tidal flat macrofaunal communities and their associated...

Estuaries Vol. 23, No. 1, p. 97-114 February 2000

Tidal Flat Macrofaunal Communities and Their Associated

Environments in Estuaries of Southern California and Northern

Baja California, Mexico

THERESA SINICROPE TALLEY 1

P AUL K. DAYTON

Marine Life Research Group Scripps Institution of Oceanography La Jotla, California 92093 0201

SILV2A E, IBARRA-OBANDO Centro de Investigaeidn C~entifica y de Educaci5n ,Superior de Ensenada (CICESE) Km 107, Ca, rretera Tijuana to Enser~ada Baja California, Mexico

ABSTRACT: Several tidal flats in both Estero de Pnnta Banda and Bahia de San Qnintln~ Baja Calffornia~ and one in Mission Bay, s o u t h e r n California~ were s a m p l e d fo r macro fauna l p roper t i e s ( taxonomic composition~ density~ species richness~ a n d func t iona l g roups fo r an imals >0 .3 ram) and associa ted env i ronmenta l variables ( sed iment proper t ies , salinity, p l an t be lowground biomass, and cover of Zostera mar/ha) in o rde r to establish a benchmark data set for these areas. T h e g roup ing o f m a c r o f a u n a into h igher t axonomic or func t iona l g roups for these compar i sons r e d u c e d variability and revealed s t ronger relat ionships. Each es tuary had a fairly distinct macro fauna l assemblage~ with that of Estero de Pnnta Banda be ing d i f fe ren t f r o m Bahia de San Qnin t in a n d Mission Bay pr imari ly due to d o m i n a n c e by a capitell id polychaete, lower p ropor t i ons of sur face depos i t feeders~ a n d h igher p ropor t i ons of f a u n a with a planktonic stage. T h e flats in Mission Bay a n d Bahia de San Quin t ln were domina t ed by peracar id crttstaceai~s, o l igochaetes and polychaet~s and had higher proport im~s of direct developers and mac ro fauna with mobi le adtdt s tages than did Estero de Punta Banda. T h e r e was an overlap o f the env i ronmenta l characterist ics a m o n g estuaries~ with m o r e variability o f s e d i m e n t and vegetat ion proper t i es within than a m o n g estuaries. Within Bahia de San Quint in , there was an oceanic to back-bay distr ibution g rad ien t of m a c r o f a u n a that was similar to that f o u n d in es tuar ies in wetter climates~ despi te the lack of a salinity g rad ien t in S an Quint in . A decoupl ing o f the ben thos and the a s s u m e d an thropogenic s t resses was obse rved with the d e g r a d e d site~ Mission Bay~ be ing mos t s imilar to the relatively pr is t ine Bahia de San Quint ln . Selection of r e fe rence si tes and sampl ing variables s h o u l d be m a d e cautiously because effects o f d i s tu rbance fac tors on the ben thos may be s i te -dependent , sca le-dependent , or negligible.

In t roduct ion

The coastal wetlands of California are an endan- gered habitat due to the loss of 90% of their orig- inal area, and the f ragmentat ion and degradat ion of the r e m a i n i n g areas t h r o u g h u r b a n i z a t i o n (Schoenher r 1999). In comparison, the estuaries of no r the rn Baja California show comparatively lit- tle effect of man, yet they face potential development and enc roachmen t as has been experienced by the estuaries of southern California. An under- standing of faunal and environmental condit ions is therefore especially impor tant in these Mexican estuaries bo th for future within-estuary comparisons and for their potential use as reference sites for the urbanized estuaries of southern California. This paper examines the macro-infaunal (animals

Cor re spond ing author; e-mail: s inicrope@coast .ucsd.edu.

-~ 0.3 ram) communit ies on the intertidal mudflats in two estuaries in Baja California and one estuary in southern California in order to establish a benchmark data set of tidal flat macrofauna, examine the environmental variables that are associated with the macrofaunal assemblages, and con- sider the feasibility of making comparisons among these systems.

Benchmark, or point of reference, data sets allow for comparisons to be made both within one system across time (e.g., before and after a distur- bance event) and between systems at any one time (e.g., disturbed versus pristine systems). Bench- mark data sets can be as simple as a list of the species present (Droege et al. 1998) or can include assoc ia ted e n v i r o n m e n t a l i n f o r m a t i o n . Unde r - standing the relationships between the species present and their env i ronment can give insight as to the processes structuring a system, and may allow

�9 2000 Estuarine Research Federation 97

98 T.S. TalIw ot al.

basic predictions to be made as to how disturbanc- es or changes in the envi ronment might affect species assemblages.

Estuaries in arid climates occur th roughou t the world (Adam 1990), yet informat ion on the macro- infaunal communit ies and associated environmental parameters of arid intertidal mud and sand flats, such as those examined in this study, is limited. It is well documen ted that macro-infaunal communit ies play an impor tan t role in the transfer of energy and nutrients within and between benthic habitats (subtidal and higher intertidal areas such as salt marshes) and with the pelagic zone (e.g., Levinton 1982; T h o m p s o n et al. 1998; tQleib 1997 and references therein).

The tidal flat habitats examined in this study have enjoyed a certain amoun t of attention, al- though the studies generally focused on one taxon and, when faunal assemblages were examined, the fauna were larger than those sampled here (non- annelids -> 1 mm, annelids -> 0.5 mm) a n d / o r were located subtidally (except Levin et al. 1998). For example, there are numerous such studies of benthic fauna in Mission Bay in southern Califor- nia (MacDonald 1969a,b; Levin 1981, 1982a,b, 1984; Dexter 1988; Crooks 1996, 1998; Levin et al. 1998), and Estero de Punta Banda (De Ita-Gargallo 1982; Von Son-Gallut 1991; Wauman-Rojas 1998) and Bahia de San Quintfn (Keen 1962; Reish 1968; Barnard 1964, 1970; MacDonald 1969a,b; Cook 1974; Bretado-Aguirre 1987; Cantfi-Martfnez 1987; Griffis and Chavez 1988; Calderon-Aguilera 1992; Dfaz-Castafieda and Rodrfguez-Villanueva 1998) in no r the rn gaja California. Our study focuses on smaller organisms (0.3 m m to approximately 1 mm in size) of intertidal macro-infaunal communities. Levin et al. (1998) found that a 0.3 m m mesh opening retains the smaller individuals of the same taxa that are found in screens with the larger, com- monly used apertures (0.5 and 1 ram), thereby al- lowing a more accurate estimate of the density and size distribution of each taxon.

S t u d y L o c a t i o n s

Tidal flats cont iguous with salt marshes were sampled within 3 estuaries in southern California and Baja California (Fig. la) . Mission Bay, located in southern California (32~ 117~ contains one 0.46-km 2 salt marsh. Estero de Punta Ban- da (EPB) (31~ 116~ located just south of Ensenada about 100 km south of the Mex ico / United States border contains g.3 km e of salt marsh ( Ibarra-Obando and Poumian-Tapia 1991). Two of the marsh areas were sampled in this study. We sampled four areas within Bahia de San Quinffn (BSQ), which is located about 400 km south of the

border (B0~ 116~ and contains 10.8 km e of salt marsh.

Mission Bay is completely su r rounded by intense urban development in contrast to the land adjacent to the Mexican estuaries that includes small amounts of development and agriculture as well as undeveloped natural areas. Freshwater input into the tidal flat studied in Mission Bay is limited to seasonal storm inputs (mostly street runoff) that flow in a channel to the eastern side of the tidal flat. The flats in Mexico have no constant freshwater inputs and experience only seasonal freshwater storm inputs.

The tidal flat surveyed within Mission Bay is located roughly 5 km from the m o u t h of the estuary and is about 30-50 m wide from the salt marsh to the upper edge of Zostera mavir~a (eelgrass, here- after referred to as Zostera) (Fig. lb). The two flats surveyed within Estero de Punta Banda are La Boca (2.8 km from the mouth) and Campo Chan- oc (4.6 km from the mouth) (Fig. lc) . La Boca flat is an expansive unvegetated sand flat that leads gradually into the subtidal, while the flat at Campo Chanoc is a smaller flat (15-20 m from marsh edge to Zostera edge) that leads into a tidal creek. Four flats were studied in Bahia de San Quintfn (Fig. ld) , the first of which consists of a flat on the sand spit, or Tombolo, border ing the western side of the estuary. This site is closest to the mouth of the estuary (5.5 km from the mouth) and gradually slopes into the subtidal (about 60-75 m from marsh to Zostera edge). The tidal flat at the head of Bahia Falsa is 8.5 km from the m o u t h and is located at the head of the western side of the estuary. The mudflat in this area is expansive and stretches about 100-150 m before the Zostera zone begins. The tidal flat east of the volcano Kenton, in the eastern part of the estuary, is roughly 11 km from the mou th and gradually slopes into the subtidal (about 20-30 m from marsh to Zostera edge). The Nor th Marsh is located at the head of the eastern arm of the estuary, the farthest distance from the m o u t h of the estuary (16 km). This area is the least well flushed and has about 20-30 m of mudflat between marsh and Zostera edge. It receives organic inputs f rom the municipal development and agriculture along this side of the estuary.

Mater ia l s a n d M e t h o d s

Vegetated (Zostera) and unvegetated areas of the tidal flats were sampled for infauna and sediments within an elevation range of 0-1 m above mean lower low water (MLLW) from April 26, 1996 to August 10, 1996 (Table 1). The upper limit of Zos- tera occurs in this tidal range, and so patches of seagrass (5-30 cm in length, 25-50% cover), as well as unvegetated areas, are characteristic of this

]]

I

Tidal Flat Macrofaunal Communities 99

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C D I I

Fig. 1. Map of the study si tesin southern and Baja California. Areas in Mack represent intertidal mudflat and adjacent salt marsh habitat. (A) Location of the estuaries. (B) Location of the tidal flat in Mission Bay (shown in black). (C) Locations of the tidal flats (X) in Estero de Punta Banda, Baja California. (D) Locations of the tidal flats (X) in Bahia de San Quint[n, San Quintfn, Baja California.

intertidal zone. In each of the sites, three samples (25 m apart) were collected from the vegetated and unvegetated areas, except in La Boca (EPB) where there was no vegetation (i.e., 6 unvegetated samples collected). Only g of the cores (unvege- tared) were collected from Kenton, so these data were excluded from the between-site comparisons and included only in the regression analysis that is discussed below.

All environmental and macrofaunal propert ies were measured within a 0.25 m z quadrat. Percent cover of Zostera and porewater salinities were measured in the field. Porewater was extracted from sediments by squeezing the sediments against a small circle of Whatman No. 2 filter paper inside of a 10-cc syringe. The infauna and sediment samples were each collected within 5 cm of each other

using an 18 cm ~ X 6 cm-deep core. Extruded sediments and infauna from the core were preserved in 8% buffered formalin and stained with Rose Bengal. In the lab, this material was sieved th rough 0.3-mm aperture mesh. All animals were removed from the ->0.3 mm fraction, identified to the lowest taxonomic level possible and stored in 70% eth- anol. Live and dead plant belowground material, consisting of roots, rhizomes and some detritus (->0.3 mm) , that was found in the infaunal cores was also removed and dried for estimates of plant be lowground biomass. Core samples for sediment propert ies were stored on ice until re turned to the laboratory (no more than 3 d later), at which point they were frozen at 20~ These sediments were later analyzed for percent organic matter and sand content after sieving th rough a 2-mm aper ture

100 T. S. Talley et al.

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Statistical A n a l y s i s

Compar i sons of sed iment p roper t ies (pe rcen t organic ma t t e r and sand contents) , vegeta t ion (percent cover of Zostera and be lowground biomass) and macro fauna l p roper t i e s (species richness [or n u m b e r of species] pe r core, a b u n d a n c e of total m a c r o f a u n a per core, p ropor t iona l abundances of major t axonomic groups, and p ropor - tional abundances of funct ional groups) within and between the estuaries were made using analysis of var iance (ANOVA) and a poster ior i Stu- dent ' s t-tests (JMP statistical software). Each macrofaunal species (or h igher taxon) was assigned to funct ional g roups (adult mobility, reproduct ive modes , and t rophic groups) based on the literature (Wirth and Stone 1963; Lasserre 1971; Fau- chald and J u m a r s 1979; Diaz 1980; Morr is et al. 1980; Giere and P fannkuche 1982; Levin 1984; Mighsmith 1985; Levinton and Stewart 1988; Wil- son 1991; Holmquis t 1994; Levinton et al. 1995; Crooks 1998). Species richness as a funct ion of n u m b e r of individuals was examined by calculating rarefact ion curves (Hur lbe r t 1971). In cases where the taxa could not be identified to species (i.e., some ol igochaetes and amph ipods ) , families were used. This provided a conservative estimate of species r ichness and will be re fe r red to as taxa richness t h r o u g h o u t this paper.

Differences and similarities in macrofauna l communi t ies ( abundances of each taxon) were examined using non-met r ic mul t id imens iona l scaling (MDS; see Clarke and Green 1988; Clarke 1993) on Bray-Curtis similarity indices of t r ans fo rmed (log~0(x + 1)) data. Analysis of similarity (ANO- SIM) was used to assess differences in c o m m u n i t y compos i t ion (taxa abundances and p ropor t iona l abundances of funct ional groups) and environmen ta l p a r a m e t e r s (organic ma t t e r content , sand content , pe rcen t cover of Zostera, plant below- g round biomass) a m o n g sites. Taxa abundances and funct ional g roup p ropor t iona l abundances were also used to de t e rmine the pe rcen t of similarity (SIMPER) within and a m o n g sites, and which taxa or groups were responsible for any differences. ANOSIM, SIMPER, and MDS analyses were run using Pr imer software (Clarke and Warwick 1994). A stress value, which is a measure of how well the two-dimensional MDS plot represents the distances

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Mean ( • SE) macrofaunal density (A), taxarictmess per core (B), and rarefaction curves (tmxa richness as a funct ion o f n u m b e r of individuals) (C) for each tidal flat studied in southern California (Mission Bay) and Baja California (Estero de Ptmta Bands and Bahia de San Quint ln) . n 10 cores (18 crn 2 x 6 c m depth) for Mission Bay and n = 6 cores for Baja California�9 Rarefaction data were poo led within each site (i.e., n = 1). Data were col lected April 26 to August 10, 1996. Dif- ferent letters indicate significance, p 0�9 a posteriori t-test. ANOVA p and F values are shown.

between the data, is shown with the MDS plot. Clarke (199S) suggests that stress values of <0.2 indicate useful representations.

Numerical abundances of the dominant macrofaunal taxonomic groups were analyzed by linear stepwise forward multiple regressions (Statistics statistical software) to identify relationships between the macrofaunal and environmental variables. Linearity of relationships was tested prior to the multiple regressions using simple regressions (JMP statistical software). The environmental variables considered in the multiple regressions were the same as those listed above for the Primer analyses. Relationships between macrofaunal taxonomic group abundances and environmental variables, including distance of each tidal flat from the mouth of the estuary, were examined with multiple regressions using data from San Quintfn, where

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All p ropor t ion data were t ransformed using arc- sin square root and integer data were t ransformed using lOgl0(X + 1) prior to all statistical analyses in order to normalize the data, homogenize varianc- es, and emphasize multiplicative effects. Means and standard errors were back-transformed for presentat ion and are the values presented through- out the text.

Sites were used as the sampling units for all statistical analyses except the multiple regressions where data from all sites were pooled (see Table 1 for n u m b e r of cores [i.e., sub-samples] per site). For the multiple regression analyses, the sub-sample, or core, data were not averaged within sites because the macrofaunal and environmental cores at each sub-sample location were paired (collected within 5 cm of each other) in order to examine correlations between the two. Averaging these data would have caused a loss of resolution of the relationships between the macrofaunal and environmental variables.

Results

ENVIRONMENTAL PROPERTIES

The two tidal flats located at the heads of the San Quintfn estuary, Bahia Falsa and Nor th Marsh (see Fig. ld) , contained higher organic matter (7- 12%) and lower sand (15-S6%) contents than the other sites (organic matter 1-3%; sand 72-93%) (Table 1). No significant differences in the cover of Zostera or plant be lowground biomass (g dw) were found between sites (Table 1). Porewater salinities remained about that of seawater (35-38%o) both within and between sites. Analysis of similarity (ANOSIM) revealed that there were not many significant differences (p -< 0.003, Bonferroni adjust- ed alpha) among the suite of environmental variables that were measured in each site (Table 2a). The differences that were observed were mostly due to differences in the sediment propert ies (organic matter and sand content) among sites (Table 1).

As with most ecological data, some of the envi- r o n m e n t a l variables m e a s u r e d were cor re la ted with each other. When the data from all sites were pooled, organic matter and sand contents were


strongly and negatively correlated (r e - 0.60; p < 0 . 0 0 0 0 1 ; F1,41 - 61.4). The percent cover of Zostera was positively correlated with plant belowground biomass (g dw) (r e - 0.51; p < 0.00001; F1,~9 - 39.9). There were no correlations between Zostera cover, and sand or organic matter contents of the sediment. Within Bahia de San Quintln, the distance from the m o u t h of the estuary was strongly correlated with organic matter content (r ~ - 0.80; p -< 0.00001; Fro9 - 74.0) and was negatively correlated with sand content (r 2 - 0.55; p - 0.0001; Fa, m - 23.7). There was no oceanic to back-bay gradient of Zostera cover or plant belowground bio- I i lasS.

INFAUNAL PROPERTIES

Density and Taxa Richness

Mean (+ 1 SE, n - 6) macrofaunal densities and taxa richness per core tended to be highest in the Mission Bay and Tombolo (BSQ) tidal flats (258 _+ 24-334 _+ 143 ind per core and 17 _+ 2-18 _+ 2 taxa per core) and lowest at La Boca, Campo Chanoc (EPB), and Nor th Marsh (BSQ) (72 + 26- 133 _+ 89 ind per core and 8 _+ 1-11 _+ 3 taxa per core; Fig. 2a,b). Taxa richness per n u m b e r of individuals (rarefaction curves) showed Bahia Falsa (BSQ) and Mission Bay as having the highest richness, with La Boca, the site nearest to the m o u t h of Estero de Punta Banda, having the lowest richness (Fig. 2c).

Infaunal Composition

P@chaetes. Mean (_+ 1 SE, n - 6) propor t ions of polychaetes were highest within Estero de Punta Banda (57 + 8% in Campo Chanoc to 78 + 12% in La Boca), in termediate at the San Quintfn sites (29 + 7%-47 + 5%), and lowest in Mission Bay (22 + 3%) (p -< 0.00001; F~,e4 - 8.1; Fig. 3). The polychaetes in the Estero de Punta Banda sites pre- dominantly consisted of the capitellid, Medioraastus ambiseta (Fig. 3). Numer i ca l l y d o m i n a n t polychaetes in the tidal flats of San Quint ln were syllid polychaetes including Exogone cf. lourei and two previously unidentif ied species of Brania (Table 3). Mission Bay had no one dominan t polychaete, and no estuary contained polychaete taxa that were ex- clusive to that estuary.

Oligochaetes. Mean (+1 SE, n - 6) propor t ions of oligochaetes were highest in the Nor th Marsh (BSQ) (50 _+ 10%), intermediate in Bahia Falsa, Tombolo (BSQ), and Mission Bay (19 -- 3%-27 _+ 9%), and lowest in the flats of Estero de Punta Banda (0 + 0%-6 + 6%) (p -< 0.00001; Fs, ea - 11.9; Fig. 3). Tubificid oligochaetes were the dominant oligochaetes in all areas except the head of Bahia Falsa where the enchytraeid oligochaete, En-

'I 06 T. 8 . Talley e t al.

�9 Polychact~s [] M~flluscs [] Insects [] O~he[ [] Oligochaet~ I-1 Ctllgt~occat~s [] Neii~rteans &Turlmeliari~ns

Mission Bay La Boca Campn ('halloc Tor~olo Bahia Paisa North Marsh Estcro de Punta Banda _ _ Bahia de San Quintfn _ _

Increased distance from mouth

Fig. 3. Mean percent composition of the higher macrofaunal taxonomic groups found in the tidal flats of Mission Bay, southern California and in Estero de P'Lmta Banda and Bahia de San Quint/n, Baja California. n 10 cores (18 cm ~ • 6 cm depth) in Mission Bay and n = 6 cores in Baja California. Data were collected April 26 to August 10, 1996.

chyt, raeus sp., was numer ica l ly d o m i n a n t (Fig. 3, Ta- ble 3).

Crustaceans. M e a n (_+1 SE, n - 6) c rus t acean densit ies were p r o p o r t i o n a l l y h ighes t in Mission Bay (48 + 6%) and lowest in La Boca, C a m p o C h a n o c (EPB), and N o r t h Marsh (BSQ) (7 + 5 % - 10 _+ 5%) (p - 0.001; F~,e4 - 5.2; Fig. 3). In all sites excep t La Boca, all or m o s t o f the c rus taceans were pe raca r id c rus taceans (Table 3). T h e tanaid, Leptochelia dubia, was numer ica l ly the mos t com- m o n in Mission Bay and Bahia Falsa. A m p h i p o d s f rom the s u b o r d e r G a m m a r i d e a were also com- m o n in Mission Bay. C o r o p h i i d a m p h i p o d s (in- c luding Corophiura spp. and the exotic Grandidierel ta japonica) compr i sed a small p r o p o r t i o n o f the total m a c r o f a u n a in all sites. A n o t h e r pe raca r id f o u n d in low n u m b e r s (0.3-1 ind pe r core) on the flats of the wes tern side of San Qu in f fn was an undescr ibed species of lep tos t racan , Nebalia sp. Ne- batia was f o u n d only in the Zostera-vegetated samples o f the H e a d of Bahia Falsa and the T o m b o l o . In La Boca, the numer ica l ly d o m i n a n t c rus t acean was the d e c a p o d , Uca cre~zutata (f iddler crab) .

Insects. M e a n (+1 SE, n - 6) p r o p o r t i o n a l abun - dance of insects (bo th larvae and adults) was signif icantly h ighes t at Bahia Paisa (BSQ) (11 _+ 3%) , i n t e r m e d i a t e at N o r t h Marsh, T o m b o l o (BSQ) and Mission Bay (0.6 _+ 0 .5%-3 _+ 2%) and n o n e were f o u n d on the flats of Estero de P u n t a B a n d a (p < 0.00001; F;.s4 - 8.3; Fig. 3). Pa t t e rns o f insect density were similar to tha t of their p r o p o r t i o n a l abun - dances (Fig. 3; Table 3). C h i r o n o m i d larvae were the numer ica l ly d o m i n a n t insect type (Table 3).

Ne'merteans and Turbeltarians. M e a n ( + 1 SE, n - 6) p r o p o r t i o n s o f n e m e r t e a n s and turbel la r ians were h ighes t in the flats o f Estero de P u n t a B a n d a (13 + 8 % - 1 5 + 7%) , i n t e rm ed ia t e in the N o r t h Marsh (BSQ) (6 + 2%) and lowest in the T o m b o l o

a nd Bahia Falsa flats (BSQ) a nd in Mission Bay (1 + 0 .4%-2 + 0.6%) (p - 0.01; F;s4 - 3.3; Fig. 3).

Molluscs. P r o p o r t i o n a l a b u n d a n c e s ( m e a n + 1 SE, n - 6) o f mol luscs did n o t differ s ignif icantly be tween sites (0.2 -+ 0 .2%-9 -- 6%) (p - 0.20; Fbea - 1.6; Fig. 3). Small densit ies o f bivalves (0.2 + 0.2 ind pe r core) were f o u n d at the Estero de P u n t a B a n d a sites (Table g). T h e exotic J a p a n e s e mussel , Museulista senhousia, was only f o u n d in Mission Bay (2 + 1 ind pe r core) . N o bivalves were col lec ted in these 18-cm ~ cores f r o m the flats in San Quint fn . T h e o p i s t h o b r a n c h Acteocina incutta was f o u n d in all flats (0.2-5 ind pe r core) excep t the N o r t h Marsh (BSQ). Ba, rleeia subtenuis (P rosobranch ia ) was no t f o u n d in Estero de P u n t a g a n d a , bu t was p re sen t in Mission Bay and all flats in San Q u i n t f n excep t N o r t h Marsh. T h e T o m b o l o had 4 d i f fe ren t taxa of gas t ropods , Bah ia Falsa had 3 taxa and the o the r sites had 1 or 2 taxa. T h e seagrass l impet , Notoacrnea @icta, was f o u n d only on the seagrass in the N o r t h Marsh.

Other Taxa. T h e m e a n (--1 SE, n - 6) p r o p o r - t ional a b u n d a n c e o f the ca t ego ry of o t h e r taxa did n o t differ be tween sites (p - 0.18; Fss4 - 1.6; Fig. 3). H o l o t h u r o i d s were f o u n d in all estuaries; pho- ron ids were rare in Mission Bay a nd Estero de Pun- ta Banda , a nd lacking f r o m the samples f rom San Quin t fn . A n e m o n e s were only f o u n d in Mission Bay, i nc lud ing the invasive, exotic a n e m o n e , Bun ode@sis sp. (Table 3).

Functional Groups Trophic Groups. P r o p o r t i o n s o f surface deposi t

feeders , the d o m i n a n t t roph ic g roup , di f fered a m o n g estuaries (ANOVA, p - 0.01, F~,~ - 3.4) with genera l ly h i g h e r p r o p o r t i o n s in Mission and San Q u i n t f n Bays (51 -68%) than in Estero de Pun- ta B a n d a (35 -40%) (Fig. 4a). P r o p o r t i o n a l abun - dances of subsur face depos i t feeders , the s e c o n d m o s t d o m i n a n t t roph ic g r o u p , did n o t differ a m o n g sites (26 -39%) (Fig. 4a) (ANOVA, p - 0.64). P r o p o r t i o n s of suspens ion feeders were h i g h e r in Mission Bay and C a m p o C h a n o c (EPB) (10 -11%) t h a n in the Bahia de San Q u i n t f n sites (0 -2%) (Fig. 4a) (ANOVA, p - 0.008, F;,s~ - 3.8). T h e sites in Estero de P u n t a B a n d a c o n t a i n e d h igher p r o p o r t i o n s (20 -21%) of carn ivores than in Mis- sion Bay, or T o m b o l o and Bahia Falsa (BSQ) (5 - 7%) (Fig. 4a) (ANOVA, p - 0.005, F~,s~ - 4.2).

Life-history Strategies. P r o p o r t i o n s of d i rec t developers were signif icantly h i g h e r (64 -77%) (ANO- VA, p < 0.00001, F;,s~ - 45.0), while the p r o p o r - t ions of taxa with a p l ank ton i c stage were signifi- cantly lower ( 2 3 - 3 6 % ) (ANOVA, p _< 0.00001, Fs.~s

- 45.0) in Mission Bay and Bahia de San Q u i n t f n than in Estero de P u n t a B a n d a (direct deve lope r 3 -28%; p l ank ton i c stage 7 2 - 9 7 % ) (Fig. 4b). T h e


M~sgicm Bay Ester de Ptlnla Banda P,a'nia de San Quintfn

1~ ~oca Caml~ ('hallo: Tomboln Bahia FaI~ North Marsh A. Tmphlc Nl*up8

SurI~ee dei~sit [etmer ~ 5~lspeesSolt [eeller Suh~un~a~ delXtgtl ~de l k~ ~ . 'mU~

B. Rr clive g~c, ups

Mobile aduhg: 30% 37,% 21% 08% 8 % 18%

Fig. 4. Mean percent composition of the macrofaunal txo- phic groups (A) and reproductive groups (B) found in the tidal flats of Mission Bay, southern California and in Estero de Punta Banda and Bahia de San Quintin, Baja California. Also shown is the percent of total macrofauna that have a mobile adult stage, n = 10 cores (18 cm~ • 6 cm depth) in Mission Bay and n 6 cores in Baja California. Data were collected April 26 to August 10, 1996.

taxa with a mobi le adul t phase were also p ropo r - t ionally h ighe r in Mission Bay and Bahia de San Qu in f fn (18 -37%) than in Estero de P u n t a B a n d a (1 -8%) (ANOVA, p < 0.00001, F~,~s - 16.3) (Fig. 4b).

Comparisons Between Estuaries

Mul t id imens iona l scaling (MDS) analysis o f macro fauna l assemblages f r o m each of the flats revealed a gene ra l d is t inc t ion be tween each of the estuaries (Fig. 5; stress - 0.19; Analysis o f Similarity [ A N O S I M ] , p < 0.015) a l t h o u g h c o m p a r i s o n s between individual sites were no t always s ignif icant at the B o n f e r r o n i adjus ted a lpha of 0.003 (Table 2b). T h e Mission Bay m a c r o f a u n a l assemblage was the m o s t similar to the sites in San Q u i n t / n ( 29 -35% similarity) (Table 2b; Fig, 5), T h e h igh a b u n d a n c e s of tubificid o l igochae tes in b o t h estuaries accoun t - ed for mos t of the h om ogene i t y . M a c r o f a u n a l assemblages in Estero de P u n t a B a n d a were jus t as d i f fe ren t f r o m those in Mission Bay (12-15% similar) as those in San Q u in f fn (11 -16% similar) (Ta- ble 2b). H i g h a b u n d a n c e s of the capitell id Medi omastus ambiseta in Estero de P u n t a B a n d a accoun t - ed for the d i f fe rences in m a c r o f a u n a l assemblages be tween Estero de P u n t a B a n d a and the o t h e r estuaries.

Analysis of similarity (ANOSIM) using the tro- ph ic g r o u p s revealed tha t the re were few significant d i f fe rences in faunal t roph ic c o m p o s i t i o n a m o n g sites (Table 4a). T h e t roph ic c o m p o s i t i o n of La Boca (EPB) was signif icantly d i f fe ren t f r o m that f o u n d in Mission Bay and T o m b o l o (BSQ). Similarity p e r c e n t a g e (SIMPER) analysis of the tro- ph ic g r o u p s revealed that the re was slightly m o r e

-2 2

O 0

o mm A a a � 9

�9 0 0

�9 m l �9 �9

-'1 6 i Dimension 1

Miss ion Bay

I Estero de Punta Baltda Bahia de San Quint ln I

�9 La Boca �9 Tombolo I �9 B a h i a F a f s a

o C a m p o C h a n o c �9 N o r t h M a r s h

Fig. 5. Multidimensional scaling ofmacrofaunal abundances within tidal flats of Mission Bay, southern California and in Es- tero de Punta Banda and Bahia de San Quintin, Baja California. Stress value 0.19. n 10 cores (18 cm ~ x 6 cm depth) in Mission Bay and n = 6 cores in Baja California. Data were collected April 26 m August 10, 1996.

similarity be tween Mission Bay and the sites in Ba- h ia de San Q u i n t i n (80-83% similar) than be tween Estero de P u n t a B a n d a and e i ther of those two estuaries ( 64 -79% similar). This was main ly due to the lower p r o p o r t i o n s of surface depos i t feeders in Estero de P u n t a B a n d a relative to the o the r two estuaries.

Analysis of similarity using the r ep roduc t i ve m o d e c o m p o s i t i o n showed signif icant d i f fe rences (p -< 0.001) be tween b o t h Mission Bay and Bahia Falsa (BSQ) and the two sites in Estero de P u n t a B a n d a (Table 4b), T h e o t h e r sites in San Q u i n f f n (Nor th Marsh and T o m b o l o ) were signif icantly dif- f e ren t only f r o m La Boca (EPB) with respec t to r e p r o d u c t i o n g r o u p compos i t ion . H o m o g e n e i t y was h igh be tween Mission Bay and the sites in Ba- h ia de San Q u i n t i n (87 -91% similar) and low between Mission Bay and the sites in Estero de P u n t a B a n d a (29 -53% similar). T h e r e was also low ho- m o g e n e i t y in the r e p roduc t i ve g r o u p compos i t i ons be tween the sites in San Q u i n f f n and Estero de P u n t a B a n d a ( B S Q v e r s u s C a m p o C h a n o c 5 0 - 6 2 % similar; B S Q v e r s u s La Boca 2 6 - 4 0 % similar). Th i s was due to h igh p r o p o r t i o n s of taxa that have a p l ank ton i c stage in Estero de P u n t a Banda , and h igh p r o p o r t i o n s of di rect deve lopers in Mission and San Q u i n t i n Bays.

Cofapa~isons Within Estuaries

T h e r e was m o r e h o m o g e n e i t y o f m a c r o f a u n a l assemblages within Estero de P u n t a B a n d a (26% sim-

'I 0 8 T.S. Talley et al.

TABLE 4. C o m p a r i s o n s o f m a c r o f a u n a l (A) t r o p h i c a n d (B) r e p r o d u c t i v e g r o u p s wi th in Mission Bay, s o u t h e r n Ca l i fo rn i a a n d Es te ro de P t m t a B a n d a a n d Bahia de San Q u i n t / n , Baja Cal i forn ia . A N O S I M pa i rwise tests above d i ag o n a l , S IMPER w i t h i n - g r o u p s imilar i ty p e r c e n t a g e on the d i a g o n a l (bo ld ) , S IMPER be tw-een-group diss imilar i ty p e r c e n t below- d i ag o n a l . A l p h a s h o u l d be se t a t 0.003 us ing the B o n f e r r o n i a d j u s t m e n t f e r A N O S I M p values. N o va lue i nd i ca t e s n o s igni f icance . Da ta were co l l e c t ed b e t w e e n Apr i l 26 to A u g u s t 10, 1996, n = 10 co res (18 cm~ • 6 c m - d e p t h ) fo r Mission Bay a n d n = 6 fo r the Baja Ca l i fo rn i a sites.

A Trophic groups Estero de Puata Barada S~n Quindr~

Mission Bay L~ Boc~ Campo Qh~noc Tombolo B~hia F~lsa North Marsh

Mission Bay 85 p 0 .002 . . . . Es te ro de P u n t a g a n d a La Boca 73 77 - - p = 0 .002 - - - -

C a m p o C h a n o c 64 62 49 - - - - - - San Quin t~n T o m b o l o 80 66 62 89 - - - -

Ba h i a Falsa 83 74 68 83 86 - - N o r t h M a r s h 82 79 65 81 86 87

B. Reproductive groups Estero de PunW. Banda San Quintin

Missiora Bay L~ Boc~ Campo Qh~noc Tombolo B~hia F~lsa North Marsh

Mission Bay 89 p -< 0.001 p --< 0.001 - - - - - - Es te ro de ~ m t a B a n d a La Boca 29 95 - - p = 0 .002 p = 0.002 p = 0.002

C a m p o C h a n o c 53 75 74 - - p 0 .002 - - San Quin t~n T o m b o l o 87 40 62 90 - - - -

Ba h i a Falsa 91 26 50 86 93 - - N o r t h M a r s h 90 31 55 88 90 88

ilarity) than between Estero de Punta Banda and the o ther estuaries (11-16%) (Table 9b). Causes of he terogenei ty between the two sites within Es- tero de Punta Banda included h igher densities and less variability of Mediomastus arnbiseta and nereid polychaetes at the site closest to the mouth , La Boca. Homogene i ty of macro fauna within San Quintfn (96-31% similarity) was similar to that found between San Quintfn and Mission Bay (99- 35% similarity) (Table 2b). Differences in composition among the San Quinffn sites were due in part to h igher densities of the undescr ibed syllid polychaetes, B'rania spp., in the site closest to the mou t h (Tombolo) relative to the other sites. Het- erogeneity between the head of Bahia Falsa and Nor th Marsh was caused by h igher densities of capitellid polychaetes and enchytraeid oligochaetes at Bahia Falsa and h igher densities of tubificid oligochaetes at Nor th Marsh.

The re were no significant differences in t rophic (Table 4a) and reproduct ive (Table 4b) group composit ions among the sites located within each estuary.

Comparisons Within ,Sites

Macrofaunal assemblages within Mission Bay were the most h o m o g e n e o u s (54% similarity), while assemblages at Campo Chanoc (EPB) were the most he t e rogeneous (18% similarity) (Table 2b). La Boca (EPB) and the San Quintfn sites had similarly h o m o g e n e o u s macrofaunal assemblages (35-42% similarity) (Table 2b). Abundances of tanaids, tubificid oligochaetes, and capitellid polychaetes contr ibuted the most to the similarity of

macrofaunal assemblages within Mission Bay. Ne- mer teans and the capitellid Mediomastus ambiseta were the most spatially h o m o g e n e o u s taxa at Cam- po Chanoc (EPB) and at La Boca, where nereid polychaetes also contr ibuted to within-site similar- it'/. Tubificid oligochaetes and the undescr ibed polychaetes, Brania spp. explained most of the macrofaunal homogene i ty at both the site closest (Tombolo) and farthest (North) f rom the m o u th at San Quintfn. Nemer teans were also impor tan t at Nor th Marsh. Homogene i ty at Bahia Falsa (BSQ) was due to uni form abundances of capitellid polychaetes, enchytraeid oligochaetes, and chi- ronomid insects.

Similarity of trophic group composit ions within sites ranged from 77-89%, except for Campo Chanoc (EPB) which showed only 49% similarity. The high propor t ions of surface and subsurface deposit feeders t h roughou t each of these sites were responsible for the high similarity measures. Simi- larities in reproduct ive group composit ions ranged from 74-95% within each site and were attribut- able to the high propor t ions of direct developers found within all sites in Mission Bay and Bahia de San Quintfn, and high propor t ions of animals with a planktonic stage found within each of the sites in Estero de Punta Banda.

E N V I R O N M E N T A L R E L A T I O N S H I P S W I T H

M A G R O F A U N A

The multiple regression analyses detected some weak, but still significant (p < 0.05), correlat ions between the macrofaunal and environmenta l variables (see Tables 5 and 6). Total macrofaunal den-

Tidal Flat Macrofaunal Communities 1 0 9

TABLE 5. Results of linear stepwise multiple regressions of macrofaunal tmxa richness and abundances, and environmental properties from the tidal flats of Mission Bay, southern Califurnia; Estero de Ptmta Banda and San Quinffn, Baja California. Data were collected between April and August 1996. n = 13 cores (18 crn~ • 6 cm-deep). Environmental variables include organic matter content, sand content, belowground biomass, and percent cover of Zostera marina. + / positive (+) or negative ( ) correlation.

DependentVariable IndependentVariable +/ R ~ or r v p F df

Taxa richness % Zostera cover + 0.28 0.002 7.4 2, 38 Organic matter content

Ofigochaeta Enchytraeidae Sand content 0.34 0.0004 9.6 2,88

% Zostera cover Naididae Sand content 0.27 0.002 7.2 2,88

Organic matter content Insecta Sand content 0.26 0.004 6.6 2,58

% Zostera cover Polychaeta

Mediomastus am biseta Sand content + 0.11 0.04 4.8 1,39 Nereidae Sand content + 0.22 0.002 10.7 1,89 Opheliidae Organic matter content - 0.18 0.02 4.1 2,38

% Z~tera cover + Syllidae Belowground biomass + 0.31 0.001 8.4 2, 38

Organic matter content

Peracarid ciqastacea Gammaridea Belowground biomass + 0.24 0.005 6.1 2,38

(non-Corophiids) Organic matter content Isopods % Zostera cover + 0.57 1 • 10 7 24.9 2,38

Organic matter content Mollusca Organic matter content - 0.20 0.004 9.5 1,39

Gastropoda Organic matter content 0.16 0.01 7.5 1,89

sity a p p e a r e d u n a f f e c t e d by the e n v i r o n m e n t a l var- i ab les m e a s u r e d , whi le t axa r i c h n e s s t e n d e d to be pos i t ive ly r e l a t e d to Zostera cover a n d nega t ive ly re- l a t ed to p e r c e n t o r g a n i c m a t t e r (Table 5). Dens i - ties o f e n c h y t r a e i d o l i g o c h a e t e s a n d insec ts were nega t ive ly c o r r e l a t e d with sand c o n t e n t . Dens i t i e s of the cap i t e l l i d Mediornastus ambiseta a n d o f n e r e i d p o l y c h a e t e s we re pos i t ive ly c o r r e l a t e d with s and c o n t e n t , whi le o p h e l i i d a n d syllid p o l y c h a e t e s were nega t ive ly c o r r e l a t e d wi th o r g a n i c m a t t e r a n d pos- i t ively a s soc i a t ed wi th t he p r e s e n c e of Zostera (per - c e n t cover a n d p l a n t b e l o w g r o u n d b i o m a s s ) . D e n - s i t ies o f i s o p o d s a n d g a m m a r i d e a n a m p h i p o d s ( n o t i n c l u d i n g c o r o p h i i d s ) were pos i t ive ly co r re - l a t ed with p r e s e n c e of Zostera, ( p e r c e n t cover a n d / or b e l o w g r o u n d b iomass ) a n d nega t ive ly a s soc i a t ed with o r g a n i c m a t t e r c o n t e n t .

W h e n d i s t ance f i o m the m o u t h of t he e s t u a r y was a d d e d to the m u l t i p l e r e g r e s s i o n m o d e l s us ing only d a t a f r o m San Q u i n t l n , dens i ty o f to ta l mac - r o f a u n a r e m a i n e d u n c o r r e l a t e d wi th any o f the en- v i r o n m e n t a l va r i ab l e s a n d n u m b e r of t axa was still nega t ive ly c o r r e l a t e d with o r g a n i c m a t t e r c o n t e n t (Table 6). T u b i f i c i d o l i g o c h a e t e dens i ty was posi - tively c o r r e l a t e d , whi l e dens i ty of n a i d i d o l igo- c h a e t e s was nega t ive ly c o r r e l a t e d with d i s t ance f r o m the m o u t h o f the estuary. Cap i t e l l i d , s p i o n i d , a n d syllid p o l y c h a e t e dens i t i e s all s h o w e d n e g a t i v e c o r r e l a t i o n s wi th the d i s t a n c e f r o m the m o u t h .

Discuss ion

S o u t h e r n C a l i f o r n i a coas ta l systems lack p r i s t i n e r e f e r e n c e si tes m a k i n g it d i f f icu l t to d e f i n e a n t h r o - p o g e n i c impac t s , Coas ta l eco log i s t s a re t h e r e f o r e c h a l l e n g e d to eva lua te the c u m u l a t i v e i m p a c t s on n a t u r a l systems, o f t en wi th on ly s h o r t - t i m e ser ies c o m p a r i s o n s wi th in a n d b e t w e e n areas , or wi th c o m p a r i s o n s of a r eas s u b j e c t e d to d i f f e r e n t types a n d levels o f d i s t u r b a n c e (see T e g n e r a n d D a y t o n 1997; D a y t o n et al, 1998). S e l e c t i n g the less de- g r a d e d e s tua r i e s of n o r t h e r n Baja C a l i f o r n i a as ref- e r e n c e sites for the d e g r a d e d w e t l a n d s o f s o u t h e r n C a l i f o r n i a s e e m s to be a n a t u r a l cho ice , y e t de- p e n d i n g u p o n w h i c h si te was c h o s e n in this study, we w o u l d have d r a w n v e r y d i f f e r e n t conc lus ions . I f Mis s ion Bay h a d b e e n c o m p a r e d only to Es te ro de P u n t a B a n d a , we m i g h t have h y p o t h e s i z e d tha t h i g h e r o r g a n i c e n r i c h m e n t on the Mis s ion Bay t idal f la t m a y have c o n t r i b u t e d to h i g h e r p r o p o r t i o n s of tub i f i c id o l i g o c h a e t e s , wh ich a r e k n o w n to be a s soc i a t e d wi th h i g h o r g a n i c s e d i m e n t c o n t e n t (Diaz 1980). T h e h i g h e r p r o p o r t i o n of a n i m a l s with d i r ec t d e v e l o p m e n t m a y have b e e n h y p o t h e - s ized as a r e su l t o f the i s o l a t i o n o f t he Mis s ion Bay t idal f la t (e.g. , r e s u l t i n g in r e s t r i c t e d la rva l r e c r u i t - m e n t fi-om o t h e r m a r s h e s ) re la t ive to t he f lats in Es te ro de P u n t a Banda . T h e s imi la r i ty b e t w e e n the d e g r a d e d Mis s ion Bay a n d the re la t ive ly p r i s t i n e B a h i a de San Q u i n t f n d e m o n s t r a t e s tha t t h e r e is a

110 T.S. Talley et al.

TABLE 6. Results of forward stepw-ise mul t ip le regress ions of macrofauna l tmxa r ichness and abundances , and env i ronmen ta l properties f rom the t idal flats of San Quint[n , Baja California. Data were col lec ted between Apri l 28 and June 22, 1996, n 15 cores (18 crn~ • 6 cm-deep). Env i ronmen ta l variables inc lude organic ma t t e r content , sand content , be l owground biomass, and p e r c e n t cover of Zostera ~r~arina and distance fi-om the m o u t h of each estuary. Distance was h ighly cor re la ted with the sec!knent p roper t i e s so the residuals of distance (the effects of sand removed) were used. + / - = positive (+) or negative ( - ) correlat ion.

D epera de rat Variable Irade peradera t Variable + / - R 2 or r 2 p F df

Taxa r ichness Organic ma t t e r con ten t 0.84 8.8 1,17 Ol igochae ta

TuMficidae Distance fi-om m o u t h + 0.25 0.028 5.8 1,17 Naididae Distance f rom m o u t h - 0.23 0.039 5 1,17

Insecta % Zos~era cover 0.56 0.001 10.4 2,16 Sand c o n t e n t

Polychaeta Capi te l l idae Distance f rom m o u t h - 0.47 0.001 15.0 1,17 Spionidae Distance t -ore m o u t h 0.36 0.006 9.6 1,17 Syllidae % Zostera cover + 0.86 7 • 10 ~ 21.9 4,14

Organic ma t t e r con ten t + Sand c o n t e n t + Distance f rom m o u t h

Decapod crustacea Sand c o n t e n t + 0.23 0.036 5.2 1,17 Peracar id crustacea Isopods % Zostera cover + 0.55 0.002 9.6 2,16

Organic ma t t e r con ten t Mollusca

Gas t ropoda Organic ma t t e r con ten t 0.56 0.0002 21.7 1,17

lack of close coupl ing between the ben thos and the assumed an th rop ogen i c impact. This signifies that these systems are m o r e complex than we first thought , and that they r e spond to a variety of factors, acting on different t empora l and spatial scales, that contr ibute to the distr ibution of macrofaunal assemblages.

SCALES OF COMMUNITY STRUCTURE

IN SPACE AND TIME

Spatial Scales In addi t ion to large-scale (101-102 km), among-

estuary variat ions in macrofauna l c o m m u n i t y structure and env i ronmenta l variables, mid-scale (101- 10 z m) spatial var iat ions (within-estuary) also exist. Spatial variat ion of the env i ronmenta l and some of the macrofauna l p roper t i es observed in this study was h igher within than a m o n g estuaries. On a small spatial scale (1-10 m) , variat ion may be observed due to microhab i ta t differences (e.g., vary- ing abundances of h igher plants). Sampl ing at each of these spatial scales would be ideal to prop- erly describe the tidal flat habitat , and was a t tempt- ed here at the cost of the n u m b e r of replicates (cores) within each site. Low n u m b e r s of replicates can cause loss of resolut ion of trends, thus mak ing it m o r e difficult to demons t ra te significant differences between sites (Thrush et al. 1994; Hewit t et al. 1998). Despite our low n u m b e r of replicates, we detected significant re lat ionships be tween sites and b e t w e e n m e a s u r e d var iab les . A l t h o u g h h i g h e r n u m b e r s of replicates should be used to p roper ly de t e rmine amoun t s of spatial variability (see Hew-

itt et al, 1993), the data p resen ted he re give an idea of the genera l pa t te rns of macrofauna l and associated env i ronmenta l p roper t i e s within and a m o n g these estuaries.

Temporal Scales

Seasonal changes in c o m m u n i t y s t ructures are an i m p o r t a n t considera t ion when making comparisons between dates or systems. Densities of tem- perate , intertidal, soft-bottom invertebrates are well d o c u m e n t e d to peak in the spring, decline t h r o u g h o u t the summer , and often exper ience a second, usually smaller, peak in the fall before de- clining again into the winter (e.g., Levin 1984; Frid and J ames 1989; Marsh and Teno re 1990; True- b lood et al. 1994; Sarda et al. 1995). The Mexican sites in this study were sampled dur ing the spring and early s u m m e r (April 26-July 6, 1996) when densities and species richness of benthic invertebrates are at their peak (Calderon-Aguilera 1992). Mission Bay was sampled in late s u m m e r (August 10, 1996) when the peaks had p resumably de- clined, yet bo th density and taxa richness in Mis- sion Bay were found to be a m o n g the highest relative to the o ther sites.

Macrofaunal data based on samples collected in April and July 1996 f rom the same mudf la t with a similar sized core (0.001 m ~ X 2 cm deep) are presented in Crooks (1998), who found that species richness did not change dramatically between April and July 1996 (e. 13-15 species). Estimates of macrofauna l density were abou t 65% lower in the s u m m e r than in the spring (Crooks 1998) sug-

gesting that our density est imates may be low for Mission Bay. Based on the macro fauna l density shifts p resen ted in Crooks (1998), the relative a b u n d a n c e of polychaetes est imated in this study (22%) may be abou t half as m u c h as it would have been in the spring, while ol igochaetes (27%) may have been m o r e a b u n d a n t by a factor of two. Per- acarid crustaceans, the dom i nan t taxon in Mission Bay in this study did not seem to show a seasonal p a t t e r n b e t w e e n sp r i ng and s u m m e r ( C r o o k s 1998). Using these est imates of f luctuat ions in propor t ional abundances , the p ropor t ions of polychaetes in Mission Bay that are r epo r t ed he re would increase to within the range of those re- por t ed in San Quinffn, and p ropor t ions of oligochaetes would r ema in in te rmedia te and similar to the values found in two of the San Quint fn sites. In Mission Bay, the same infaunal species or taxa have been found on the mudf la t across seasons, but the abundances of each change (e.g., Levin 1984; Crooks 1998; Levin et al. 1998). The variability be tween the estuaries, and even be tween sites within the estuaries, was grea ter than the variability be tween late spring and s u m m e r on the Mission Bay mudflat .

RELATIONSHIPS BETWEEN MACROFAUNA AND THEIR ]:(NVIRONMENT

Distribution Gradients

T h e estuaries examined in this study are characteristic of arid Med i t e r r anean climates and are considered seasonally inverse estuaries (Largier et al. 1997). High evapora t ion and a lack of freshwater inputs dur ing the dry season (Levin 1983; Largier et al. 1997) result in inverse salinity and t empe ra tu r e gradients within the estuaries. Such condit ions often occur year . round in the Mexican estuaries (Chavez de Nishikawa and Alvarez-Bor- rego 1974; Alvarez-Borrego et al. 1975). Despite the d o c u m e n t e d p resence of this inverse gradient in the bay water, the pore-water salinities in these areas were all found to be abou t that of seawater (35-38%o). In wetter climates, macro fauna l distri- bu t ion gradients in estuaries are believed to be due in par t to decreasing salinity f rom the m o u t h to the head of the estuary (see Levinton 1982; Mc- Lusky et al. 1993; Ysebaert et al. 1993). Oligo- chaetes (especially the family Tubificidae) and insects are often the do m i nan t taxa in the low-salinity, u p p e r reaches, while polychaetes and molluscs have been associated with the lower reaches of estuaries (McLusky et al. 1993; Ysebaert et al. 1993). Despite the lack of a salinity gradient in Bahia de San Quintfn , we found similar pat terns , with tubificid ol igochaetes positively correlated, and three dominan t polychaete families negatively correlat-

Tidal Flat Macrofaunal Communities 11 1

ed, with distance f rom the m o u t h ( i n d e p e n d e n t of sed iment proper t ies) . Possible explanat ions for the similar macro fauna l distr ibution pa t t e rns found in San Quint fn include decreasing gradients of tidal ampl i tude (Moreira et al. 199g) and changing hy- drodynamics (e.g., r educed wave energy and flush- ing) f rom m o u t h to head of the estuary. Condi- tions specific to Bahia de San Quint fn may also play a role in the macro fauna l distributions. These include seasonal r u n o f f f rom agricultural fields into the bay and a b reakdown of the typical inverse-estuary currents by overr iding uni-direct ional winds (Farreras and Cabre ra 1979). These physical factors could, in turn, affect the amoun t s of adul t and larval dispersal and rec ru i tmen t , and environmen ta l condi t ions (e.g., sed iment organic mat te r and particle size) t h r o u g h o u t the estuary. High wind or wave energy has been observed to influ- ence benth ic macrofauna l c o m m u n i t y s t ructures within estuaries t h rough sed imen t dis turbance and post-larval dispersal (Commi to et al. 1995; T u r n e r et al. 1995; Schaffner 1999).

,Sediment and Vegetation Effects

While m o u t h to back bay energy gradients may indirectly affect macro fauna l distr ibutions t h rough the s t ructur ing of sed iment proper t ies , the rela- t ionship between m a c r o f a u n a and sed imen t properties, i n d e p e n d e n t of distance f rom the mouth , was examined , as was the re la t ionship with Zostera cover. Sed iment p roper t i es including particle size and organic ma t t e r (Sanders 1958; Pearson and Rosenberg 1978; Whit latch 1980; McLusky et al. 1993; Snelgrove and Bu tman 1994), and the pres- ence and absence of seagrass (Or th 1977; Stoner 1980a, b; Edgar et al. 1994) are known to inf luence density, species richness, and compos i t ion of macrofaunal assemblages. The sed iment p roper t i es measu red in this study appea r to be i m p o r t a n t to m a c r o f a u n a as they were related to the densities of m e m b e r s of all the major t axonomic groups. T h e p resence of Zostera was corre la ted with a few taxa of macrofauna , but only in combina t ion with sed- imen t p roper t ies (see Table 5). The inf luence of Zostera on sed imen ta ry and macrofauna l p roper t i e s in this study appears to be less c o m p a r e d to other areas (e.g., effects on sediment: Ginsburg and Low- ens tam 1958; Scoffin 1970; effects on macrofauna : Or th 1977, 1984; Reise 1978; Lewis and Stoner 1983; S u m m e r s o n and Peterson 1984). The cover and height of Zostera was relatively low in our study areas, so we did no t expect s t rong Zostera effects.

ITEASIBILITY OF COMPARISONS

Since a lack of pristine re ference sites in southern Cal i fornia has left us with the need to evaluate ecological impacts by compar ing the same system

1 1 2 T.S. Talley et al.

t h r o u g h t ime , or by m a k i n g c o m p a r i s o n s b e t w e e n systems of d i f f e r e n t d i s t u r b a n c e levels a n d types, it is i m p o r t a n t to f ind feas ib le ways in w h i c h to m a k e these c o m p a r i s o n s . T h e r e was a g r e a t e r s imi la r i ty of m a c r o f a u n a l a s s e m b l a g e s b e t w e e n San Q u i n f f n a n d Mis s ion Bay t h a n b e t w e e n these e s tua r i e s a n d Es te ro de P u n t a B a n d a , b u t m a n y lower t a x o n o m - ic-level m a c r o f a u n a l d i f f e r e n c e s still exist. G r o u p - ing t axa in to h i g h e r t a x o n o m i c or f u n c t i o n a l g r o u p s (e.g., t r o p h i c a n d r e p r o d u c t i v e ) m a y re- duce var iab i l i ty (Warwick 1988) a n d revea l g e n e r a l p a t t e r n s b e t w e e n systems. T h e r a n g e of s imi la r i ty b e t w e e n B a h i a de San Q u i n f f n a n d Mis s ion Bay us ing taxa a b u n d a n c e d a t a was 9 9 - 3 5 % (see T a b l e 6b) , wh i l e s imi la r i ty us ing r e p r o d u c t i v e g r o u p s ( 8 7 - 9 1 % ) or t r o p h i c g r o u p s ( 8 0 - 8 3 % ) (see T a b l e 4a a n d b) was m u c h h ighe r . Al l t h r e e es tua r ies var- i ed l i t t le f rom each o t h e r wi th r e s p e c t to t r o p h i c g r o u p c o m p o s i t i o n . However , B a h i a de San Q u i n - ffn a n d Mis s ion Bay were s imi la r to each o ther , a n d b o t h were d i f f e r e n t f r o m Es te ro de P u n t a B a n d a with r e s p e c t to r e p r o d u c t i v e g r o u p s (d i r ec t devel - o p e r s or t hose spec i e s wi th p l a n k t o n i c la rvae) a n d p r o p o r t i o n of m a c r o f a u n a tha t have a m o b i l e a d u l t stage. E x a m p l e s o f m o b i l e adu l t s i n c l u d e d i p t e r a n insec ts ( W i r t h a n d S t o n e 1963), the o l i g o c h a e t e P a r a n a i s litoralis, w h i c h lives at the s e d i m e n t surface a n d m a y swim ( L e v i n t o n et al. 1995) or be easily c a r r i e d by b e d l o a d t r a n s p o r t , a n d p e r a c a r i d c r u s t a ceans , m a n y of wh ich a r e c a p a b l e of swim- ru ing ( M o r r i s et al. 1980) or r a f t i ng on p l a n t mater ia l ( H i g h s m i t h 1985; H o l m q u i s t 1994). Th i s h i g h e r level g r o u p i n g also a ids in s o r t i n g o u t the g e n e r a l cause of o b s e r v e d d i f f e rences . Fo r exam- p le , t he s imi la r i ty in t r o p h i c g r o u p s b e t w e e n Mis- s ion Bay a n d B a h i a de San Q u i n t f n may i m p l y t ha t the systems have s imi l a r b e n t h i c food web s t ructures or f ood (e.g. , o r g a n i c m a t t e r ) sources . Dif- f e r e n c e s in r e p r o d u c t i v e g r o u p s b e t w e e n Es te ro de P u n t a g a n d a a n d the o t h e r si tes may i n d i c a t e dif- f e r e n c e s in c o n d i t i o n s tha t i n f l u e n c e d i spe r sa l or r e c r u i t m e n t such as w a t e r c o l u m n or h y d r o l o g i c c o n d i t i o n s (e.g., c u r r e n t s , upwe l l i ng , r e t e n t i o n t ime , p l a n k t o n , etc) (e.g. , F a r r e r a s a n d C a b r e r a 1979; L a r a - L a r a e t al. 1980; A l v a r e z - g o r r e g o a n d A l v a r e z - g o r r e g o 1982).

I t is l ikely tha t l a rge-sca le o c e a n o g r a p h i c p ro - cesses a r e r e s p o n s i b l e for the r e c r u i t m e n t o f ani- ma l s in to e a c h bay, whi l e phys ica l d i s t u r b a n c e a n d m i c r o h a b i t a t e n v i r o n m e n t a l g r a d i e n t s w i th in these e s tua r i e s a r e i m p o r t a n t to the s t r u c t u r e a n d dis t r i - b u t i o n o f m a c r o f a u n a l a s s e m b l a g e s at s m a l l e r scales in space a n d t ime. L o c a l s t r u c t u r e s such as the p r e s e n c e o r a b s e n c e o f p l a n t s h o o t s o r r o o t s m a y c o n t r o l a b u n d a n c e s o f s o m e t axa on even s m ~ i e r s c~es , T h e d e c o u p l i n g o f the b e n t h o s f r o m the a p p a r e n t i n d i c a t o r s o f e n v i r o n m e n t a l d e g r a -

d a t i o n cou ld r e su l t f r o m these p a r t i c u l a r i n d i c a t o r s a c t i ng on d i f f e r e n t scales than , o r n o t s t rong ly af- fec t ing , t he m a c r o f a u n a o r the i r a s soc i a t ed envi- r o n m e n t a l p r o p e r t i e s (e.g. , s e d i m e n t p r o p e r t i e s or wi th in -bay e n e r g y g r a d i e n t s ) . T h e effects of envi- r o n m e n t a l d i s t u r b a n c e s , i n c l u d i n g u r b a n a n d ag- r i c u l t u r a l d e v e l o p m e n t , on m a c r o f a u n a l assem- b l ages s h o u l d n o t be g e n e r a l i z e d , as they m i g h t be s i t e - d e p e n d e n t o r s c a l e - d e p e n d e n t . T h e s e l ec t i on of b o t h a r e f e r e n c e site a n d the va r i ab l e s to be s a m p l e d s h o u l d be b a s e d on the s u s p e c t e d dis tur- b a n c e wi th ca re fu l c o n s i d e r a t i o n to scale. O n e pos- s ible a l t e rna t i ve a p p r o a c h for d e a l i n g with the sit- u a t i o n e n c o u n t e r e d in this study, w h e r e t he m a c r o - i n f a u n a l a s s e m b l a g e s in the d i s t u r b e d a n d refer - ence site were fa i r ly s imilar , w o u l d be to e x a m i n e an i n d i c a t o r spec ies tha t r e s p o n d s to the speci f ic h y p o t h e s i z e d stress,

ACKNOWLEDGMENTS

We would like to thank D. M. Talley for iris help with the trips to the study sites and his unconditional dedication while there, we would also like to thank K. Bailey, D. Fruetel, A. A. Larson, R Moberg, A. RoNes-Bustamante, K. Riser, E. B. Scripps-D, M. Sigala, and L. I. Vilchis for their help in the field and the laboratory, E. Montiel for help with library research, J. Griffin for her graphics expertise, M. Graham, J. Hewitt, and L. Levin for data analysis advice,J. Hewitt for her data analysis assistance and in, perturbable nature, J. Crooks and L. Levin for reviewing an earlier version of the manuscript, and L. Levin for intellectual input. Also appreciated was taxonomic assistance was provided by J. Crooks, K. Coates, L. Harris, B. Healy, K. Fitzhugh, C. Martin, M. Milligan, 12 Phillips, and E. Vetter. We additionally would like m thankJ. Hughes and two anonymous reviewers for critically reviewing the manuscript. This work was funded by a Pew Conservation Fellowship awarded to R K. Dayton.

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Received for consideration, July 28, 1998 Accepted for publication, Aug~sr 17, 1999

tidal flat macrofaunal communities and their associated...

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