vol. 175, no. 2 the american naturalist february 2010 �

Notes and CommentsIs Diet Quality an Overlooked Mechanism for Bergmann’s Rule?

Chuan-Kai Ho,1,* Steven C. Pennings,1 and Thomas H. Carefoot2

1. Department of Biology and Biochemistry, University of Houston, Houston, Texas 77204; 2. Department of Zoology, University ofBritish Columbia, Vancouver, British Columbia V6T 1Z4, Canada

Submitted February 20, 2009; Accepted August 21, 2009; Electronically published December 16, 2009

Online enhancement: appendix.

abstract: Bergmann’s rule (body size increases with latitude) haslong interested biologists; however, its mechanism remains unclear.An overlooked mechanism (latitudinal variation in plant quality)might help explain Bergmann’s rule. We studied three herbivores. Inthe field, the planthopper Prokelisia and the sea hare Aplysia, but notthe long-horned grasshopper Orchelimum, were larger at high lati-tudes, following Bergmann’s rule. In the laboratory, all three speciesgrew larger or faster on high-latitude plants. High-latitude diets in-creased Prokelisia size and Aplysia growth rates by 8% and 72%,respectively, enough to explain the increase in field body size towardhigh latitudes. Therefore, latitudinal variation in herbivore body sizecould be influenced by latitudinal variation in plant quality, whichmay directly or indirectly also affect body size in detritivores, par-asitoids, and predators. Studies of Bergmann’s rule should considerthe influence of biotic factors on body size in addition to abioticfactors such as temperature and precipitation.

Keywords: body size, herbivore, plant quality, latitudinal variation,biogeography, Spartina alterniflora.

Introduction

Biologists are interested in how abiotic and biotic factorsgenerate ecological patterns, not just because we wish tounderstand how organisms are shaped by their environ-ment but also because we seek to predict what will happengiven future environmental changes. One of the most strik-ing ecological patterns that has been discovered is Berg-mann’s rule, which states that body size tends to increasewith latitude or with lower temperatures (Bergmann 1847;Mayr 1956). Bergmann’s rule was originally proposed forendotherms and is obeyed by 76% of birds and 71% ofmammals (Millien et al. 2006). Surprisingly, however,Bergmann’s rule is also obeyed by about 80% of ecto-therms (Atkinson 1994; Walters and Hassall 2006).

* Corresponding author. Present address: Department of Marine Biology,

Texas A&M University, Galveston, Texas 77551; e-mail: chuanho@tamug.edu.

Am. Nat. 2010. Vol. 175, pp. 269–276. � 2009 by The University of Chicago.0003-0147/2010/17502-51095$15.00. All rights reserved.DOI: 10.1086/649583

Body size has profound effects on the physiology andlife history of an organism, as well as an organism’s in-teractions with other individuals or species (Werner et al.1983; Partridge and French 1996; Brown et al. 2004). SinceBergmann’s rule states that body size varies across geo-graphic regions, it has drawn the attention of both ecol-ogists and evolutionary biologists (Blanckenhorn and De-mont 2004; Blanckenhorn et al. 2006; Stillwell et al. 2008).However, despite over a century of study, the mechanismsunderlying Bergmann’s rule are still unclear. It was orig-inally proposed that temperature explained Bergmann’srule in endotherms (Bergmann 1847; Mayr 1956). Underthis scenario, larger animals are favored at low tempera-tures because their lower surface area-to-volume ratio cre-ates an advantage in conserving body heat. This expla-nation for Bergmann’s rule has largely been discountedfor endotherms (Ashton et al. 2000; Freckleton et al. 2003)and is even less compelling for ectotherms, especially thosethat are small or aquatic, whose body temperature largelyfluctuates with ambient temperature. An alternative ex-planation for Bergmann’s rule came from the perspectiveof life history (Atkinson 1994; Partridge and French 1996;Angilletta et al. 2004). Basically, this explanation suggestedthat organisms are selected to delay maturation in colderenvironments and therefore reach a larger adult size de-spite a slower growth rate.

While temperature and other abiotic factors that covarywith latitude, such as rainfall, have been the primary focusof efforts to understand Bergmann’s rule (James 1970;Sand et al. 1995; Azevedo et al. 1996; Van Voorhies 1996;Ashton et al. 2000; Millien et al. 2006; Walters and Hassall2006; Yom-Tov and Geffen 2006), biotic factors that varywith latitude (e.g., food availability) have only occasionallybeen examined (McNab 1971; Arnett and Gotelli 2003).To our knowledge, the role of food quality in explainingBergmann’s rule has not been directly examined, althoughpast authors have speculated that food quality may varywith latitude and consequently affect animal body size(e.g., Langvatn and Albon 1986; Herfindal et al. 2006).

270 The American Naturalist

Plant quality (e.g., chemical defenses, nitrogen content)often varies across latitude, with better plant quality athigh latitude (Bolser and Hay 1996; Siska et al. 2002;Wright et al. 2004; C.-K. Ho and S. C. Pennings, unpub-lished manuscript). Given that plant quality is likely criticalto herbivore growth, it is reasonable to speculate that betterplant quality at high latitudes might support better growthof herbivores, leading to Bergmann’s rule. Although thisexplanation is limited to herbivores, they represent a sub-stantial proportion of animal species. Moreover, similarmechanisms might operate at other trophic levels if largerherbivores represent a better resource for higher trophiclevels (see “Discussion”).

In summary, we argue that the focus on seeking abioticexplanations for Bergmann’s rule has caused biologists tooverlook biotic factors that might contribute to latitudinalpatterns in body size. Here, we examine the hypothesisthat food quality contributes to latitudinal patterns in bodysize of three herbivore species. We tested two predictions:(1) in the field, herbivores will be larger at high latitudes,consistent with Bergmann’s rule, and (2) in the laboratory,plants collected from high latitudes will support bettergrowth of herbivores, suggesting that variation in plantquality across latitude could contribute to Bergmann’srule.

Methods

Study Species

We studied three herbivore species: the planthopper Pro-kelisia marginata, the long-horned grasshopper Orcheli-mum fidicinium, and the sea hare Aplysia juliana. All spe-cies will be referred to generically hereafter. The inclusionof two terrestrial herbivores and one marine herbivoreensured that our results were not habitat specific.

Prokelisia, a multivoltine planthopper, is the most abun-dant herbivore species in low salt marshes in the Atlanticand Gulf Coasts of the United States (Denno et al. 1985,1996). Prokelisia is a phloem-feeding specialist on Spartinaalterniflora, which is one of the most abundant plants insalt marshes along the Atlantic and Gulf Coasts of theUnited States. On the Atlantic Coast of North America,the distribution of Spartina ranges from Florida to Quebec(USDA 2009). Orchelimum, a univoltine long-hornedgrasshopper, is one of the most abundant orthoptera foundon S. alterniflora in the Atlantic Coast of the United States;it extends from Florida into New England but is rare northof Virginia (Wason and Pennings 2008). Orchelimum feedsheavily on S. alterniflora and, like many tettigoniids, alsoincludes arthropod prey in its diet (Smalley 1960; Penningset al. 2001). Aplysia is an opisthobranch gastropod with acosmopolitan distribution, occurring over a wide range of

latitude, from New Zealand through northern Japan (Eales1960; Carefoot 1987). Aplysia consumes green algae of thegenus Ulva throughout most of its range (Carefoot 1987)and also consumes the brown alga Undaria pinnatifida intemperate waters (Saito and Nakamura 1961).

Patterns of Body-Size Variation in the Field

To document patterns in body size across latitude for thesethree herbivore species, we collected new data from field-collected specimens or referred to published data. FromJuly 16 to 28, 2007, we used sweep nets to collect hundredsof Prokelisia individuals from Spartina plants located alongcreek banks at each of 15 salt marsh sites (table A1 in theonline edition of the American Naturalist) from Florida toMassachusetts, over 12� of northern latitude. We randomlyselected 20 adults/site and measured their body lengthfrom the frons (tip of the head) to the end of the abdomen.We calculated the average body length for males and fe-males separately for each site, examined the effect of sexon body size using an ANCOVA with latitude as a covar-iate, and evaluated the interactive effect between latitudeand sex on body size by comparing the regression slopebetween sexes.

We obtained body-size data for Orchelimum from Wa-son and Pennings (2008). They measured tibia length asan indicator of body size of adult Orchelimum that werecollected from 20 salt marsh sites from Florida to RhodeIsland, over 11� of northern latitude, from 2004 to 2006(19 individuals/site, on average). We calculated the averagetibia length for males and females separately for each siteand analyzed the data the same way as for Prokelisia. Tibialength was a less variable measurement than body lengthfor Orchelimum because animals adopted a variety of moreor less “hunched” postures after collection; nevertheless,analyses of body length and tibia length led to identicalconclusions.

Since Aplysia has a flexible body and indeterminategrowth, we used maximum body mass as the best indicatorof variation in body size. We extracted data on maximumbody size of Aplysia from published studies conducted inthe Southern (Tanzania, Brazil, Australia, New Zealand)and Northern (Barbados, Hawaii, Florida, Okinawa, Ja-pan) Hemispheres (see fig. 1 legend). In addition, datafrom six locations were added using our unpublished ob-servations and personal communications from other sci-entists. The final data set covered over 35� of latitude ineach hemisphere. Since Aplysia is a simultaneous her-maphrodite, we did not divide the data by sex.

Diet Quality and Bergmann’s Rule 271

Do Diets from Different Latitudes Affect HerbivorePerformance in the Laboratory?

To examine how host plants from different latitudes affectthe performance of herbivores, we conducted factorialgrowth experiments (plant origin # herbivore origin) withProkelisia and Orchelimum and a single-factor (plant spe-cies) experiment with Aplysia. To simplify the design ofexperiments with Prokelisia and Orchelimum, we groupedthe sites from which we collected plants and herbivoresinto high-, medium-, and low-latitude regions (5 sites/region; table A1).

The Prokelisia experiment was a 3 (plant regions) # 3(Prokelisia regions) factorial design, with five replicates ofeach combination of regions. We collected Spartina plants( ) and Prokelisia adults from May 30 to JuneN p 5/site11, 2006, at the same sites described above (table A1).Spartina were potted in a mixture of 60% potting soil and40% sand; no fertilizer was added. Prokelisia (N p

) were cultured in polyester cages on additional20/siteSpartina plants collected from their native sites. Prokelisiaand Spartina were brought to the greenhouse on SapeloIsland, Georgia. Once these Prokelisia produced offspringin August 2006, three juveniles (fourth instar, two stagesbefore adulthood) from each site were reared on cagedSpartina. Twice a week, we removed individuals that hadreached adulthood, and we measured their body length.We scored Prokelisia for sex when they were adults becauseit is difficult to determine the sex of juveniles. Data wereanalyzed as a three-way ANOVA, with plant region, her-bivore region, and sex as main effects. We did not measureinitial size of Prokelisia because we wished to minimizehandling of delicate nymphs; therefore, we analyzed finaladult size rather than growth rate.

The Orchelimum experiment was a 3 (plant re-gions) # 2 (Orchelimum regions) factorial design becauseOrchelimum was too rare to collect successfully at the high-latitude sites. Each combination of regions had an averageof eight replicates ( for each plant region;N p 15 N p

, 23 for Orchelimum from medium- and low-latitude22regions). We collected Spartina plants ( ) fromN p 8/siteMay 30 to June 11, 2006, at the same sites described aboveand potted them in a mixture of 60% potting soil and40% sand; no fertilizer was added. Because Orchelimumhas only one generation a year (Smalley 1960), we usedfield-collected individuals instead of laboratory-raised ju-veniles for the laboratory experiment. Orchelimum juve-niles (fourth instar, two stages before adulthood) werecollected from July 16 to 28, 2006, from the same fieldsites described above (except the high-latitude region). OnJuly 29, 2006, we measured the body mass and tibia lengthof each Orchelimum and placed each individual into a glassjar with a Spartina leaf freshly cut from a plant from a

high-, medium-, or low-latitude site. Leaves were replacedevery 2 days. After 1 month, we remeasured body massand tibia length. Since adult Orchelimum become prevalentin the field about 2 months after the peak of nymph abun-dance (C.-K. Ho and S. C. Pennings, personal observa-tions), a 1-month laboratory experiment represents a largeproportion of the growth period of Orchelimum. Dataanalysis was similar to that in the Prokelisia experiment.We quantified the impact of plant diet on Orchelimumindividuals by calculating their relative growth rate in size,

, since not all of them reached adulthood(ln S � ln S )/DT1 0

or survived the same period of time; S1, S0, and DT rep-resent final size, initial size, and time period, respectively.

The Aplysia experiment reflected the natural distribu-tion of its host plants across latitude. We conducted ex-periments with Aplysia at the Noto Marine Laboratory(37�30�N, 137�10�E), Noto Peninsula, Japan, in 1993.Rocky intertidal and shallow subtidal areas near the lab-oratory are dominated by the algae Ulva and Undaria.Aplysia (32–116-g initial mass) were collected near thelaboratory, blotted dry with a towel, weighed, maintainedin the laboratory on a diet of Ulva (a low-latitude diet),Undaria (a high-latitude diet), or both ( , 8, and 9,N p 9respectively) with food replaced daily, and reweighed after7 days. Aplysia performance was quantified as relativegrowth rate in body mass, , since Aply-(ln M � ln M )/DT1 0

sia has a flexible body, a relatively long (16 months) post-metamorphic life span, and indeterminate growth; M1 andM0 represent the body mass in the end and at the beginningof the experiment, respectively.

Results

Patterns of Body-Size Variation in the Field

Two out of three species followed Bergmann’s rule, whileone species showed the opposite pattern. Prokelisia werelarger at higher latitudes, and females were larger thanmales (no latitude # sex interaction; fig. 1A). In contrast,Orchelimum were smaller at higher latitudes, with femalesagain larger than males (no latitude # sex interaction; fig.1B). Aplysia were an order of magnitude larger at highthan at low latitudes, but the relationship was stepwiserather than linear (fig. 1C). Aplysia were typically less than50 g in mass at most low-latitude sites but commonlyreached over 500 g at high-latitude sites in Japan and NewZealand.

Do Diets from Different Latitudes Affect HerbivorePerformance in the Laboratory?

In all three species, diet significantly affected herbivoreperformance. Prokelisia grew larger when fed plants from

272 The American Naturalist

Figure 1: Latitudinal variation in body size of Prokelisia (A), Orchelimum(B; data from Wason and Pennings 2008), and Aplysia (C). For Aplysia,numbers in parentheses indicate the number of independent observationsat each location: New Zealand (Willan and Morton 1984), Australia (P.D. Steinberg, personal communication), Brazil (Marcus and Marcus 1955and Marcus 1958 combined to make one data point), Tanzania (Beb-bington 1974), Barbados (Carefoot 1980), Hawaii (Edmundson 1946;Sarver 1978; Kay 1979; Switzer-Dunlap and Hadfield 1979; T. H. Carefoot,personal observations), Florida (Pilsbry 1951), Okinawa (T. H. Carefoot,personal observations; S. C. Pennings, personal observations), Japan(Saito and Nakamura 1961; Usuki 1970; S. C. Pennings and T. H. Care-foot, personal observations for two locations).

high- versus low-latitude regions (fig. 2A). As in the field,females were larger than males (fig. 2A), and there was nointeraction between plant region and sex ( ; tableP p .74A2 in the online edition of the American Naturalist). Or-chelimum grew faster when fed plants from high- versuslow-latitude regions (fig. 2B). In this case, sex neither af-fected growth rate (fig. 2B) nor interacted with plant region( ; table A2). Aplysia grew faster when fed Undaria,P p .70a major component of its diet at high latitudes, than whenfed Ulva, its diet at low latitudes (fig. 2C; table A2). Amixture of both Undaria and Ulva was not superior toUndaria alone.

Herbivore region did not affect Prokelisia body lengthor Orchelimum tibia growth rate ( and .91, re-P p .11spectively) but did interact with sex in the Orchelimumexperiment ( ; table A2). We did not address her-P p .04bivore region for Aplysia because we studied animals onlyfrom one geographic region.

Discussion

All three species grew faster or attained larger sizes whenfed foods representing a high- versus a low-latitude diet.This supports our hypothesis that variation in plant qualityacross latitude could contribute to explaining Bergmann’srule. The two species that follow Bergmann’s rule in thefield, Prokelisia and Aplysia, represent a dioecious, terres-trial species and a hermaphroditic, marine species, re-spectively. The fact that both show the same pattern revealsthe potential for plant quality to explain body-size patternsin herbivores representing different ecological systems andlife-history traits. Because plant quality is known to changeacross latitude in both marine and terrestrial systems (Bol-ser and Hay 1996; Siska et al. 2002; Wright et al. 2004;Toju and Sota 2006; C.-K. Ho and S. C. Pennings, un-published manuscript), latitudinal variation in plant qual-ity could help explain Bergmann’s rule in a wide varietyof herbivores.

Both phenotypic plasticity and heritable differences inbody size are likely to contribute to Bergmann’s rule. Forexample, studies on how environmental factors affect bodysize, that is, the temperature-size rule (Atkinson 1996),tend to explain Bergmann’s rule on the basis of phenotypicplasticity (Angilletta and Dunham 2003). In contrast, stud-ies of Drosophila have tended to focus on genetically basedvariation in body size among populations (Partridge andFrench 1996; Huey et al. 2000). Our field data could reflectthe result of both plasticity (to food quality) and heritabledifference in body size since these two factors are con-founded in the field. Our laboratory data, however, shouldsolely reflect plasticity in body size since the experimentaldesign controlled for herbivore origin. While this studywas not intended to untangle the relative importance of

Diet Quality and Bergmann’s Rule 273

Figure 2: A–C, Effect of diet on laboratory growth of Prokelisia (A), Orchelimum (B), and Aplysia (C). D, Body length of Prokelisia raised in thelaboratory on host plants from three latitudinal regions (X-axis) versus the body length of individuals collected in the field from three latitudinalregions (Y-axis). Dotted line indicates a 1 : 1 relationship. Data are means � 1 SE.

plasticity and genetic control, these two factors could berelated via genetic assimilation or accommodation (West-Eberhard 2005; Braendle and Flatt 2006) and deserve fur-ther investigation.

For Prokelisia, animals raised in the laboratory weresmaller than animals collected in the field (fig. 2D), likelyreflecting the fact that animals in the laboratory were notable to move among plants and select the most nutritiousones on which to feed. The variation in body size amongProkelisia raised on host plants from different latitudes(about an 8% increase from low- to high-latitude diets)was similar to the variation observed in the field (abouta 5% increase from low to high latitudes). This suggeststhat plant quality alone could explain Bergmann’s rule inProkelisia. Similarly, Prokelisia raised on plants from a sin-gle latitude grew 10% larger on fertilized than on control

plants (Cook and Denno 1994), again suggesting that var-iation in plant quality alone could explain the magnitudeof variation in body size observed across latitude. Spartinaplants from high latitudes are higher in quality likely be-cause they are softer and have a higher nitrogen contentand reduced chemical defenses compared with plants fromlow latitudes (Siska et al. 2002; C.-K. Ho and S. C. Pen-nings, unpublished manuscript). These differences in plantquality were constitutive, rather than induced by the en-vironment (Salgado and Pennings 2005).

For Aplysia, a high-latitude diet including Undaria in-creased growth rate by 55% (Undaria alone) to 72% (Un-daria and Ulva) compared to a low-latitude diet of Ulva.Such a difference in growth rate, compounded over severalweeks, would easily lead to the order-of-magnitude dif-ference in body mass observed in the field. In the case of

274 The American Naturalist

Aplysia, there is also evidence that latitudinal variation intemperature could play a role in body size. Aplysia grownthrough their entire postmetamorphic life at 20�C weretwice as big as those at 28�C (roughly, summer water tem-peratures of central Japan and Hawaii, respectively; Had-field and Switzer-Dunlap 1990). However, water temper-ature alone is unlikely to be the primary factor determiningbody size since water temperature varies continuously withlatitude, but the observed latitudinal pattern of maximumbody mass in Aplysia is discontinuous—a step function(fig. 1C). This step function is, however, consistent withthe pattern that might be produced by an abrupt shift toa new diet driven by the distributional limit of Undaria.In addition, the magnitude of variation produced by lab-oratory temperature experiments (twofold; Hadfield andSwitzer-Dunlap 1990) was too small to explain the vari-ation in the field (tenfold). We conclude, therefore, thatlatitudinal variation in diet could be a large part of theexplanation for Bergmann’s rule in Aplysia.

For Orchelimum, laboratory results were similar to thoseobtained with Prokelisia and Aplysia: a diet of high-latitudeplants led to faster growth than a diet of low-latitudeplants. In the field, however, Orchelimum showed the con-verse to Bergmann’s rule, which is observed less often thanBergmann’s rule (Atkinson 1994; Millien et al. 2006). Thissuggests that factors other than plant quality (or temper-ature) were more important in determining latitudinal var-iation in Orchelimum body size in the field. An explanationfor the converse to Bergmann’s rule is that the shortergrowing season at high latitudes selects for fast develop-mental time and, hence, smaller body size (Mousseau1997). Support for this hypothesis comes from the factthat Orchelimum is largely replaced at high latitudes by arelated long-horned grasshopper Conocephalus spartinaethat is about 33% smaller (Wason and Pennings 2008).Growing-season length might represent less of a constraintfor Prokelisia, which is multivoltine (Denno et al. 2003),or for Aplysia, which grows throughout the entire year (S.C. Pennings and T. H. Carefoot, personal observations).Since some salt marsh arthropods are more abundant atlow than at high latitudes (Pennings et al. 2009), anotherpossible explanation for the converse to Bergmann’s rulein field Orchelimum is that Orchelimum might eat a dietwith a higher proportion of animal prey at low latitudes,leading to better growth.

So far, our argument that latitudinal variation in plantquality could help explain Bergmann’s rule applies onlyto herbivores, but this argument could be extended tocover other types of consumers. For example, high-qualitylitter derived from high-quality plants might support bet-ter growth of detritivores at high latitudes (Greenwood etal. 2007, for a local example). Because parasitoids canattain larger sizes in larger hosts (Kouame and Mackauer

1991), latitudinal variation in herbivore body size mightalso drive latitudinal variation in parasitoid body size. Sim-ilarly, larger herbivores at high latitudes might supportlarger body sizes in predators. Even if these speculationsare not borne out in future studies, herbivores representa large proportion of animals, and so our results mayrepresent an important, if partial, mechanism contributingto Bergmann’s rule.

In this note, we have emphasized the importance of dietin contributing to Bergmann’s rule because this mecha-nism has been largely overlooked (but see Stillwell et al.2007). We do not intend to dismiss the importance ofabiotic factors (e.g., temperature, rainfall) in also contrib-uting to latitudinal variation in body size. Rather, we wouldsuggest that, in many cases, Bergmann’s rule may be bestexplained by some combination of biotic and abiotic fac-tors, rather than any single, universal explanation. In par-ticular, a large number of laboratory studies have shownthat variation in temperature can affect body size (An-derson 1973; Partridge et al. 1994; Atkinson 1996). Asmentioned above, temperature probably plays a role inlatitudinal variation in Aplysia body size but by itself can-not explain the shape or the magnitude of the body-sizevariation. In addition, biotic factors (such as food quality)might interact with abiotic factors to drive the pattern ofbody size. For example, life-history theory suggests thatcolder environments (i.e., high latitude) favor organismswith delayed maturation and bigger adult size. In the field,better food quality at high latitudes might enable organ-isms to tolerate a harsh environment and delay matura-tion. Furthermore, if biotic interactions (i.e., predator-preyinteractions) vary across latitude, then higher predationpressure might select for larger prey because of size refugesfrom predation (Werner et al. 1983; Bronmark and Miner1992) or smaller prey because of early maturation (Wilburand Fauth 1990). Therefore, we encourage future studiesof Bergmann’s rule to expand beyond a focus on abioticfactors to consider diet and other biotic factors that mightinteract with abiotic factors to produce latitudinal varia-tion in body size.

Acknowledgments

We thank the National Oceanic and Atmospheric Admin-istration’s National Estuarine Research Reserve (NERR)Graduate Research Fellowship (GRF) program (NA04NOS 4200137), National Science Foundation (OCE99-82133, DEB-0296160, 0638796, 0709923), and Natural Sci-ences and Engineering Research Council of Canada forfunding and the Ashepoo, Combahee, and Edisto BasinReserve for serving as the GRF host reserve. We thank stafffrom 12 NERR and three Long-Term Ecological Research(LTER) sites, especially L. Blum, T. Buck, C. Buzzelli, M.

Diet Quality and Bergmann’s Rule 275

Dionne, R. Gleeson, C. Hopkinson, D. Hurley, M. Ken-nish, P. Kenny, K. McGlathery, P. Murray, K. O’Brien, J.Porter, K. Raposa, W. Reay, R. Scarborough, B. Smith, B.Stankelis, B. Stroud, B. Truitt, C. Weidman, H. Wells, E.L. Wenner, and C. Zemp, for assistance. We thank R. Aze-vedo, B. Cole, R. Denno (1945–2008), T. Frankino, E.Siemann, M. Travisano, and two anonymous reviewers foradvice and comments on the manuscript. This work wouldnot be done without support from Y. Chung, C.-Y. Ho,H.-C.-M. Ho, A. Lynes, F.-J. Sha, L. Wason, and K. Wieski.This is a contribution of the Georgia Coastal EcosystemsLTER program and contribution 987 from the Universityof Georgia Marine Institute.

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Associate Editor: Maydianne C. B. AndradeEditor: Mark A. McPeek