) coding and dummy variables to isolate the comparisons of interest. ‘Stegastes’ refers to reefs with Stegastes present vs. removed or absent. ‘Stegastes −’ isolates differences between Stegastes removed and naturally absent reefs. ‘Turf’ isolates differences between reefs in which turf was present versus removed or naturally absent. ‘Caging’ refers to nubbins protected by cages vs. cage control and exposed nubbins. ‘Exposure’ isolates differences between cage control and exposed nubbins. Pocillopora verrucosa and Porites australiensis did not experience any predation.
Table D-2. Frequency of algal overgrowth (Logistic Regression) Taxon Variable Estimate ±S.E. Wald Χ2 df Pr > Χ2
Acropora striata
Stegastes 0.58 1.27 0.21 1 0.64 Stegastes − -1.36 1.44 0.88 1 0.35 Turf 1.94 0.84 5.47 1 0.02 Caging 0.91 0.81 1.28 1 0.25 Exposure 0.36 0.86 0.17 1 0.67
Montipora flowerii
Stegastes 2.41 1.12 4.65 1 0.03 Stegastes − 0.61 1.18 0.27 1 0.60 Turf 0.70 0.53 1.69 1 0.19 Caging 1.22 0.61 3.90 1 0.04 Exposure -0.24 0.69 0.11 1 0.73
Pocillopora verrucosa
Stegastes 10.39 216.7 0.002 1 0.96 Stegastes − 11.13 216.7 0.003 1 0.96 Turf 0.74 0.90 0.67 1 0.41 Caging 0.43 0.95 0.20 1 0.65 Exposure -0.75 1.25 0.35 1 0.55
Porites australiensis
Stegastes 1.42 0.84 2.86 1 0.09 Stegastes − 0.92 0.85 1.17 1 0.27 Turf 1.23 0.45 7.40 1 0.007 Caging 0.28 0.52 0.28 1 0.60 Exposure 0.28 0.52 0.28 1 0.60
Notes: Results of logistic regression isolating which experimental variables best predicted variation in the frequency of algal overgrowth of corals among and within reefs (PROC LOGISTIC, SAS 9.13). We used binomial (1 or 0) coding and dummy variables to isolate the comparisons of interest. ‘Stegastes’ refers to reefs with Stegastes present vs. removed or absent. ‘Stegastes −’ isolates differences between Stegastes removed and naturally absent reefs. ‘Turf’ isolates differences between reefs in which turf was present versus removed or naturally absent. ‘Caging’ refers to nubbins protected by cages vs. cage control and exposed nubbins. ‘Exposure’ isolates differences between cage control and exposed nubbins.
Table D-3. Turf abundance and coral overgrowth (Linear Regression)
Notes: Results of linear regressions testing the degree to which turf abundance explains variation in (arc sine square root transformed) algal overgrowth of corals (PROC REG, SAS 9.13).
Taxon R2 Adj. R2. F value df Pr > F Acropora striata 0.51 0.46 13.26 1, 13 0.003 Montipora flowerii 0.19 0.14 3.21 1, 13 0.10 Pocillopora verrucosa 0.04 -0.03 0.55 1, 13 0.47 Porites australiensis 0.56 0.53 16.56 1, 13 0.001
Figure D-1. Frequency of algal overgrowth for Pocillopora verrucosa. Mean
frequency of algal overgrowth (± 95% CI) for Pocillopora verrucosa as a function of Treatment and Sub-Treatment (Caged vs. Exposed=Cage control and Open).
APPENDIX E RESULTS OF FULL MODELS TESTING THE TERRITORIAL EFFORT EXPENDED BY
STEGASTES NIGRICANS AND RESPONSES BY IMPORTANT MOBILE FISHES (DENSITY, FORAGING, REEF USE)
Table E-1. Chase frequency (GLMM)
Notes: Differences in frequency of chases by Stegastes nigricans using a fixed effect of Reef Type’ (S. nigricans present, removed, or absent) and ‘Day’ as a random effect. Chase frequency was calculated as the sum of the number of reefs on which chases occurred divided by the number of reefs in that category and averaged through time (PROC GLIMMIX, SAS 9.13, binomial error distribution).
Effect F value Df Pr>F Reef Type 5.15 2,597 0.006
Table E-2. Contrasts of chase frequency (GLMM) Contrasts Estimate Range t
value df Pr > t
Absent vs Present 0.07 0.009-0.5 -2.62 597 0.009 Absent vs Removed 0.15 0.02-1.1 -1.84 597 0.07 Present vs Removed 0.47 0.2-0.9 -2.15 597 0.03 Notes: Differences in frequency of chases by Stegastes nigricans using a fixed effect of ‘Reef Type’ (Stegastes nigricans present, removed, or absent) and ‘Day’ as a random effect. Chase frequency was calculated as the sum of the number of reefs on which chases occurred divided by the number of reefs in that category and averaged through time (PROC GLIMMIX, SAS 9.13, binomial error distribution). Estimate refers to odds ratios with range indicating the 95% lower and upper confidence intervals.
Table E-3. List of species documented for each target fish family • Acanthuridae: Acanthurus nigrofuscus,Ctenochaetus binotatus, Naso lituratus
• Chaeodontidae: Chaetodon citrinellus, C. lunulatus, C. ornatissimus, C. reticulates, C. vagabundis
• Scaridae: Scarus altipinnis, S. oviceps, S. psittacus, S. sordidus
Table E-4. Densities of target families of coral reef fishes (GLMM)
Family Variable F value df Pr > F Acanthuridae (surgeonfishes) Reef Type 3.81 2,193 0.02 Chaetodontidae (butterflyfishes) Reef Type 2.94 2,193 0.06 Scaridae (parrotfishes) Reef Type 2.86 2,193 0.06
Notes: Densities of fishes were calculated as the mean number of the total individuals observed in a given fish family per reef per day. We tested fish density using a fixed effect of ‘Reef Type’ (Stegastes nigricans present, removed, or absent) and ‘Day’ as a random effect (after manipulations only: Day 0 – 30), for each taxonomic fish ‘Family’ (Acanthuridae, Chaetodontidae, and Scaridae) (PROC GLIMMIX, SAS 9.13, Poisson error distribution).
Table E-5. Contrasts of densities of target families of coral reef fishes (GLMM) Family Contrasts Est. Range t-value df Pr > t Acanthuridae Absent vs Present 1.22 1.0-1.5 2.13 193 0.03
(surgeonfishes) Absent vs Removed 1.00 0.8-1.2 0.03 193 0.98 Present vs Removed 1.21 1.0-1.4 2.53 193 0.01
Chaetodontidae Absent vs Present 0.55 0.3-1.1 -1.73 193 0.09 (butterflyfishes) Absent vs Removed 0.44 0.2-0.9 -2.40 193 0.01
Present vs Removed 1.24 0.8-1.9 1.00 193 0.31 Scaridae Absent vs Present 1.11 0.7-1.7 0.05 193 0.62
(parrotfishes) Absent vs Removed 0.76 0.5-1.1 -1.37 193 0.17 Present vs Removed 1.46 1.0-2.0 2.31 193 0.02
Notes: Differences in densities of fishes using a fixed effect of ‘Reef Type’ (Stegastes nigricans present, removed, or absent) and ‘Day’ as a random effect, for each taxonomic fish ‘Family’ (PROC GLIMMIX, SAS 9.13, Poisson error distribution). Densities of fishes were calculated as the mean number of the total individuals observed in a given fish family per reef per day. Estimate refers to the odds ratio. Range indicates the 95% lower and upper confidence intervals.
Table E-6. Reef use by target families of coral reef fishes (GLMM) Family Variable F value df Pr > F
Acanthuridae (surgeonfishes) Reef Type 30.13 2,197 <0.0001 Chaetodontidae (butterflyfishes) Reef Type 5.61 2,197 0.004 Scaridae (parrotfishes) Reef Type 29.03 2,197 <0.0001 Notes: Differences in frequency of reef use using a fixed effect of ‘Reef Type’ (Stegastes nigricans present, removed, or absent) and ‘Day’ as a random effect, for each taxonomic fish ‘Family’ (PROC GLIMMIX, SAS 9.13, binomial error distribution) with relevant contrasts reported below. During counts fish were assigned a microhabitat use code to designate the location of fish when sighted (Table 1). “Reef use” summarizes the frequency at which individuals were observed using dead portions of the reef, living coral, and turf (versus using the water column or sand / rubble / pavement substrates within 1 m of the reef base).
Table E-7. Contrasts of reef use by target families of coral reef fishes (GLMM) Family Contrasts Est. Range t-value df Pr > t Acanthuridae Absent vs Present 5.41 2.2-13.1 3.78 197 0.0002 (surgeonfishes) Absent vs Removed 0.17 0.06-0.4 -3.93 197 0.0001
Present vs Removed 31.82 13.2-77.0 7.72 197 <0.0001 Chaetodontidae Absent vs Present 0.64 0.2-2.5 -0.65 197 0.52 (butterflyfishes) Absent vs Removed 0.20 0.05-0.7 -2.50 197 0.01
Present vs Removed 3.25 1.4-7.7 2.71 197 0.007 Scaridae Absent vs Present 0.83 0.3-2.4 -0.35 197 0.73 (parrotfishes) Absent vs Removed 0.055 0.02-0.2 -5.56 197 <0.0001
Present vs Removed 14.96 6.8-32.9 6.77 197 <0.0001 Notes: Differences in frequency of reef use using a fixed effect of ‘Reef Type’ (Stegastes nigricans present, removed, or absent) and ‘Day’ as a random effect, for each taxonomic fish ‘Family’ (PROC GLIMMIX, SAS 9.13, binomial error distribution) with relevant contrasts reported below. During counts fish were assigned a microhabitat use code to designate the location of fish when sighted (Table 1). “Reef use” summarizes the frequency at which individuals were observed using dead portions of the reef, living coral, and turf (versus using the water column or sand / rubble / pavement substrates within 1 m of the reef base). Estimate refers to the odds ratio. Range indicates the 95% lower and upper confidence intervals.
Table E-8. Foraging frequency of target families of coral reef fishes (GLMM) Family Variable F-value df Pr > F Acanthuridae (surgeonfishes) Reef Type 9.48 2,197 <0.0001 Chaetodontida (butterflyfishes) Reef Type 6.01 2,197 0.002 Scaridae (parrotfishes) Reef Type 20.15 2,197 <0.0001 Notes: Differences in frequency of foraging by fishes using a fixed effect of ‘Reef Type’ (Stegastes nigricans present, removed, or absent) and ‘Day’ as a random effect, for each taxonomic fish ‘Family’ (PROC GLIMMIX, SAS 9.13, binomial error distribution). Each sampling period, observed individuals were noted as foraging (1) or not foraging (0).“Foraging” represents the frequency we observed individuals of a given family actively foraging according to treatment (n=8 reefs / treatment) throughout the experiment (n=5 sampling periods). Estimate refers to the odds ratio. Range indicates the 95% lower and upper confidence intervals.
Table E-9. Contrasts of foraging frequency of target families of reef fishes (GLMM) Family Contrasts Est. Range t-value df Pr > t Acanthuridae Absent vs Present 1.24 0.5-3.1 0.47 197 0.64 (surgeonfishes) Absent vs Removed 0.24 0.09-0.6 -3.01 197 0.002
Present vs Removed 5.16 2.4-11.3 4.12 197 <0.0001 Chaetodontidae Absent vs Present 0.76 0.2-2.7 -0.42 197 0.68 (butterflyfishes) Absent vs Removed 0.21 0.06-0.7 -2.56 197 0.01
Present vs Removed 3.61 1.5-8.6 2.91 197 0.004 Scaridae Absent vs Present 2.15 0.8-5.5 1.61 197 0.10 (parrotfishes) Absent vs Removed 0.17 0.07-0.4 -3.88 197 0.0001
Present vs Removed 12.2 5.4-27.3 6.10 197 <0.0001 Notes: Differences in frequency of foraging by fishes using a fixed effect of ‘Reef Type’ (Stegastes nigricans present, removed, or absent) and ‘Day’ as a random effect, for each taxonomic fish ‘Family’ (PROC GLIMMIX, SAS 9.13, binomial error distribution). Each sampling period, observed individuals were noted as foraging (1) or not foraging (0).“Foraging” represents the frequency we observed individuals of a given family actively foraging according to treatment (n=8 reefs / treatment) throughout the experiment (n=5 sampling periods). Estimate refers to the odds ratio. Range indicates the 95% lower and upper confidence intervals.
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APPENDIX F DETAILED METHODOLOGY FOR LAB AND FIELD OBSERVATIONS OF
COMPETITION BETWEEN PORITES AND ALGAL TURF
Table F-1. Test of average change in live Porites (LMM)
Data Variable numDF
denDF F-value Pr > F
Full dataset Treatment 3 21 3.33 0.04 Normal data only Treatment 3 15 3.28 0.05 Notes: Results of LMM to evaluate the average linear change in live Porites by ‘Treatment’ (lme (package: nlme), R v. 2.9.2). Treatments included a CONTROL (+Turf, +Sediment, -Vermetid snails); REMOVAL (-Turf, -Sediment,-Vermetid snails); SEDIMENT (+Turf, -Sediment,-Removals); and VERMETID (+Turf, +Sediment,+Vermetid) (See Table 3-1). This model included a random effect of ‘Quadrat’ nested within ‘Reef’. Note, the data were not normal and the analysis was repeated for the subset of the data that satisfied normality, with no change in the outcome, thus full model results are reported with confidence.
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Table F-2. Contrasts for change in live Porites (LMM) Comparison Effect DF t-value Pr > t Control vs. Removal Turf Effect 21 1.04 0.30 Control vs. Sediment Sediment Effect 21 2.27 0.03 Control vs. Vermetid Vermetid Effect 21 0.41 0.68 Notes: Results of LMM contrasts to isolate effects of interest on the average linear change in live Porites (see Table 3-1, lme (package: nlme), R v. 2.9.2). Treatments included a CONTROL (+Turf, +Sediment, -Vermetid snails); REMOVAL (-Turf, -Sediment,-Vermetid snails); SEDIMENT (+Turf, -Sediment,-Removals); and VERMETID (+Turf, +Sediment,+Vermetid).
159
Table F-3. Test of average change in bleaching front (LMM)
Data Variable numDF
denDF F-value Pr > F
Full data set Treatment 3 21 0.26 0.86 Notes: Results of LMM to evaluate the average linear change in live Porites by ‘Treatment’ (lme (package: nlme), R v. 2.9.2). Treatments included a CONTROL (+Turf, +Sediment, -Vermetid snails); REMOVAL (-Turf, -Sediment,-Vermetid snails); SEDIMENT (+Turf, -Sediment,-Removals); and VERMETID (+Turf, +Sediment,+Vermetid) (See Table 3-1). This model included a random effect of ‘Quadrat’ nested within ‘Reef’
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Figure F-1. Paired reef surveys: Reef Size. Mean reef volume (maximum length x
perpendicular width x average height ± 95% CI) of paired Porites reefs colonized by Stegastes nigricans (‘Colonized’) and uncolonized Porites reefs (‘Uncolonized’) did not differ significantly (t=1.87, df=22, P>0.05).
161
A) B)
C) D)
Figure F-2. Example photo quadrats from a sample experimental reef at Time=0. (A)
Treatment 1: −vermetid snails/+turf/+sediment (Control = Only Turf and Sediment; N=8). (B) Treatment 2: −vermetid snails/−turf/−sediment (All removed, N=9). C) Treatment 3: –vermetid snails/+Turf/−Sediment (Sediment removal, N=9). D) Treatment 4: +vermetid snails/+turf/+sediment (Vermetid snails present, N=7). Note in the removal treatment bands of thick and thin dead skeleton were evident when turf was removed, suggesting rates of overgrowth are not constant and there may be seasonal, in addition to spatial, variation in the rate of overgrowth.
162
Figure F-3. Schematic of line measurements for transition zone experiment. Yellow lines
illustrate representative measurements of combined turf and substrate (turf or dead coral). Red lines indicate length of substrate (turf or dead coral) alone. Small transparent red lines adjacent to the meeting point of these two lines estimated the size of the dead tissue zone. Linear measurements were taken from initial (Febuary 14th, 2007) and final (March 30th, 2007) photographs of each Treatment quadrat (see Table 3-1 and Figure F-2) randomly assigned to each experimental reef (N=9).
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APPENDIX G EXPERIMENTAL REEFS BEFORE AND AFTER FARMERFISH REMOVALS
Table G-1. Experimental reef characters BEFORE manipulations.
Pair Treatment Num
Reef Size (m2)
Mean STNI (± 95%C.I.) Acropora Pocillopora
A Present 1 13.87 18.3 ± 2.8 7 20 A Removed 17 12.59 15.0 ± 3.9 18 18 B Present 3 5.58 8.0 ± 1.1 5 21 B Removed 13 5.37 6.7 ± 1.3 6 5 C Present 4 4.68 6.0 ± 0.0 1 5 C Removed 5 4.10 6.7 ± 1.3 3 11 D Present 8 13.40 19.3 ± 0.7 6 25 D Removed 16 14.08 23.0 ± 0.0 9 22 E Present 15 3.13 6.7 ± 1.7 6 8 E Removed 9 3.08 6.7 ± 0.7 3 10 F Present 14 7.88 11.3 ± 1.3 5 14 F Removed 7 7.43 12.7 ± 0.7 8 15 G Present 22 9.78 21.5 ± 1.0 17 18 G Removed 24 13.54 22.0 ± 0.0 13 20 H Present 26 3.76 10.0 ± 0.0 17 26 H Removed 25 3.21 11.0 ± 0.0 9 15 Notes: ‘Pairs’ (A – H) of experimental reefs were randomly assigned to a Stegastes nigricans (STNI) ‘Treatment’. ‘Num’ is the arbitrary field designation for reefs. The main factors of interest were ‘Reef Size’ (length x width), mean number of adult STNI, and in situ abundances of Acropora (N=133) and Pocillopora (N=253) in July 2007, prior to farmerfish removals. The last two pairs (G & H) were added in July 2007, prior to manipulations, after storm damage reduced sample sizes of larger corals, in particular.
164
Table G-2. Differences in the average size of experimental reefs (LM) Variable DF Sum Sq Mean Sq F-value Pr > F Treatment 1 0.37 0.37 0.31 0.59 Pair 7 274.74 39.25 33.52 0<0.0001 Residuals 7 8.20 1.17 Notes: Differences in the average size of experimental (length x width, m2) as a function ‘Treatment’ (Stegastes nigricans PRESENT versus REMOVED) and ‘Pair’ (A-H; N=8; see Table G-1, G-5) (Linear Model (LM), lm, R v. 2.9.2).
165
Table G-3. Reef size model estimates (LM). Variable Estimate Std.Error t-value Pr > t Pair A 13.38 0.81 16.49 <0.0001 Pair B -7.76 1.08 -7.17 0.0001 Pair C -8.84 1.08 -8.17 <0.0001 Pair D 0.51 1.08 0.47 0.65 Pair E -10.12 1.08 -9.36 <0.0001 Pair F -5.58 1.08 -5.15 0.001 Pair G -1.57 1.08 -1.45 0.19 Pair H -9.75 1.08 -9.01 <0.0001 Treatment:Present -0.30 0.54 -0.56 0.59 Notes: Estimates of differences in reef size (length x width, m2) as a function ‘Treatment’ (Stegastes nigricans PRESENT versus REMOVED’) and ‘Pair’ (A-H; N=8; see Tables G-1 and G-2) (Linear Model (LM), lm, R v. 2.9.2).
166
Table G-4. Average density of Stegastes nigricans before removals (LMM). Variable numDF denDF F-value Pr > F Treatment 1 7 0.09 0.77 Pair 7 7 68.21 <0.0001 Notes: Differences in the density of adult Stegastes nigricans on experimental reefs ‘Before’ removals as a function ‘Treatment’ (‘Stegastes nigricans PRESENT versus REMOVED) and ‘Pair’ (A-H; N=8; see Tables G-1, G-2, and G-3), with ‘Reef’ as a random effect (Linear Mixed Model (LMM), lme, R v. 2.9.2).
167
Table G-5. Stegastes nigricans density estimates before removals (LMM) Variable Estimate Std.Error df t-value Pr > t Pair A 0.93 0.16 7 5.91 0.006 Pair B 1.33 0.21 7 6.37 0.004 Pair C 1.91 0.21 7 9.11 <0.0001 Pair D -0.04 0.21 7 -0.18 0.87 Pair E 3.07 0.21 7 14.67 <0.0001 Pair F 0.68 0.21 7 3.27 0.01 Pair G 0.16 0.21 7 0.73 0.49 Pair H 2.66 0.21 7 12.68 <0.0001 Treatment: Present 0.03 0.10 7 0.30 0.77 Notes: Estimates of differences in density of adult Stegastes nigricans during the observation period (i.e., ‘Before’ removals) as a function ‘Treatment’ (Stegastes nigricans PRESENT versus REMOVED) and ‘Pair’ (A-H; N=8; see Tables G-1 through G-4), with ‘Reef’ as a random effect (Linear Mixed Model (LMM), lm, R v. 2.9.2).
168
Table G-6. Average density of Stegastes nigricans after removals (LMM) Variable numDF denDF F-value Pr > F Treatment 1 7 26.82 0.001 Pair 7 7 055 0.78 Notes: Differences in the density of adult Stegastes nigricans on reefs at the termination of the ‘Experimental’ period (i.e., after farmerfish were removed) as a function ‘Treatment’ Stegastes nigricans PRESENT versus REMOVED) and ‘Pair’ (A-H; N=8; see Tables G-1 through G-5) (Linear Model (LM), lm, R v. 2.9.2).
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Table G-7. Stegastes nigricans density estimates after removals (LMM) Variable Estimate Std.Error t-value Pr > t Pair A 0.06 0.48 0.13 0.90 Pair B -0.08 0.64 -0.12 0.91 Pair C -0.25 0.64 -0.39 0.71 Pair D 0.14 0.64 0.21 0.83 Pair E 0.23 0.64 0.36 0.72 Pair F -0.13 0.64 -0.20 0.85 Pair G 0.26 0.64 0.40 0.69 Pair H 0.82 0.64 1.30 0.23 Treatment: Present 1.62 0.32 5.18 0.001 Notes: Estimates of differences in abundance of adult Stegastes nigricans at the termination of the ‘Experimental’ period (i.e., after farmerfish were removed) as a function ‘Treatment’ (Stegastes nigricans PRESENT versus REMOVED) and ‘Pair’ (A-H, see Table G-1, G-2), with ‘Reef’ as a random effect (Linear Mixed Model (LMM), lm, R v. 2.9.2).
170
Figure G-1. Mean size of experimental reefs. Mean reef size (length x width, m2; ± 95%
C.I.) did not differ between ‘Treatment’ (F1,7=0.31, P=0.59) but size did vary by ‘Reef Pair’ (Appendix G: Tables G-2 and G-3). Measurements were taken at the end of the BEFORE observational period (i.e., prior to experimental removals July 2007, N=8 reefs per Treatment).
171
Figure G-2. Mean density of Stegastes nigricans before removals. Mean density of adult
farmerfish (± 95% C.I.) on experimental reefs did not differ throughout the observational period (i.e., prior to experimental removals, July 2006 - July 2007, N=6 reefs per Treatment; Appendix G: Tables G-4 and G-5).
172
Figure G-3. Mean density of Stegastes nigricans at the termination of the experiment.
Mean density of adult farmerfish (± 95% C.I.) was significantly lower on reefs with S. nigricans removed (i.e., at the termination of the ‘Experimental’ period, April 2008, N=8 reefs per Treatment; Appendix G: Tables G-6 and G-7).
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APPENDIX H POPULATION MEASURES FOR ACROPORA AND POCILLOPORA IN THE
PRESENCE AND REMOVAL OF FARMERFISH
Table H-1. Mortality frequency for Acropora & Pocillopora (GLMM, LRT). Taxon Variable ΔlogLik Χ2 df Pr > Χ2
Acropora Treatment 6.31 12.61 1 0.0003 Period 2.29 4.58 1 0.03 Previous Size 59.92 119.84 1 <0.0001 Reef Size -0.05 0.00 1 1.00 Treatment:Period 5.75 11.51 1 0.0007 Treatment:Previous Size 2.37 4.74 1 0.03 Period:Previous Size 0.001 5e-04 1 0.98 Treatment:Period:Previous Size 1.02 2.03 1 0.15
Pocillopora Treatment 7.60 15.18 1 <0.0001 Period 3.00 6.00 1 0.01 Previous Size 74.79 149.59 1 <0.0001 Reef Size 0.43 0.86 1 0.36 Treatment:Period 8.77 17.54 1 <0.0001 Treatment:Previous Size 0.58 1.16 1 0.28 Period:Previous Size 1.43 2.68 1 0.10 Treatment:Period:Previous Size 0.22 0.44 1 0.51
Notes: Results of Likelihood Ratio Tests (LRT) using backward reduction of the full Generalized Linear Mixed Model (GLMM) defined a priori to isolate which experimental variables best predicted variation in the frequency of mortality among and within reefs. For both Acropora (N=192) and Pocillopora (N=381), the full model tested was: Mortality ~ Treatment + Period + Previous Size +Reef size + Treatment*Period + Previous Size*Period + Period*Previous Size + Treatment*Period*Previous Size + σPAIR + σREEF, where σ designate random effects of Pair (N=8) and Reef (N=16) (glmer, lme4 package, binomial distribution, logit link, fit with Laplace approximation, R v 2.9.2). ‘Treatment’ refers to the presence or removal of Stegastes nigricans from experimental reefs (during ‘experimental’ period only). ‘Period’ distinguishes between the 2006-07 observational period before removals occurred (versus the 2007-08 experimental period). ‘Previous Size’ is a continuous covariate testing whether the size of an individual at the previous time step influences the likelihood of mortality. ‘Reef size’ isolates differences due to increases in the size of experimental reefs (Appendix G: Table G-1). In addition, we tested all interactions of the factors of interest (Treatment, Period, and Previous Size). Significant interactions and all main effects were retained in the final model (Table H-4).
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Table H-2. Mortality frequency model estimates (GLMM).
Taxon Variable Estimate ±S.E. z value df Pr > z Acropora Before (Present,Size=1.0) -0.89 0.93 -0.95 1 0.34
Treatment (Removed) -2.86 1.04 -2.72 1 0.006 Period (Experimental) 0.61 0.66 0.92 1 0.36 Previous size -0.14 0.08 -1.88 1 0.06 Reef size 0.01 0.06 0.21 1 0.83 TTTRemoved:PERIODExptal 3.11 1.06 2.91 1 0.003 TTTRemoved:Previous size 0.17 0.09 1.85 1 0.06
Pocillopora Before (Present,Size=0) -1.79 0.70 -2.56 1 0.01 Treatment (Removed) 0.90 0.59 -1.51 1 0.13 PERIOD (Experimental) 1.34 0.68 1.97 1 0.05 Previous size -0.06 0.04 -1.42 1 0.16 Reef size -0.06 0.04 -1.60 1 0.11 TTTRemoved:PERIODExptal 1.25 0.74 1.70 1 0.09 PeriodExptal:Previous Size 0.003 0.05 0.08 1 0.94
Notes: Parameter estimates for final GLMM logistic regressions used to isolate which experimental variables best predicted variation in the frequency of mortality among and within reefs (Wald z, Χ2 distribution). For Acropora (N=65), the final model was: Mortality ~ Treatment + Period + Previous Size +Treatment*Period + Previous Size*Period + Reef size + σPAIR + σREEF, where σ designate random effects of Pair (N=8) and Reef (N=16) (glmer, lme4 package, binomial distribution, logit link, R v 2.9.2, Table H-3). For Pocillopora (N=134), the model was the same, but did not contain the ‘Period*Previous Size’ interaction (please see Table H-3). ‘Before (Stegastes)’ establishes reefs with Stegastes present in the before period as a baseline (Size=0, Intercept).‘Treatment (Removed)’ isolates differences between Stegastes removed and naturally present reefs. ‘Period (Experimental)’ isolates differences between the before and experimental periods. ‘Previous size’ refers to differences due to increases in the previous size of individuals. ‘Reef size’ isolates differences due to increases in the size of experimental reefs (Appendix G: Table G-1). Abbreviations: TTT=Treatment and Exptal=Experimental.
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Table H-3. Follow-up mortality analyses for Acropora (GLMM, LRT)
Subset Variable ΔlogLik Χ2 df Pr > Χ2 Acropora BEFORE ONLY
Treatment 0.61 1.23 1 0.26 Previous Size 1.04 2.08 1 0.15 Reef Size 0.01 0.01 1 0.92 Treatment:Previous Size 0.04 0.09 1 0.77
Acropora PRESENT ONLY
Period 0.39 0.77 1 0.38 Previous Size 12.18 24.36 1 <0.001 Reef Size 0.51 2.42 1 0.12 Period:Previous Size 0.64 1.29 1 0.26
Notes: Results of Likelihood Ratio Tests (LRT) using backward reduction of the GLMM models defined a priori to isolate which experimental variables best predicted variation in the frequency of mortality for select subsets of the data. For Acropora in the before period only (both treatments) (N=65), the full model tested was: Mortality ~ Treatment + Previous Size +Reef size + Previous Size*Period + σPAIR + σREEF, where σ designate random effects of Pair (N=6) and Reef (N=12). For Acropora within reefs with Stegastes nigricans present only (N=94), the full model tested was: Mortality ~ Period + Previous Size +Reef size + Previous Size*Period + σPAIR + σREEF, where σ designate random effects of Reef (N=8) (Note: Pair was omitted, as it is redundant without the other Treatment). I used logistic regression for both models (glmer, lme4 package, binomial distribution, logit link, fit with Laplace approximation, R v 2.9.2).‘Treatment’ refers to the presence or removal of Stegastes nigricans from experimental reefs. ‘Period’ distinguishes between the 2006-07 observational period before removals occurred (versus the 2007-08 experimental period). ‘Previous Size’ is a continuous covariate testing whether the size of an individual at the previous time step influences the likelihood of mortality. ‘Reef size’ isolates differences due to increases in the size of experimental reefs (Appendix G: Table G-1).In addition, I tested all interactions of the relevant of interest for each subset of the data.
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Table H-4. Follow-up mortality analyses for Pocillopora (GLMM, LRT)
Subset Variable ΔlogLik Χ2 df Pr > Χ2 Pocillopora BEFORE ONLY
Treatment 1.03 2.05 1 0.15 Previous Size 1.60 3.20 1 0.07 Reef Size 0.17 0.34 1 0.56 Treatment:Previous Size 0.13 0.26 1 0.61
Pocillopora PRESENT ONLY
Period 0.39 0.78 1 0.38 Previous Size 29.11 58.22 1 <0.0001 Reef Size 0.00 1e-04 1 0.99 Period:Previous Size 0.05 0.10 1 0.75
Notes: Results of Likelihood Ratio Tests (LRT) using backward reduction of the GLMM models defined a priori to isolate which experimental variables best predicted variation in the frequency of mortality for select subsets of the data. For Pocillopora in the before period only (both treatments) (N=134), the full model tested was: Mortality ~ Treatment + Period + Previous Size +Reef size + Previous Size*Period + σPAIR + σREEF, where σ designate random effects of Pair (N=6) and Reef (N=12). For Pocillopora within reefs with Stegastes nigricans present only (N=206), the full model tested was: Mortality ~ Treatment + Period + Previous Size +Reef size + Previous Size*Period + σPAIR + σREEF, where σ designate random effects of Reef (N=8) (Note: Pair was omitted, as it is redundant without the other Treatment). I used logistic regression for both models (glmer, lme4 package, binomial distribution, logit link, fit with Laplace approximation, R v 2.9.2).‘Treatment’ refers to the presence or removal of Stegastes nigricans from experimental. ‘Period’ distinguishes between the 2006-07 observational period before removals occurred (versus the 2007-08 experimental period). ‘Previous Size’ is a continuous covariate testing whether the size of an individual at the previous time step influences the likelihood of mortality. ‘Reef size’ isolates differences due to increases in the size of experimental reefs (Appendix G: Table G-1).In addition, I tested the interactions of interest for each subset of the data.
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Table H-5. Differences in final size of Acropora and Pocillopora (LMM).
Taxon Variable Est.
S.E.
numDF
denDF
F-value Pr > F
Acropora Before (Present,Size=1.0) 2.06 0.78 1 101 14.30 0.0003 Treatment (Removed) -0.51 0.93 2 6 14.89 0.008 Period (Experimental) -1.98 0.94 1 101 10.81 0.001 Previous Size -0.11 0.05 1 101 70.99 <0.000
1 Reef Size 0.04 0.05 1 6 0.21 0.66 Treatment:Period 6.92 1.51 1 101 38.07 <0.000
1 Treatment:Previous Size 0.03 0.08 1 101 131.1
3 <0.000
1 Period:Previous Size 0.24 0.07 1 101 13.30 0.0004 Treatment:Period:Previous Size -1.20 0.11 1 101 116.6
1 <0.000
1 Pocillopora Before (Present,Size=1.0) 1.20 0.60 1 250 3.33 0.07
Treatment (Removed) -0.27 0.65 1 6 0.06 0.81 Period (Experimental) -0.80 0.83 1 250 4.85 0.03 Previous Size -0.06 0.03 1 250 8.12 0.004 Reef Size 0.02 0.04 1 6 0.24 0.64 Treatment:Period -1.27 1.38 1 250 0.50 0.48 Treatment:Previous Size -0.01 0.04 1 250 0.63 0.43 Period:Previous Size -0.02 0.05 1 250 1.31 0.25 Treatment:Period:Previous Size 0.15 0.08 1 250 3.42 0.07
Notes: Results of the Linear Mixed Model (LLM) defined a priori to isolate which experimental variables best-predicted variation in the final size of individuals (max length, cm) among and within reefs. For both Acropora (N=122) and Pocillopora (N=272), the full model tested was: Size ~ Treatment + Period + Previous Size + Reef size + Treatment*Period + Previous Size*Period + Period*Previous Size + Treatment*Period*Previous Size + σPAIR (σREEF), where σ designate random effects of Reef (N=16) nested within Pair (N=8) (lme, nlme package, R v 2.9.2). The ‘Intercept’ refers to differences for very small (Size=0) individuals. ‘Treatment’ refers to the presence or removal of Stegastes nigricans from experimental reefs (which occurred during the ‘experimental’ period only). ‘Period’ isolates differences in size between the 2007-08 experimental period, and the 2006-07 observational period (before removals occurred). ‘Previous Size’ is a continuous covariate isolating differences in the final size due to the size of an individual at the previous time step. ‘Reef size’ isolates differences due to increases in the size of experimental reefs (Table G-1). In addition, we tested all interactions of the factors of interest (Treatment, Period, and Previous Size). Please note, because variability was not constant between periods, I added a term to specify constant variance within (but not between) periods (weights=varident(form=~1|Period)).
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Table H-6. Follow-up change in size analyses for Acropora (LMM)
Subset Variable Est.
S.E.
numDF
denDF
F-value Pr > F
Acropora BEFORE ONLY
Before (Present,Size=0) 2.44 0.86 1 42 19.43 0.0001 Treatment -0.43 0.94 1 3 1*10-6 0.99 Previous Size -0.11 0.04 1 42 6.81 0.01 Reef Size -0.006 0.06 1 3 0.02 0.90 Treatment:Previous Size 0.03 0.08 1 42 0.12 0.73
Acropora PRESENT ONLY
Before (Present,Size=0) 2.43 0.81 1 67 30.01 <0.0001 Period -2.06 0.93 1 67 1.07 0.30 Previous Size -0.11 0.04 1 67 0.005 0.92 Reef Size -0.005 0.06 1 6 0.12 0.94 Period:Previous Size 0.24 0.06 1 67 13.48 0.0005
Notes: Results of the Linear Mixed Model (LLM) defined a priori to evaluate the Δ size of individuals (Size – Previous Size) for select subsets of the data. For Acropora in the BEFORE period only (both treatments) (N=55), the full model tested was: Δ Size ~ Treatment + Previous Size +Reef size + Previous Size*Period + σPAIR + σREEF, where σ designate random effects of Pair (N=6) and Reef (N=12). For Acropora within reefs with Stegastes nigricans PRESENT only (N=78), the full model tested was: Δ Size ~ Period + Previous Size +Reef size + Previous Size*Period + σREEF, where σ designate random effects of Reef (N=8) (Note: Pair was omitted, as it is redundant without the other Treatment). ‘Intercept’ refers to differences for very small (Size=0) individuals. ‘Treatment’ refers to the presence or removal of Stegastes nigricans on experimental reefs. ‘Period’ distinguishes between the 2006-07 observational period before removals occurred (versus the 2007-08 experimental period). ‘Previous Size’ is a continuous covariate testing whether the size of an individual at the previous time step influences the likelihood of mortality. ‘Reef size’ isolates differences due to increases in the size of experimental reefs (Appendix G: Table G-1). In addition, I tested relevant interactions for each subset of the data as reported above. Please note, because variability was not constant between periods, I added a term to specify constant variance within (but not between) periods to the latter model (weights=varident(form=~1|Period)).
179
Table H-7. Follow-up change in size analyses for Pocillopora (LMM)
Subset Variable Est.
S.E.
numDF
denDF
F-value Pr > F
Pocillopora BEFORE ONLY
Before (Present,Size=1.0) 1.59 0.76 1 106 4.59 0.03 Treatment (Removed) -0.34 0.70 1 4 0.56 0.49 Previous Size -0.06 0.03 1 106 9.33 0.003 Reef Size -0.02 0.06 1 4 0.06 0.82 Treatment:Previous Size 0.004 0.04 1 106 0.008 0.92
Pocillopora PRESENT ONLY
Before (Present,Size=1.0) 0.77 0.56 1 162 6.78 0.01 Period (Experimental) -0.76 0.81 1 162 5.31 0.02 Previous Size -0.06 0.02 1 162 11.00 0.001 Reef Size 0.07 0.05 1 6 2.05 0.20 Period:Previous Size 0.01 0.05 1 162 0.09 0.76
Notes: Results of the Linear Mixed Model (LLM) defined a priori to evaluate the Δ size of individuals (Size – Previous Size) for select subsets of the data. For Pocillopora in the BEFORE period only (both treatments) (N=120), the full model tested was: Δ Size ~ Treatment + Previous Size +Reef size + Previous Size*Period + σPAIR + σREEF, where σ designate random effects of Pair (N=6) and Reef (N=12). For Pocillopora within reefs with Stegastes nigricans PRESENT only (N=173), the full model tested was: Δ Size ~ Period + Previous Size +Reef size + Previous Size*Period + σREEF, where σ designate random effects of Reef (N=8) (Note: Pair was omitted, as it is redundant without the other Treatment). ‘Intercept’ refers to differences for very small (Size=0) individuals. ‘Treatment’ refers to the presence or removal of Stegastes nigricans on experimental reefs. ‘Period’ distinguishes between the 2006-07 observational period before removals occurred (versus the 2007-08 experimental period). ‘Previous Size’ is a continuous covariate testing whether the size of an individual at the previous time step influences the likelihood of mortality. ‘Reef size’ isolates differences due to increases in the size of experimental reefs (Appendix G: Table G-1). In addition, I tested relevant interactions for each subset of the data as reported above. Please note, because variability was not constant between periods, I added a term to specify constant variance within (but not between) periods to the latter model (weights=varident(form=~1|Period)).
180
Figure H-1. Raw mortality values for Acropora. Mortality (=1) versus survival (=0) as a function
of Previous Size (cm) by ‘Treatment’ (Stegastes nigricans PRESENT or REMOVED) and ‘Period’ (BEFORE or EXPERIMENTAL).
181
Figure H-2. Raw mortality values for Pocillopora. Mortality (=1) versus survival (=0) as a
function of Previous Size (cm) by ‘Treatment’ (Stegastes nigricans PRESENT or REMOVED) and ‘Period’ (BEFORE or EXPERIMENTAL).
182
Figure H-3. Representative photos of Acropora predation before and after removals of
Stegastes nigricans. Note: There are a few branch tips missing before, but substantial skeletal loss and development of crustose coralline algae after removals, which is consistent high grazing pressure by excavating corallivores and herbivores.
183
Figure H-4. Representative photos of Pocillopora predation before and after removals of
Stegastes nigricans. Note: There is some predation by butterflyfishes before and drastic shrinkage, consistent with crown-of-thorns seastar Acanthaster planci feeding scars, after removals.
184
APPENDIX I TRANSITION MATRICES FOR ACROPORA AND POCILLOPORA IN THE
PRESENCE AND REMOVAL OF FARMERFISH
Figure I-1. Schematic of size classes and types of transitions for Acropora and
Pocillopora.
185
Figure I-2. Size structure transition matrix for Acropora on all reefs prior to experimental
manipulations. This matrix combines colonies on both control and (scheduled to be) removal reefs (i.e., with Stegastes nigricans present during the BEFORE ‘Period’, July 2006- April 2007). Individuals that fragmented are represented by red dots, while all others are in black. Size classes, marked by grey lines on the X (Previous size, cm) and Y (Current size, cm) axes, correspond to the size class schematic in Figure I-1. The black line marks the 1:1 line and runs through those cells that represent ‘looping’, or staying in the same size class. Cells below this diagonal vector represent ‘shrinkage’ from a larger size class to a smaller size class, while cells above represent ‘growth’ in the opposite direction. For each cell, raw transition values (bold) and probabilities (small) are in red. Raw mortality (bold) and probabilities (small) are in blue, and also represented by small black lines, along the x-axis. The pink line represents the Size~Previous size (lm), with no mortalities or fragments included. The teal line represents the same relationship with fragments (but no mortalities).
186
Figure I-3. Size structure transition matrix for Acropora following application of clove oil
to experimental CONTROL reefs (i.e., with Stegastes nigricans present during the EXPERIMENTAL ‘Period’, July 2007-Apr 2008). Individuals that fragmented are represented by red dots, while all others are in black. Size classes, marked by grey lines on the X (Previous size, cm) and Y (Current size, cm) axes, correspond to the size class schematic in Figure I-1. The black line marks the 1:1 line and runs through those cells that represent ‘looping’, or staying in the same size class. Cells below this diagonal vector represent ‘shrinkage’ from a larger size class to a smaller size class, while cells above represent ‘growth’ in the opposite direction. For each cell, raw transition values (bold) and probabilities (small) are in red. Raw mortality (bold) and probabilities (small) are in blue, and also represented by small black lines, along the x-axis. The pink line represents the Size~Previous size (lm), with no mortalities or fragments included. The teal line represents the same relationship with fragments (but no mortalities).
187
Figure I-4. Size structure transition matrix for Acropora following application of clove oil
and removal of farmerfish (i.e., experimental reefs in which Stegastes nigricans was REMOVED during the EXPERIMENTAL ‘Period’, July 2007-Apr 2008). Individuals that fragmented are represented by red dots, while all others are in black. Size classes, marked by grey lines on the X (Previous size, cm) and Y (Current size, cm) axes, correspond to the size class schematic in Figure I-1. The black line marks the 1:1 line and runs through those cells that represent ‘looping’, or staying in the same size class. Cells below this diagonal vector represent ‘shrinkage’ from a larger size class to a smaller size class, while cells above represent ‘growth’ in the opposite direction. For each cell, raw transition values (bold) and probabilities (small) are in red. Raw mortality (bold) and probabilities (small) are in blue, and also represented by small black lines, along the x-axis. The pink line represents the Size~Previous size (lm), with no mortalities or fragments included. The teal line represents the same relationship with fragments (but no mortalities).
188
Figure I-5. Size structure transition matrix for Pocillopora on all reefs prior to
experimental manipulations. This includes control and (scheduled to be) removal reefs (i.e., with Stegastes nigricans present during the BEFORE ‘Period’, July 2006- April 2007). Individuals that fragmented are usually represented by red dots (none present), while all others are in black. Size classes, marked by grey lines on the X (Previous size, cm) and Y (Current size, cm) axes, correspond to the size class schematic in Figure I-1. The black line marks the 1:1 line and runs through those cells that represent ‘looping’, or staying in the same size class. Cells below this diagonal vector represent ‘shrinkage’ from a larger size class to a smaller size class, while cells above represent ‘growth’ in the opposite direction. For each cell, raw transition values (bold) and probabilities (small) are in red. Raw mortality (bold) and probabilities (small) are in blue, and also represented by small black lines, along the x-axis. The pink line represents the Size~Previous size (lm), with no mortalities or fragments included.
189
Figure I-6. Size structure transition matrix for Pocillopora following application of clove
oil to experimental CONTROL reefs (i.e., with Stegastes nigricans present during the EXPERIMENTAL ‘Period’, July 2007-Apr 2008). Individuals that fragmented are usually represented by red dots (none present), while all others are in black. Size classes, marked by grey lines on the X (Previous size, cm) and Y (Current size, cm) axes, correspond to the size class schematic in Figure I-1. The black line marks the 1:1 line and runs through those cells that represent ‘looping’, or staying in the same size class. Cells below this diagonal vector represent ‘shrinkage’ from a larger size class to a smaller size class, while cells above represent ‘growth’ in the opposite direction. For each cell, raw transition values (bold) and probabilities (small) are in red. Raw mortality (bold) and probabilities (small) are in blue, and also represented by small black lines, along the x-axis. The pink line represents the Size~Previous size (lm), with no mortalities or fragments included.
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Figure I-7. Size structure transition matrix for Pocillopora following application of clove
oil and removal of farmerfish (i.e., experimental reefs in which Stegastes nigricans was REMOVED during the EXPERIMENTAL ‘Period’, July 2007-Apr 2008). Individuals that fragmented are represented by red dots, while all others are in black. Size classes, marked by grey lines on the X (Previous size, cm) and Y (Current size, cm) axes, correspond to the size class schematic in Figure I-1. The black line marks the 1:1 line and runs through those cells that represent ‘looping’, or staying in the same size class. Cells below this diagonal vector represent ‘shrinkage’ from a larger size class to a smaller size class, while cells above represent ‘growth’ in the opposite direction. For each cell, raw transition values (bold) and probabilities (small) are in red. Raw mortality (bold) and probabilities (small) are in blue, and also represented by small black lines, along the x-axis. The pink line represents the Size~Previous size (lm), with no mortalities or fragments included. The teal line represents the same relationship with fragments (but no mortalities).
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LIST OF REFERENCES
Adjeroud, M., Y. Chancerelle, M. Schrimm, T. Perez, D. Lecchini, R. Galzin, and B. Salvat. 2005. Detecting the effects of natural disturbances on coral assemblages in French Polynesia: a decade survey at multiple scales. Aquatic Living Resources 18:111-123.
Altieri, A. H., B. R. Silliman, and M. D. Bertness. 2007. Hierarchical organization via a facilitation cascade in intertidal cordgrass bed communities. American Naturalist 169:195-206.
Bak, R. P. M. and M. S. Engel. 1979. Distribution, abundance, and survival of juvenile hermatypic corals (scleractinia) and the importance of life history strategies in the parent coral community. Marine Biology 54:341-352.
Bellwood D. R., T. P. Hughes , C. Folke, and M. Nyström. 2004. Confronting the coral reef crisis. Nature 429:827-833.
Berlow, E. L., S. A. Naverrete, C. J. Briggs, M. E. Power, B. A. Menge.1999. Quantifying variation in the strengths of species interactions. Ecology 80:2206-2224.
Bertness, M. D. and G. H. Leonard. 1997. The role of positive interactions in communities: Lessons from intertidal habitats. Ecology 78:1976-1989.
Bertness, M. D., G. C. Trussell, P. J. Ewanchuk, and B. R. Silliman. 2002. Do alternate stable community states exist in the Gulf of Maine rocky intertidal zone? Ecology 83:3434-3448.
Bertness, M. D., G. C. Trussell, P. J. Ewanchuk, B. R. Silliman, and C. M. Crain. 2004. Consumer-controlled community states on Gulf of Maine rocky shores. Ecology 85:1321-1331.
Berumen, M. L. and M. S. Pratchett. 2006. Recovery without resilience: persistent disturbance and long-term shifts in the structure of fish and coral communities at Tiahura Reef, Moorea. Coral Reefs 25:647-653.
Birrell, C. L., L. J. McCook, and B. L. Willis. 2005. Effects of algal turfs and sediment on coral settlement. Marine Pollution Bulletin 51:408-414.
Bolker, B. M, M. E. Brooks, C. J.Clark, S. W.Geange, J. R. Poulsen, M. H. H. Stevens, and J. S. S. White. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24:127-135.
Boogert, N. J., D. M. Paterson, and K. N. Laland. 2006. The implications of niche construction and ecosystem engineering for conservation biology. Bioscience 56:570-578.
192
Bouchon, C. 1985. Quantative study of scleractinian coral communities of Tiahura Reef (Moorea, French Polynesia). Pages 279-290 in Proceedings of the 5th International Coral Reef Symposium, Volume 6. Papeete, Tahiti.
Boyer, S. E., J. S. S. White, A. C. Stier, and C. W. Osenberg. 2009. Effects of the fish anesthetic clove oil (eugenol) on coral health and growth. Journal of Experimental Marine Biology & Ecology 369:53-57.
Bruno, J. F., J. J. Stachowicz, and M. D. Bertness. 2003. Inclusion of facilitation into ecological theory. Trends in Ecology and Evolution 18:119-125.
Bruno, J. F. and E. R. Selig. 2007. Regional decline of coral cover in the Indo-Pacific: timing, extent, and subregional comparisons. Public Library of Science One 2: e711. doi:10.1371/journal.pone.0000711.
Burkepile, D. E. and M. E. Hay. 2006. Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128-3139.
Burkepile, D. E. and M. E. Hay. 2008. Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proceedings of the National Academy of Sciences 105:16201-16206.
Caswell, H. 2001. Life table response experiments, Pages 258-278 in Matrix Population Models, 2nd Ed., Sinauer, Sunderland, Massachusetts, USA.
Chase, J. M., M. A. Liebold, A. L. Downing, and J. B. Shurin. 2000. The effects of productivity, herbivory, and plant species turnover in grassland food webs. Ecology 81:2485-2497.
Ceccarelli, D. M., G. P. Jones, and L. J. McCook. 2001. Territorial damselfishes as determinants of the structure of benthic communities on coral reefs. Oceanography and Marine Biology 39:355-389.
Ceccarelli, D. M., G. P. Jones, and L. J. McCook. 2005. Foragers versus farmers: contrasting effects of two behavioural groups of herbivores on coral reefs. Oecologia 145:445-453.
Ceccarelli, D. M. 2007. Modification of benthic communities by territorial damselfish: a multi-species comparison. Coral reefs 26:853-866.
Cole, A. J., M. S. Pratchett, and G. P. Jones. 2008. Diversity and functional importance of coral-feeding fishes on tropical coral reefs. Fish and Fisheries Bulletin 9:286-307.
Coles, S. L., and R. Strathmann. 1973. Observations on coral mucus ‘flocs’ and their potential trophic significance. Limnology and Oceanography 18:673-678.
193
Colgan, M. W. 1987. Coral reef recovery on Guam (Micronesia) after catastrophic predation by Acanthaster planci. Ecology 68:1592-1605.
Colgan, M. W. 1985. Growth rate reduction and modification of a coral colony by a vermetid mollusc, Dendropoma maxima. Pages 205-210 in Proceedings of the 5th International Coral Reef Symposium, Volume 6. Papeete, Tahiti.
Connell, J. H. 1973. Population ecology of reef-building corals. Pages 205-245 in O. A. Jones and R. Endean, eds. Biology and geology of coral reefs, Volume 2. Academic Press, New York.
Connell, J. H. 1978. Diversity in tropical rain forests and coral reefs. Science 199:1302-1310.
Connell, J. H., T. P. Hughes, and C. C. Wallace. 1997. A 30-year study of coral abundance, recruitment, and disturbance at several scales in space and time. Ecological Monographs 67:461-488.
Crain, C. M. and M. D. Bertness. 2005. Community impacts of a tussock sedge:Is ecosystem engineering important in benign habitats? Ecology 86:2695-2704.
Crain, C. M. and M. D. Bertness. 2006. Ecosystem engineering across environmental gradients: implications for conservation and management. Bioscience 56:211-218.
Crossland, C. 1928. Notes on the ecology of the reef-builders of Tahiti. Proceedings of the Zoological Society 3:717-735.
Crouse, D. T., L. B. Crowder, H. Caswell. 1987. A stage-based population model for loggerhead sea turtles and implications for conservation. Ecology 68:1412-1423.
Darwin, C. 1842. The structure and distribution of coral reefs. Smith, Elder & Co., London, England.
Dayton , P. K. 1972. Toward an understanding of community resilience and the potential effects of enrichments to the benthos at McMurdo Sound, Antarctica. Pages 81-96 in Proceedings of the Colloquium on Conservation Problems in Antartica, Allen Press.
Davies, P. S. 1989. Short-term growth measurements of corals using an accurate buoyant weighing technique. Marine Biology 101:389-395.
DeMartini, E. E., A. M. Friedlander, S. A. Sandin, and E. Sala. 2008. Differences in fish-assemblage structure between fished and unfished atolls in the northern Line Islands, central Pacific. Marine Ecology Progress Series 365:199-215.
194
Doak, D. F., J. A. Estes, B. S. Halpern, U. Jacob, D. R. Lindberg, J. Lovvorn, D. H. Monson, M. T. Tinker, T. M. Williams, J. T. Wootton, I. Carroll, M. Emmerson, F. Micheli, and M. Novak. Understanding and predicting ecological dynamics: are major surprises inevitable? Ecology 89: 952-961.
Doherty, P. J. 1981. Coral reef fishes: recruitment-limited assemblages? Pages 465-470 in Proceedings of the 4th International Coral Reef Symposium, Volume 2. Manila, Phillipines.
Done, T. J., P. K. Dayton, A. E. Dayton, and R. Stegner. 1991. Regional and local variability in recovery of shallow coral reef communities. Coral Reefs 9:183-192.
Dulvy, N. K., R. P. Freckleton, and N. V. C. Polunin. 2004. Coral reef cascades and the indirect effects of predator removal by exploitation. Ecology Letters 7:410-416.
Ebersole, J. P. 1977. The adaptive signficance of interspecific territoriality in the reef fish Eupomacentrus leucostictus. Ecology 58:914-920.
Edmunds, P. J. 2005. The effect of sub-lethal increases in temperature on the growth and population trajectories of three scleractinian corals on the southern Great Barrier Reef. Oecologia 146:350-364.
Elahi, R. and P. J. Edmunds. 2007a. Consequences of fission in the coral Siderastrea sidereal: growth rates of small colonies and clonal input to population structure. Coral Reefs 26:271-276.
Elahi, R. and P. J. Edmunds. 2007b.Tissue age affects calcification in the scleractinian coral, Madracis mirabilis. Biological Bulletin 212:20-28.
Ellison, A. M., M. S. Bank, B. D. Clinton, E. A. Colburn, K. Elliot, C. R. Ford, D. R. Foster, B. D. Kloeppel, J. D. Knoepp, G. M. Lovett, J. Mohan, D. A. Orwig, N. L. Rodenhouse, W. V. Sobczak, K. A. Stinson, J. K. Stone, C. M. Swan, J. Thompson, B. Von Holle, and J. R. Webster. 2005. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3:479-486.
Eriksson, B. K., A. Rubach, and H. Hillebrand. 2006. Biotic habitat complexity controls species diversity and nutrient effects on net biomass production. Ecology 87:246-254.
Friedlander, A. M. and E. E. DeMartini. 2002. Contrasts in density, size, and biomass of reef fishes between the northwestern and the main Hawaiian islands: the effects of fishing down apex predators. Marine Ecology Progress Series 230: 253-264.
Frydl, P. 1978. The effect of parrotfish (Scaridae) on coral in Barbados, W.I. International Review of Hydrobiology 64:737-748.
195
Galzin, R. and J. P. Pointier. 1985. Moorea Island, Society Archipelago. Pages 157-164 in Proceedings of the 5th International Coral Reef Symposium, Volume 2. Papeete, Tahiti.
Galzin, R. 1987. Structure of fish communities of French Polynesian coral reefs. II. Temporal scales. Marine Ecology Progress Series 41: 137-145.
Galzin, R., J. S. S. White, and T. Lison de Loma. In Preparation. Can grazers limit coral recovery? Spatiotemporal trends in Moorea, French Polynesia (For submission to Science).
Gleason, M. G. 1993. Effects of disturbance on coral communities: bleaching in Moorea, French Polynesia. Coral Reefs 12:193-201.
Gleason, M. G. 1994. Factors influencing the recovery of corals after natural disturbance on reefs in Moorea, French Polynesia. Ph.D. dissertation, University of California, Berkeley, 358 pp.
Gleason, M. G. 1996. Coral recruitment in Moorea, French Polynesia: the importance of patch type and temporal variation. Journal of Experimental Marine Biology & Ecology 207:79-101.
Glynn, P. W. 1985. El Niño-associated disturbance to coral reefs and post disturbance mortality by Acanthaster planci. Marine Ecology Progress Series 26:295-300.
Glynn, P. W. and M. W. Colgan. 1988. Defense of corals and enhancement of coral diversity by territorial damselfishes. Pages 157-163 in Proceedings of the 6th International Coral Reef Symposium, Volume 2. Townsville, Australia.
Goreau, T. F., J. C. Lang, E. A. Graham, and P. D. Goreau. 1972. Structure and ecology of the Saipan reefs in relation to predation by Acanthaster planci (Linneus). Bulletin of Marine Science 22:113-152.
Green, A. L. 1992. Damselfish territories: focal sites for studies of the early life history of labroid fishes. Pages 601-605 in Proceedings of the 7th International Coral Reef Symposium, Volume 1. Guam, Micronesia.
Green, A. L. 1998. Spatio-temporal patterns of recruitment of labroid fishes (Pisces: Labridae and Scaridae) to damselfish territories. Environmental Biology of Fishes 51:235-244.
Haley, M. P. and C. R. Müller. 2002. Territorial behaviour of beaugregory damselfish (Stegastes leucostictus) in response to egg predators. Journal of Experimental Marine Biology and Ecology. 273:151-159.
Hall, VR and TP Hughes. 1996. Reproductive strategies of modular animals: comparative studies of reef-building corals. Ecology 77:950-963.
196
Halpern, B. S., K. Cottenie, and B. R. Broitman. 2006. Strong top-down control in southern California kelp forest ecosystems. Science 312:1230-1232.
Harrington, L, K Fabricius, G De’ath, and A Negri. 2004. Recognition and selection of settlement substrata determine post-settlement survival in corals. Ecology 85:3428-3437.
Hartman, C. D., J. S. S. White, and C. W. Osenberg. In Preparation. Effects of the farmerfish Stegastes nigricans on size and abudance of vermetid snails. (For submission to Marine Ecology Progress Series).
Hata H. and M. Kato. 2002. Weeding by the herbivorous damselfish Stegastes nigricans in nearly monocultural algae farms. Marine Ecology Progress Series 237:227-231.
Hata, H., and M. Nishihira. 2002. Territorial damselfish enhances multi-species co-existence of foraminifera mediated by biotic habitat structuring. Journal of Experimental Marine Biology and Ecology 270:215-240.
Hata, H., M. Nishihira, and S. Kamura. 2002. Effects of habitat-conditioning by the damselfish Stegastes nigricans (Lacepede) on the community structure of benthic algae. Journal of Experimental Marine Biology and Ecology 280:95-116.
Hata, H. and M. Kato. 2003. Demise of monocultural algal farms by exclusion of territorial damselfish. Marine Ecology Progress Series 263:159-167.
Hata, H. and M. Kato. 2004. Monoculture and mixed-species algal farms on a coral reef are maintained through intensive and extensive management by damselfishes. Journal of Experimental Marine Biology and Ecology 313:285-296.
Hata, H. and M. Kato. 2006. A novel obligate cultivation mutualism between damselfish and Polysiphonia algae. Biology Letters 2:593-596.
Hay, M. E. 1981. Herbivory, algal distribution, and the maintenance of between-habitat diversity on a tropical fringing reef. American Naturalist 118: 520-540.
Highsmith, R. C. 1982. Reproduction by fragmentation in corals. Marine Ecology Progress Series 7: 207-227.
Hixon, M. A. 1997. Effects of reef fish on corals and algae. Pages 230-248 in Birkeland , C., ed. Life and death of coral reefs, Chapman and Hall, New York, U.S.A
Hixon, M. A. and W. N. Brostoff. 1981. Fish grazing and community structure of Hawaiian reef algae. Pages 507-514 in Proceedings of the 4th International Coral Reef Symposium, Volume 2. Manila, Phillipines.
Hixon, M. A. and W. N. Brostoff. 1983. Damselfish as keystone species in reverse: intermediate disturbance and diversity of reef algae. Science 220:511-513.
197
Hixon, M. A. and W. N. Brostoff. 1996. Succession and herbivory: effects of differential fish grazing on Hawaiian coral-reef algae. Ecological Monographs 66:67-90.
Hoegh-Guldburg, O. 1988. A method for determining the surface area of corals. Coral Reefs 7:113-116.
Hoegh-Guldburg, O., P. J. Mumby, A. J. Hooten, R. S. Steneck, P. Greenfield, E. Gomez, C. D. Harvell, P. F. Sale, A. J. Edwards, K. Caldiera, N. Knowlton, C. M. Eakin, R. Iglesias-Prieto, N. Muthiga, R. H. Bradbury, A. Dubi, and M. E. Hatziolos. Science 318:1737-1742.
Hoey, A.S. and D.R. Bellwood. 2008. Cross-shelf variation in the role of parrotfishes on the Great Barrier Reef. Coral Reefs 27:37-47.
Hughes R. N. and A. H. Lewis 1974. On the spatial distribution, feeding and reproduction of the vermetid gastropod dendropoma maximum. Journal of Zoology, London 172:531-547.
Hughes, T. P. 1984. Population dynamics based on individual size rather than age: a general model with a coral reef example. American Naturalist 123:778-795.
Hughes, T. P. 1989. Community Structure and diversity of coral reefs: the role of history. Ecology 70:275-279.
Hughes, T. P. 1990. Recruitment limitation, mortality, and population regulation in open systems: a case study. Ecology 71:12-20.
Hughes, T. P. 1994. Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547-1551.
Hughes, T. P. and J. H. Connell. 1999. Multiple stressors on coral reefs: a long-term perspective. Limnology and Oceanography 44:932-940.
Hughes, T. P. and J. B. Jackson. 1980. Do corals lie about their age? Some demographic consequences of partial morality, fission, and fusion. Science 209: 713-715.
Hughes, T. P. and J. E. Tanner. 2000. Recruitment failure, life histories, and long-term decline of Caribbean corals. Ecology 81:2250-2263.
Hughes, T. P., A. H. Baird, E. A. Dinsdale, V. J. Harriot, N. A. Moltschaniwskyj, M. S. Pratchett, J. E. Tanner, and B. L. Willis. 2002. Detecting regional variation using meta-analysis and large-scale sampling: latitudinal patterns in recruitment. Ecology 83: 436-451.
198
Hughes, T. P., M. Rodrigues, D. R. Bellwood, D. Ceccarelli, O. Hoegh-Guldberg, L. McCook, N. Moltschaniwskyj, M. S. Pratchett, R. S. Steneck, and B. Willis. 2007. Phase shifts, herbivory, and the resilience of coral reefs to climate change. Current Biology 17:360-365.
Huston, M. A. 1985. Patterns of species diversity on coral reefs. Annual Review of Ecology and Systematics 16:149-177.
Idjadi, J. A., and P. J. Edmunds. 2003. Free-living colonies of Porites in Moorea, French Polynesia. Bulletin of Marine Science 72:1025-1031.
Jan, R. -Q., C. -T. Ho, and F. -K. Shiah. 2003. Determinants of territory size of the dusky gregory. Journal of Fish Biology 63:1589-1597.
Jayewardene, D., M. J. Donahue, and C. Birkeland. 2009. Effects of fréquent fish prédation on corals in Hawaii. Coral Reefs 28:499-506.
Jones, C. G. J. H. Lawton, M. Shachak. 1994. Organisms as ecosystem engineers. Oikos 69:373-386.
Jones, C. G., J. H. Lawton, M. Shachak. 1997. Positive and negative effects of organisms as physical ecosystem engineers. Ecology 77:1946-1957.
Jones, G. P., L. Santana, L. J. McCook, and M. I. McCormick. 2006. Resource use and impact of three herbivorous damselfishes on coral reef communities. Marine Ecology Progress Series 328:215-224.
Kappner, I., S. Al-Moghrabi, C. Richter. 2000. Mucus-net feeding by the vermetid gastropod Dendropoma maxima in coral reefs. Marine Ecology Progress Series 204:309-313.
Kaufman, L. 1977. The three spot damselfish: Effects on benthic biota of Caribbean coral reefs. Pages 559-564 in Proceedings of the 3rd International Coral Reef Symposium, Volume 1. Miami, Florida, USA.
Klumpp, D. W., D. McKinnon, and P. Daniel. 1987. Damselfish territories: zones of high productivity on coral reefs. Marine Ecology Progress Series 40:41-51.
Klumpp, D. W., A. D. McKinnon, and C. N. Mundy. 1987. Damselfish territories: zones of high productivity on coral reefs. Marine Ecology Progress Series 40:41-51.
Klumpp, D. W., A. D. McKinnon, and C. N. Mundy. 1988. Motile cryptofauna of a coral reef: abundance and trophic potential. Marine Ecology Progress Series 45:95-108.
Klumpp, D., W., and N. V. C. Polunin. 1989. Partitioning among grazers of food resources within damselfish territories on a coral reef. Journal of Experimental Marine Biology and Ecology 125:145-169.
199
Knowlton, N. 2001. The future of coral reefs. Proceedings of the National Academy of Sciences 98:5419-5425.
Knowlton, N., J. C. Lang, and B. D. Keller. 1988. Fates of staghorn coral isolates on hurricane-damaged reefs in Jamaica: the role of predators. Pages 83-88 in Proceedings of the 6th International Coral Reef Symposium, Volume 2. Townsville, Australia.
Knowlton, N. and J. B. C. Jackson. 2008. Shifting baselines, local impacts, and global change on coral reefs. Public Library of Science Biology 6: e54. doi:10.1371/journal.pbio.0060054.
Kohler, K. E. and S. M. Gill. 2006. Coral Point Count with Excel extensions: A visual basic program for the determination of coral and substrate coverage using random point count methodology. Computers and Geosciences 32:1259-1269.
Lessios, H.A., D. R. Robertson, and J. D. Cubit. 1984. Spread of Diadema mass mortality through the Caribbean. Science 226:335-337.
Letourneur, Y., R. Galzin, and M. Harmelin-Vivien. 1997. Temporal variations in the diet of the damselfish Stegastes nigricans (Lacepède) on a Réunion fringing reef. Journal of Experimental Marine Biology and Ecology 217:1-18.
Letourneur, Y. 2000. Spatial and temporal variability in territoriality of a tropical benthic damselfish on a coral reef (Reunion island). Environmental Biology of Fishes 57:377-391.
Lewis, S. M. 1986. The role of herbivorous fishes in the organization of a Caribbean reef community. Ecological Monographs 56:184-200.
Lison de Loma, T., M. L. Harmelin-Vivien, O. Naim, and M. F. Fontaine. 2000. Algal food processing by Stegastes nigricans, a herbivorous damselfish: differences between an undisturbed and a disturbed coral reef site (La Réunion, SW Indian Ocean). Oceanologica Acta 23:793-804.
Lison de Loma, T. and E. Ballesteros. 2002. Microspatial variability inside epilithic algal communities within territories of the damselfish Stegastes nigricans at La Réunion. Indian Ocean). Botanica Marina 45:316-323.
Littler, M. M., P. R. Taylor, and D. S. Littler. 1989. Complex interactions in the control of coral zonation on a Caribbean reef flat. Oecologia 80:1432-1939.
Lobel, P. S. 1980. Herbivory by damselfishes and their role in coral reef community ecology. Bulletin of Marine Science 30: 273-289.
Mantyka, C. S. and D. R. Bellwood. 2007. Direct evaluation of macroalgal removal by herbivorous coral reef fishes. Coral Reefs 26:435-442.
200
Mapstone, B. D., N. L. Andrew, Y. Chancerelle, B. Salvat. 2007. Mediating effects of sea urchins on interactions among corals, algae and herbivorous fish in the Moorea lagoon, French Polynesia. Marine Ecology Progress Series 332:143-153.
McClanahan, T. R., M. Ateweberhan, N. A. J. Graham, S. K. Wilson, C. Ruiz Sebastián, M. M. M. Guillaume, and J. H. Bruggemann. 2007. Western Indian Ocean coral communities: bleaching responses and susceptibility to extinction. Marine Ecology Progress Series 337:1-13.
McCook, L. J. 1996. Effects of herbivores and water quality on Sargassum distribution on the central Great Barrier Reef: cross-shelf transplants. Marine Ecology Progress Series 139:179-192.
McCook, L. J. 1999. Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18:357-367.
McCook, L. J., J. Jompa, and G. Diaz-Pulido. 2001. Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400-417.
Miller, M. W. and M. E. Hay. 1998. Effects of fish predation and seaweed competition on the survival and growth of corals. Oecologia 113:231-238.
Mills, L. S., M. E. Soulé, D. F. Doak.1993. The keystone-species concept in ecology and conservation. Bioscience 43:219-224.
Mora, C. 2008. A clear human footprint in the coral reefs of the Caribbean. Proceedings of the Royal Society B 275:767-773.
Morton J. E. 1965. Form and function in the evolution of the vermetidae. Bulletin of the British Museum of Natural History, Zoology 11:583-630.
Mumby, P. J., C. P. Dahlgren, A. R. Harborne, C. V. Kappel, F. Micheli, D. R. Brumbaugh, K. E. Holmes, J. M. Mendes, K. Broad, J. N. Sanchirico, K. Buch, S. Box, R. W. Stoffle, and A. B. Gill. 2006. Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98-101.
Mumby, P.J., A. R. Harborne, J. Williams, C. V. Kappel, D. R. Brumbaugh, F. Micheli, K. E. Holmes, C. P. Dahlgren, C. B. Paris, and P. G. Blackwell. Trophic cascades facilitates coral recruitment in a marine reserve. Proceedings of the National Academy of Sciences 104: 8362-8367.
Nelder, J. A. 1998. The great mixed-model muddle is alive and flourishing, alas! Food Quality and Preference 9:157-159.
Nugues, M. M. and C. M. Roberts. 2003. Coral mortality and interaction with algae in relation to sedimentation. Coral Reefs 22:507-516.
201
O’Donnell, J. L. and J. S. S White. In Preparation. Habitat selectivity and size allometry of the Christmas tree worm, Spirobranchus giganteous (Polychaeta: Serpulidae) (For submission to the Bulletin of Marine Science).
Osenberg, C. W., B. M. Bolker, J. S. S. White, C. M. St. Mary, and J. S. Shima. 2006. Statistical issues and study design in ecological restorations: lessons learned from marine reserves. Pages 280-302 in Falk, D. A., H., M. A. Palmer, J. B. Zedler, eds., Foundations of Restoration Ecology, Island Press, Washington D.C., U.S.A.
Paine, R. T. 1966. Food web complexity and species diversity. American Naturalist 100:65-75.
Paine, R. T. 1969. A note on trophic complexity and community stability. American Naturalist 103:91-93.
Paine, R. T. 1992. Food-web analysis through field measurement of per capita interaction strength. Nature 355:73-75.
Penin, L., M. Adjeroud, M. Schrimm, and H. S. Lenihan. 2007. High spatial variability in coral bleaching around Moorea (French Polynesia): patterns across locations and water depths. Comptes Rendus Biologies 330:171-181.
Peyrot-Clausade, M., P. Hutchings, and G. Richard. 1992. Temporal variations of macroborers in massive Porites lobata on Moorea, French Polynesia. Coral Reefs 11:161-166.
Porter, J. W. 1972. Predation by Acanthaster and its effect on coral species diversity. American Naturalist 106:487-492.
Potts, D. C. 1977. Suppression of coral populations by filamentous algae within damselfish territories. Journal of Experimental Marine Biology and Ecology 28:207-216.
Power, M., D. Tilman, J. A. Estes, B. A. Menge, W. J. Bond, L. S. Mills, G. Daily, J. C. Castilla, J. Lubchenco, and R. T. Paine. 1996. Challenges in the quest for keystones. Bioscience 46:609-620.
Power, M. 1997. Estimating impacts of a dominant detritivore in a neotropical stream, Trends in Ecology and Evolution 12:47-48.
Pratchett, M. S. Influence of coral symbionts on feeding preferences of crown-of-thorn starfish Acanthaster planci in the western Pacific. Marine Ecology Progess Series 214:111-119.
Purcell, S. W. 2000. Association of epilithic algae with sediment distribution on a windward reef in the northern Great Barrier Reef, Australia. Bulletin of Marine Science 66:199-214.
202
Randall, J. E. 1977. The effect of fishes on coral reefs. Pages 159-166 in Proceedings of the 2nd International Coral Reef Symposium, Volume 1. Brisbane, Australia.
Randall, J. E. 2005. Reef and shore fishes of the South Pacific: New Caledonia to Tahiti and the Pitcairn Islands. University of Hawaii Press, Honolulu, HI, 707 pp.
Ribak, G., J. Heller, A. Genin. 2005. Mucus-Net Feeding on Organic Particles by the Vermetid Gastropod Dendropoma Maximum In and Below the Surf Zone. Marine Ecology Progress Series 293:77-87.
Risk, M. J. and P. W. Sammarco. 1982. Bioerosion of corals and the influence of damselfish territoriality: a preliminary study. Oecologia 52:376-380.
Ritchie, M. E., D. Tilman, and J. M. H. Knops. 1998. Herbivore effects on plant and nitrogen dynamics in oak savanna. Ecology 79:165-177.
Robertson, D. R., S. G. Hoffman, and J. M. Sheldon. 1981. Availability of space for the territorial Caribbean damselfish Eupomacentrus planifrons. Ecology 62:1162-1169.
Robertson, D. R. 1996. Interspecific competition controls abundance and habitat use of territorial Caribbean damselfishes. Ecology 77:885-899.
Rotjan, R. D. and S. M. Lewis. 2008. Impact of coral predators on tropical reefs. Marine Ecology Progress Series 367:73-91.
Sale, P. F. 1977. Maintenance of high diversity in coral reef fish communities. American Naturalist 111: 337-359.
Sale, P. F. 1982. Stock-recruit relationships and regional coexistence in a lottery competitive system: a simulation study. American Naturalist 120:139-159.
Sammarco, P. W. 1983. Effects of fish grazing and damselfish territoriality on coral reef algae. I. Algal community structure. Marine Ecology Progress Series 13:1-14.
Sammarco, P. W. and J. H. Carleton. 1981. Damselfish territoriality and coral community structure: reduced grazing, coral recruitment, and effect on coral spat. Pages 525-535 in Proceedings of the 4th International Coral Reef Symposium, Volume 2. Manila, Philippines.
Sammarco, P.W., J. H. Carleton, and M. J. Risk. 1986. Effects of grazing and damselfish territoriality on bioerosion of dead corals: direct effects. Journal of Experimental Marine Biology and Ecology 98:1-19.
Sammarco, P. W., and M. J. Risk. 1990. Large-scale patterns in internal bioerosion of Porites: cross continental shelf trends on the Great Barrier Reef. Marine Ecology Progress Series 59:145-156.
203
Sammarco, P. W. and A. H. Williams. 1982. Damselfish territoriality: Influence on Diadema distribution and implications for coral community structure. Marine Ecology Progress Series 8:53-59.
Sandin, S.A., J.E. Smith, E.E. DeMartini, E.A. Dinsdale, S.D. Donner, A.M. Friedlander, T. Konotchick, M. Malay, J.E. Maragos, D. Obura, O. Pantos, G. Paulay, M. Richie, F. Rohwer, R.E. Schroeder, S. Walsh, J.B.C. Jackson, N. Knowlton, E. Sala. 2008. Baselines and degradation of coral reefs in the northern Line Islands. Public Library of Science One 3: e1548.
Shima, J. S., C. W. Osenberg, C. M. St. Mary, and L. Rogers. 2006. Implication of changing coral communities: do larval traits or habitat features drive variation in density-dependent mortality and recruitment of a juvenile reef fish? Pages 226-231 in Proceedings of the 10th International Coral Reef Symposium, Volume 1. Okinawa, Japan.
Shima, J. S., C. W. Osenberg, and C. M. St. Mary. 2008. Quantifying site quality in a heterogeneous landscape: recruitment of a reef fish. Ecology 89:86-94.
Sluka, R. D., and M. W. Miller. 2001. Herbivorous fish assemblages and herbivory pressure on Laamu Atoll, Republic of Maldives. Coral Reefs 20: 255-262.
Smith, J. E., M. Shaw, R. A. Edwards, D. Obura, O. Pantos, E. Sala, S. A. Sandin, S. Smriga, M. Hatay, and F. L. Rohwer. 2006. Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecology Letters 9:835-845.
Soulé, M. E., J.A. Estes, J. Berger, and C. Martinez del Rios. 2003. Ecological effectiveness: Conservation goals for interactive species. Conservation Biology 17:1238-1250.
Sousa, W. P. 1979a. Experimental investigations of disturbance and ecological succession in a rocky intertidal algal community. Ecological Monographs 49:228-254.
Sousa, W. P. 1979b. Disturbance in marine intertidal boulder fields: the nonequilibrium maintenance of species diversity. Ecology 60:1225-1239.
Spooner, D. E., and C. C. Vaughn. 2006. Context-dependent effects of freshwater mussels on stream benthic communities. Freshwater Biology 51:1016-1024.
Suefuji, M. and R. van Woesik. 2001. Coral recovery from the 1998 bleaching event is facilitated by Stegastes territories, Okinawa, Japan. Coral Reefs 20:385-386.
Steneck, R. S. and Sala, E. A. 2005. Large marine carnivores: trophic cascades and top-down controls in coastal ecosystems past and present. Pages 110-137 in Ray, J., K. Redford, R. Steneck and J. Berger, eds., Large Carnivores and the conservation of biodiversity, Island Press.
204
Stewart, H. L., S. J. Holbrook, R. J. Schmitt, and A. J. Brooks. 2006. Symbiotic crabs maintain coral health by clearing sediment. Coral Reefs 25:609-615.
Stoddart, J. 1983. Asexual production of planulae in the coral Pocillopora damicornis. Marine Biology 76: 279-284.
Veron, J. E. N. 2000. Corals of the world, Volumes 1-3, 1381 pp. Australian Institute of Marine Science, Queensland, Australia.
Vine, P. J. Effects of algal grazing and aggressive behavior of the fishes Pomacentrus lividus and Acanthurus sohal on coral-reef ecology. Marine Biology 24:131-136.
Vuxton, E. A., J. S. S. White, and B.M. Bolker. In Preparation. Effects of the dusky farmerfish, Stegastes nigricans, on algal community structure (For submission to Bulletin of Marine Science).
Warner, R. R., and P. L. Chesson. 1985. Coexistence mediated by recruitment fluctuations: a field guide to the storage effect. American Naturalist 125:769-787.
Webster, M. S. and G. R. Almany. 2002. Positive indirect effects in a coral reef fish community. Ecology Letters 5:549-557.
Werner, E. E. and J. F. Gilliam. 1984. The ontogenetic niche and species interactions in size-structured populations. Annual Review of Ecology, Evolution, & Systematics 15:393-425.
Wellington, G. M. 1982. Depth zonation of corals in the Gulf of Panama: control and facilitation by resident reef fishes. Ecological Monographs 52:223-241.
White, J.S.S. and B.M. Bolker. In Preparation. Key engineer indirectly alters demographic rates and recovery of corals (For submission to American Naturalist)
White, J.S.S., S.E. Boyer, and A. Delval. In Preparation-a. Indirect effects of Stegastes nigricans on massive Porites coral and implications for other community members (For submission to Coral Reefs).
White, J. S. S., A. R. Thompson, and S. Ferse. In Preparation-b. Hierarchical sampling design tests spatial variation in distribution and abundance of sessile epifauna on dominant massive Porites spp. (For submission to the Marine Ecology Progress Series).
White, J. S. S. and J. L. O’Donnell. 2010. Indirect effects of a key ecosystem engineer alter survival and growth of foundation coral species. Ecology In press.
Williams, A. H. 1980. The threespot damselfish: a noncarnivorous keystone species. American Naturalist 116:138-142.
205
Williams, A. H. 1981. An analysis of competitive interactions in a patchy back-reef environment. Ecology 62:1107-1120.
Wilson, S. and D. R. Bellwood. 1997. Cryptic dietary components of territorial damselfishes (Pomacentridae, Labroidei). Marine Ecology Progress Series 153:299-310.
Woodley, J. D., E. A. Chornesky, P. A. Clifford, J. B. C. Jackson, S. Kaufman, N. Knowlton, J. C. Lang, M. P. Pearson, J. W. Porter, M. C. Rooney, K. W. Rylaarsdam, V. J. Tunnicliffe, C. M. Wahle, J. L Wulff, A. S. G. Curtis, M. D. Dallmeyer, B. P. Jupp, M. A. R. Koehl, J. Neigel, and E. M. Sides. 1981. Hurricane Allen’s impact on Jamaican coral reefs. Science 214:749-755.
Wootton, J. T. 1997. Estimates and test of per capita interaction strength: diet, abundance, and impact of intertidally foraging birds. Ecological Monographs 67:45-64.
Wright, J.P., C. G. Jones, and A. S. Flecker. 2002. An ecosystem engineer, the beaver, increases species richness at the landscape scale. Oecologia 132:96-101.
Zuur, A., F., E. N. Leno, N. J. Walker, A. A. Saveliev, and G. M. Smith. 2009. Mixed effects models and extensions in ecology with R. Springer, New York, U.S.A. 574 pp.
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BIOGRAPHICAL SKETCH
Jada-Simone Shanti White was born in Phoenix, Arizona, and raised in northern
California. She was first introduced to Polynesia through several school-related trips to
Hawaii. These experiences had a profound impact and Jada attended Hawaii Pacific
University after graduating from Mercy High School in 1995. At the time, she was Pre-
Professional, on track to Medical School, but she realized through her experiences at
H.P.U. that there might be other options to study and contribute to the biological
sciences. She returned to northern California and pursued basic study in biology at
Butte Community College. At Butte, she was given hands-on opportunities to learn
about field ecology by her mentor, Albin Bills, and she never looked back. She started
working at the Department of Fish and Game Habitat Conservation Division collecting
basic population data for four runs of Chinook salmon in the Sacramento River Valley,
undertook additional projects studying the California Newt on Table Mountain, and
rounded out her experience by studying Steelhead and Rainbow Trout on the Feather
River and its tributaries with the Department of Water Resources. When she had
exhausted all coursework at Butte College, and gained considerable field experience,
she transferred to University of California Santa Barbara. Within the first semester she
joined the Schmitt-Holbrook lab, which had a large research program conducting
fieldwork in Moorea, French Polynesia. Volunteer work became a technician position,
which blossomed into a senior honors thesis opportunity, and ultimately resulted in
additional professional experiences in both French Polynesia and Santa Barbara. In
2003, she moved to Gainesville, Florida to develop strong quantitative and natural
history skills at the University of Florida and continue her work contributing to our
understanding of community change in Polynesia.