development of expectations of larval amphibian assemblage structure in southeastern depression...

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Ecological Applications, 10(4), 2000, pp. 1219–1229q 2000 by the Ecological Society of America

DEVELOPMENT OF EXPECTATIONS OF LARVAL AMPHIBIANASSEMBLAGE STRUCTURE IN SOUTHEASTERN DEPRESSION

WETLANDS

JOEL W. SNODGRASS,1,2,3 A. LAWRENCE BRYAN, JR.,2 AND JOANNA BURGER1

1Division of Life Sciences and Consortium for Risk Evaluation with Stakeholder Participation (CRESP),Environmental and Occupational Health Sciences Institute, Rutgers University, Piscataway, New Jersey 08855 USA

2Savannah River Ecology Laboratory, University of Georgia, Drawer E, Aiken, South Carolina 29802 USA

Abstract. We surveyed larval amphibians and fish in 25 relatively pristine depressionwetlands on the upper Atlantic coastal plain of South Carolina to examine relationshipsamong hydroperiod length, fish presence/absence and larval amphibian assemblage struc-ture. Our goals were to test the application of general models of lentic community structureto Southeastern depression wetlands and to develop expectations of larval amphibian as-semblage structure at reference sites. Amphibian species richness showed a unimodal patternalong a hydroperiod gradient, with wetlands that contained water for 8–10 mo/yr havingthe highest species richness. Wetlands that contained water for longer periods (i.e., driedonly during severe drought) often contained fish and had relatively low amphibian speciesrichness. Most species occurred along a restricted portion of the hydroperiod gradient, andsome species were found almost exclusively in wetlands with fish. Associations among theoccurrence of species led to relatively discrete breaks in assemblage structure along thehydroperiod gradient. Canonical correspondence analysis of catch-per-unit-effort data iden-tified four groups of wetlands with similar assemblage structure: (1) short (drying in spring),(2) medium (drying in summer), and (3) long (drying in fall or semi-annually) hydroperiodwetlands without fish; and (4) long hydroperiod wetlands with fish. Our results suggestthat general models of community structure in lentic systems are applicable to southeasternisolated wetlands and should form the basis for developing expectations of larval amphibianassemblage structure in these systems.

Key words: amphibians; biological monitoring; Carolina bays; community structure; fish; hy-droperiod; reference conditions; Savannah River Site, South Carolina; species richness; wetlands.

INTRODUCTION

Development of biological assessment and monitor-ing programs to evaluate aquatic resources has con-centrated on what has become known as the ‘‘referencecondition’’ approach (Reynoldson et al. 1997). The ref-erence condition approach involves comparing condi-tions at a site of interest (to be assessed or monitored,or both) to conditions that are ‘‘representative of agroup of minimally disturbed sites organized by se-lected physical, chemical, and biological characteris-tics.’’ The reference condition approach has been suc-cessfully applied in aquatic systems of Canada (Rey-noldson et al. 1995), Australia (Parsons and Norris1996, Marchant et al. 1997), the U. K. (Wright 1995)and the U.S. (Karr and Chin 1997) using macroinver-tebrates and fish.

The application of the reference condition approachrequires a basic understanding of community structurein the aquatic system under study so that expectationsunder minimally disturbed conditions can be devel-oped. Thus, one of the challenges of defining reference

3 Present address: Department of Biology, Towson Uni-versity, Towson, Maryland 21252 USA.

Manuscript received 28 August 1998; revised 5 July 1999;accepted 28 July 1999; final version received 19 August 1999.

conditions is incorporating variation associated withnatural environmental gradients that influence thegroup of organisms being used in biological monitoringprograms. The ability of biological monitoring pro-grams to provide early and accurate detection of humanimpacts to aquatic systems depends on variation amongreference sites (Reynoldson et al. 1997). If variationdue to natural environmental gradients among refer-ence sites is not accounted for, impacts that cause ashift that is similar to movement along the gradientwill not be detected. For example, if species richnessvaries along an environmental gradient, then an impactthat reduces species richness at a site on the high spe-cies richness end of the gradient will not be detecteduntil the impact become severe. Inclusion of ecologicalprinciples and conceptual models of community struc-ture in the development of biological monitoring pro-grams can increase the efficiency and accuracy of theseprograms (Hart 1994). Specifically, environmental gra-dients identified as strong structuring forces in con-ceptual models of community structure in aquatic sys-tems should be included in sampling plans for definingreference conditions.

The syntheses of general models of community struc-ture in lentic systems (Wiggins et al. 1980, Schneider

1220 JOEL W. SNODGRASS ET AL. Ecological ApplicationsVol. 10, No. 4

and Frost 1996, Wellborn et al. 1996) suggest that ex-pectations of amphibian community structure at lenticreference sites can be developed. Models of communitystructure in lentic systems suggest that interactionsamong the abiotic constraints of hydroperiod length,predation, and life history characteristics of individualspecies will produce predictable patterns of communitystructure along a hydroperiod gradient from temporaryponds to permanent lakes (Wiggins et al. 1980, Schnei-der and Frost 1996, Wellborn et al. 1996). Species thatpersist in temporary ponds (that dry annually) musthave the ability to survive dry periods (e.g., terrestrialadult forms, encysted eggs, or ability to move to otheraquatic habitats) and complete the aquatic phase oftheir life cycle before ponds dry. In more permanentponds and lakes (that never dry or dry only duringdroughts), larger predators can complete their life cycleand are expected to eliminate smaller species typicalof temporary ponds. Because traits that increase fitnessat one point on the hydroperiod gradient can decreasefitness on other portions of the gradient, distinct com-munities will develop along the gradient (Wellborn etal. 1996). This lentic community model is particularlyapplicable to larval amphibian assemblages (Heyer etal. 1975, Wilbur 1984).

In this paper we use existing conceptual models oflentic community structure to design and carry out asampling plan for defining reference conditions for lar-val amphibian assemblages in depression wetlands ofthe Savannah River Site on the upper Atlantic coastalplain of southeastern North America. We sampled lar-val amphibians in 22 wetlands spanning the range ofannual hydroperiod length (from permanent wetlandsto wetlands that hold water for two to three months ayear), and with and without fish populations. We se-lected hydroperiod length and fish presence/absencebecause general models of community structure in len-tic systems suggest these will be strong structuring fac-tors. Because we selected wetlands based on hydro-period length and fish presence/absence, with a prioriexpectations of patterns, our analyses represent a testof the ability of models of community structure in lenticsystems to predict patterns in southeastern depressionwetlands.

METHODS

Study site

We sampled amphibians on the 780 km2 SavannahRiver Site (SRS), located on the northern shore of theSavannah River on the upper coastal plain of SouthCarolina. The SRS is a U.S. Department of Energynuclear production site that was established in the early1950s. For security reasons, access to a large bufferarea around SRS has been controlled since 1951. Nat-ural habitats within this buffer zone have been pro-tected from human disturbances and represent some ofthe most pristine habitats in the region. There are .300

depression wetlands located within the SRS boundary(Kirkman et al. 1996), most of which have not beenimpacted by site operations. For these reasons, the SRSrepresents a unique opportunity for development of ex-pectations of amphibian assemblage structure in un-disturbed depression wetlands of the region.

Depression wetlands (some of which also are re-ferred to as temporary ponds, Carolina bays or poco-sins) are common features of the Atlantic coastal plain.Fish populations naturally occur in 10–20% of the de-pression wetlands on the upper Atlantic Coastal Plainof South Carolina (Snodgrass et al. 1996) and depres-sion wetlands are important breeding sites for manyamphibians (Gibbons and Semlitsch 1991). Waterchemistry of depression wetlands at the SRS is typicalof softwater, acidic systems (Newman and Schalles1990). Dissolved oxygen levels normally range be-tween 0% and 50% saturation, varying both temporallyand spatially (Schalles and Shure 1989); and pH rangesbetween 4.9 and 6.1 (Schalles et al. 1989). Annualhydroperiods follow a typical pattern of winter re-charge and spring to late summer drawdown or com-plete drying (Pechmann et al. 1989, Lide et al. 1995,Semlitsch et al. 1996).

To determine larval amphibian assemblage structurewe haphazardly selected a subset of 25 wetlands froma larger group of 99 wetlands for which we had a prioriknowledge of wetland hydroperiod and fish presence/absence (Snodgrass et al. 1996). The 25 wetlands wereselected to include the range of annual hydroperiodlength (from 3 to 12 months) and included six wetlandswith fish populations. Wetlands were selected such thatthey were distributed across the landscape of the SRS.The numbers used to refer to wetlands are those as-signed by Schalles et al. (1989) who also provides in-formation on wetland locations within the SRS.

Amphibian sampling

We sampled larval amphibians during three discreteperiods (winter, 18 February–28 March; spring, 21April–19 May; and summer, 23 June–11 July; all 1997)using hoop traps, minnow traps (metal), and dipnets.These sampling periods encompassed the larval periodsof all amphibians known to utilize isolated wetlandsfor breeding on the SRS (Gibbons and Semlitsch 1991).During each sampling period, we deployed 1–3 hooptraps and 3–10 minnow traps in each wetland. Thenumber of traps used in each wetland was dependenton wetland size and the number of mesohabitats (e.g.,floating vegetation, open water) present. Traps weredeployed so that all mesohabitats were sampled. Trapswere checked every 24 hr for one 72-hr period duringeach discrete sampling period.

During each sampling period, we also conducted ac-tive sampling using dipnets. Two individuals searchedall mesohabitats and dipnetted all amphibians sighted.Blind sweeps with dipnets also were made in all me-sohabitats. Duration of active sampling varied from 20

August 2000 1221AMPHIBIANS AND BIOLOGICAL MONITORING

to 90 minutes depending on wetland size at the timeof sampling and the number of mesohabitats present.

Most salamanders and adult amphibians, and all fish,were identified in the field and returned to the wetland.All tadpoles were preserved in 10% formalin and re-turned to the laboratory for identification. Tadpoleswere identified according to Altig (1970) and Travis(1981). We collected voucher specimens of all am-phibian species encountered.

Analyses

For all analyses we used only larval forms with thefollowing exceptions. Three totally aquatic salaman-ders (Amphiuma means, Siren lacertina, and S. inter-media) were encountered in our study area. When theseaquatic salamanders were present we captured them atlow frequencies. We included both adult and larvalaquatic salamanders in analyses and assumed the pres-ence of either indicated successful reproduction. Am-bystoma talpoideum has both terrestrial and paedo-morph adult forms (Semlitsch 1985). We included pae-domorphs and larval A. talpoideum in our analyses.Finally, Notophthalmus viridescens has aquatic larvaland adult forms that are sometimes separated by animmature terrestrial eft (Healy 1974). We included bothaquatic forms of N. viridescens in our analyses andassumed the presence of either indicated successful re-production.

As a relative measure of wetland hydroperiod, wecalculated a wetland drying score as the number oftimes a wetland was visited and it held water (Snod-grass et al. 1996). Wetlands were visited five times,approximately evenly distributed, during 1990 andagain five times between September 1996 and August1997 (the annual hydrodrological cycle encompassingour sampling period). Our drying scores ranged from1 (i.e., water present 10% of the time) for wetlandswith relatively short hydroperiods to 10 for wetlandswith long hydroperiods.

We tested three predictions of current lentic com-munity models: (1) species richness will exhibit a un-imodal pattern along a gradient of increasing hydro-period length; (2) decreased species richness in longerhydroperiod wetlands is correlated with the presenceof large predators (i.e., fish); and (3) distinct breaks inassemblage structure will occur along the hydroperiodgradient.

We tested hypothesis (1) using a quadratic equationof the form

2y 5 a 1 b x 2 b x1 2

where y is species richness and x is drying score. Sig-nificance of both b1 and b2 indicates a significant un-imodal pattern of species richness along the hydroper-iod gradient. We also tested the null hypothesis thatthe quadratic model did not provide a better fit than asimple linear model using an F test (Zar 1984).

We tested hypothesis (2) using a linear regressionapproach to ANCOVA. The model used was

y 5 a 1 b x 1 b x 1 b x x1 1 2 2 3 1 2

where y is species richness, x1 is drying score, and x2

is presence of fish coded as a dummy variable. In thismodel, a and b1 are the intercept and slope, respec-tively, of the line relating species richness to dryingscores among wetlands without fish, and b2 and b3 arethe intercept and slope, respectively, of the line relatingspecies richness to drying scores among wetlands withfish. For both the quadratic and the ANCOVA models,dependent variables were log transformed to moreclosely approximate the assumptions of the models.

To test hypothesis (3) we used canonical correspon-dence analysis (CCA; ter Braak 1988) and a test forclustered distribution of wetland larval amphibian as-semblages in ordination space (Matthews 1998). CCAis a direct gradient analysis ordination technique thatincorporates a linear regression step, relating assem-blage structure directly to environmental variables, inthe reciprocal averaging algorithm (ter Braak 1986).Inclusion of the linear regression steps constrains theordination axis so as to summarize variation related toenvironmental variables. We included drying scoresand fish presence/absence (coded as a nominal variable)to investigate the distribution of amphibian larvaealong the hydroperiod and fish presence/absence gra-dients. We used catch-per-unit-effort (number of am-phibians·trap21·24 hr trap period21 1 number of am-phibians/hr of active sampling) as dependent variablesin the CCA. To test for significant variation in assem-blage structure along environmental gradients we usedstepwise addition of environmental variables to theCCA model. The significance of individual environ-mental variables was tested using the Monte Carlo per-mutation test (999 permutations) of the CANOCO com-puter program (ter Braak 1988). We tested the nullhypothesis that the distribution of sample scores in themultivariate space created by the first two axes of theCCA was random (i.e., did not vary significantly froma Poisson distribution) using a x2 test of goodness offit following the methods of Matthews (1998).

RESULTS

Species richness and abundance

We collected 12 464 larval (Appendix A) and 326adult amphibians, representing 25 species during thestudy. Of these 25 species, we collected only larvaeforms of seven (Eurycea quadridigitata, Gastrophrynecarolinensis, Hyla chrysoscelis, Hyla femoralis, Pseu-dacris triseriata, Rana grylio, Scaphiopus holbrooki)and only adults forms of one (Pseudotriton montanus).We also collected 1131 fish representing 12 speciesfrom six wetlands (Appendix B). Five amphibian spe-cies were collected in only one or two wetlands (Ap-pendix A), and therefore we did not include these spe-


FIG. 1. Fits of quadratic regression equations (A, B) and ANCOVA (C, D) to relationships among wetland hydroperiodlength and larval amphibian species richness and total larvae collected. In all plots, open and solid circles represent wetlandswithout and with fish, respectively.

TABLE 1. Results of regression analyses relating larval amphibian species richness and totalnumber of larvae collected to drying score, an index of hydroperiod length, in 25 isolatedwetlands in South Carolina.

Dependentvariable(model)

Independentvariable

Parameterestimate

SE ofestimate P r2

Log (richness 1 1)Linear Constant

Drying score†0.2050.090

0.1140.016

0.085,0.001

0.57

Polynomial ConstantDrying score†Drying score‡

20.2270.299

20.019

0.1450.0570.005

0.132,0.001

0.001

0.74

Log (no. larva collected 1 1)Linear Constant

Drying score†0.6490.062

0.4320.062

0.1470.004

0.31

Polynomial ConstantDrying score†Drying score‡

20.9580.978

20.069

0.5590.2180.019

0.101,0.001

0.001

0.57

Note: Results of simple linear regression and second-order polynomial regression are givenfor comparison.

† Drying score for 1990 and 1997.‡ Drying score for 1997 only.

cies in the assemblage structure analyses. Three wet-lands dried early in 1997. While we collected adults atthese wetlands during the first sample period, we col-lected no larvae from these wetlands during subsequentsampling periods because they were dry. Because thesewetlands were dry within two weeks of our first sam-pling period, we assumed no successful amphibian re-production took place in these wetlands, and their lar-

vae species richness was 0 for 1997. We did not includewetlands with 0 species richness in the assemblagestructure analyses.

Larval amphibian species richness and total numberof larvae collected per wetland showed unimodal pat-terns along the hydroperiod gradient with peaks in wet-lands with drying scores of 6–8 (Fig. 1). Quadraticmodels provided significant fits to these patterns and


TABLE 2. Results of ANCOVA of the effects of drying score and fish presence/absence on larval amphibian species richnessand total number of larvae collected from 25 isolated wetlands in South Carolina.

Dependentvariable

Independentvariable

Parameterestimate

SE ofestimate P r2

Log(richness 1 1) constantdrying scorefish presence/absenceinteraction

0.0920.1181.567

20.200

0.1070.0180.8460.093

0.401,0.001

0.0780.043

0.70

Log(no. larva collected 1 1) constantdrying scorefish presence/absenceinteraction

0.1390.3286.565

20.850

0.3720.0612.9420.323

0.712,0.001

0.0370.016

0.60

Note: A regression approach to ANCOVA, with fish presence/absence coded as a dummy variable, was used.

FIG. 2. Biplot of CCA (canonical correspondence anal-ysis) results for wetlands. Points are site scores. Arrows rep-resent environmental variable scores (arrowhead position)and direction of environmental gradients. Each separate sym-bol represents a cluster of wetlands with similar larval am-phibian assemblage structure.

account for 17% and 26% more of the variation inspecies richness and total number of larvae collected,respectively, than did simple linear models (Table 1).In both cases the overall F test indicated a significantly(P , 0.05) better fit of the polynomial models than thesimple regression models. ANCOVA models also pro-duced significant fits to the data (Table 2). Proportionsof variation accounted for by the quadratic and AN-COVA models were similar (Tables 1 and 2), sug-gesting fish predation is the mechanism behind de-creases in species richness and total number of larvaecollected in longer hydroperiod wetlands. Species rich-ness and total number of larvae collected were posi-tively correlated with hydroperiod length among wet-lands without fish, but these relationships were nega-tive among wetlands with fish (Fig. 1). The significanceof all terms in the models, and positive signs of theparameters associated with the main effects of hydro-period (slopes of the lines relating richness and abun-dance to hydroperiod among wetlands without fish) and

negative signs of the parameters associated with theinteraction terms (slopes of the lines relating richnessand abundance to hydroperiod among wetlands withfish) indicate these patterns are significant.

Assemblage structure

Larval amphibian assemblage structure was relatedto hydroperiod and fish presence/absence. The stepwiseapproach to CCA indicated that both drying scores andfish presence/absence were significantly (P 5 0.001 forboth) related to larval amphibian assemblage structure.The first two axes of the CCA accounted for 30% ofthe variation in the species data and were related tofish presence/absence and hydroperiod, respectively.Fish presence/absence accounted for 72% of the cor-relation between the environmental variables and as-semblage structure while drying score accounted forthe remaining 28%.

There were distinct breaks in assemblage structurealong the hydroperiod and fish presence/absence gra-dients. The distribution of site scores in ordinationspace defined by the first two axes of CCA differedsignificantly (x2 5 7.83, P 5 0.050) from random. Abiplot of environmental variables and CCA site scoreson the first two ordination axes (Fig. 2) indicated threediscrete groups of wetlands without fish along the hy-droperiod gradient: (1) short hydroperiod wetlandswith drying scores of 2–6, (2) medium hydroperiodwetlands with drying scores of 6–8, and (3) long hy-droperiod wetlands with drying scores of 8–10. On thissame plot, long hydroperiod wetlands with and withoutfish were separated along the fish presence/absence gra-dient. Wetland ordination scores clustered along thehydroperiod gradient despite overlap in their dryingscores. When drying scores for 1997 alone (AppendixA) are considered, CCA results are similar (data notshown) and all groups show complete separation inrelationship to drying scores; 1997 drying scores forshort, medium, and long hydroperiod wetlands withoutfish were 1–2, 3–4, and 5, respectively.

Species preferences (defined here as their areas ofhighest abundance) on the hydroperiod and fish pres-ence/absence gradients also showed clustered distri-


FIG. 3. Biplot of CCA (canonical correspondence anal-ysis) results for species. Points are species scores which canbe interpreted as preferences based on abundance. Speciesare abbreviated using the first three letters of their genera andspecies names. Arrows represent environmental variablescores (arrowhead position) and direction of environmentalgradients.

bution in ordination space (Fig. 3); and, many speciesshowed strong preferences for particular hydroperiodsor the presence or absence of fish. For example, mar-bled salamanders (Ambystoma opacum), narrow mouthtoads (Gastrophryne carolinensis), and barking tree-frogs (Hyla gratiosa) occurred almost exclusively inshort, medium, and long hydroperiod wetlands withoutfish, respectively; and, lesser sirens (Siren intermedia)occurred exclusively in long hydroperiod wetlands withfish (Appendix A). Some species showed wider rangesof distribution along the hydroperiod and fish presence/absence gradients, but exhibited relative high occur-rence rates within a restricted range on the gradients.For example, the southern leopard frog (Rana utricu-laria) occurred in short, medium, and long hydroperiodwetlands with and without fish, but was most abundantin medium hydroperiod wetlands without fish (Appen-dix A).

DISCUSSION

General models of lentic community structure

The patterns in larval amphibian community struc-ture that we observed suggest that general models ofcommunity structure in temperate lentic systems areapplicable to depression wetlands of the southeasternUpper Coastal Plain of North America. General modelsof community structure in lentic systems predict: (1)a unimodal pattern of species richness with a peak inwetlands with intermediate hydroperiods (Heyer et al.1975, Wilbur 1984), (2) reduced species richness inlonger hydroperiod wetlands will be correlated withthe presence of large predators (Wiggins et al. 1980,Schneider and Frost 1996), and (3) trade-offs in lifehistory characteristics that maximize fitness along the

hydroperiod gradient will produce breaks along the gra-dient in community structure (Wellborn et al. 1996).We found support for all three predictions including asignificant unimodal pattern in species richness, re-duced species richness in longer hydroperiod wetlandswith fish populations, and breaks in larval amphibianassemblage structure along the hydroperiod gradient.

While the general patterns revealed by our spatialsurvey were consistent with predictions of models oflentic community structure, there were some detailsthat may need to be modified in applying the model tosoutheastern wetlands. First, the presence of fish alonewas not correlated with declines in amphibian speciesrichness, but the occurrence of fish and permanent hy-droperiod (drying score of 10) was. In both of the short-er hydroperiod wetlands with fish, periodic drying re-sulted in extirpation of fish populations. Wetlands 77and 147 dried completely in 1990 and 1996, respec-tively. Fish were extirpated from wetland 147 duringthe 1996 drying (J. W. Snodgrass, J. Burger, and A. L.Bryan, unpublished data). While the recolonization ofwetlands by fishes may be rapid (e.g., one species waspresent in wetland 147 by the end of our samplingefforts in 1997), amphibians appear to be able to takeadvantage of wetlands when fish are absent. Therefore,expectations of amphibian occurrence in southeasternwetlands should be developed recognizing the inter-action among hydroperiod length and fish presence/absence.

A second modification concerns the absence in thesoutheast of harsh winter conditions, which may influ-ence the distribution of fish among lentic habitats. Inthe lentic model proposed by Wellborn et al. (1996), abreak in community structure is expected between per-manent, fishless habitats and habitats with fish. Fishare excluded from some permanent habitats because ofanoxic conditions under winter ice cover in shallownorthern habitats (Tonn and Magnuson 1982). Exclu-sion of fish from the longest hydroperiod wetlands inour study results from wetland isolation rather thanfrom harsh environmental conditions (Snodgrass et al.1996). Thus, the ‘‘predator transition’’ described byWellborn et al. (1996) occurs among southeastern wet-lands, but it is determined by habitat landscape positionrather than geomorphology of lentic habitats.

A number of temporal and spatial surveys have re-lated amphibian assemblage structure to hydroperiodand fish presence/absence. Temporal studies havefound increasing species richness and abundance ofmetamorphosing juvenile amphibians with increasinghydroperiod length (Pechmann et al. 1989, Semlitschet al. 1996). Spatial surveys have documented a neg-ative correlation between amphibian species richnessand presence of fish populations in Ontario, Canada(Hecnar and M’Closkey 1997), Michigan and Califor-nia, United States (Collins and Wilbur 1979, Bradford1989), and Sweden (Bronmark and Edenhamn 1994).Our results, in combination with other surveys, indicate


that hydroperiod length and fish presence are strongstructuring forces of amphibian communities andshould be included in any model of expected amphibiancommunity structure.

Models of community structure and the response ofcommunities to disturbance are based on trade-offs inlife history traits that maximize fitness on one portionof the hydroperiod gradient while decreasing fitness onother portions of the gradient (Wellborn et al. 1996).Wellborn et al. (1996) suggested two transitions alongthe hydroperiod gradient: (1) a permanence transitionwhere hydroperiod length becomes long enough to sup-port large invertebrate predators and very active, rap-idly developing prey are replaced by larger, moderatelyactive prey, and (2) a predator transition where physicalconditions allow the replacement of invertebrate pred-ators by fish and large, moderately active prey are re-placed by small, inactive prey. We found three tran-sitions (between four groups) in our study, the lattertwo corresponding to the transitions proposed for tem-porate systems. The first transition was between shortand medium length hydroperiod wetlands and does notappear to correspond to any of the transitions suggestedby Wellborn et al. (1996). This transition was definedmore by an increase in species richness with only onespecies, Ambystoma opacum, being characteristic ofshort hydroperiod wetlands. A. opacum is the onlyabundant species occurring in our survey that lays eggsin terrestrial habitats before wetlands fill (Noble andBrady 1933). The habit of laying eggs before wetlandsfill may effectively increase the hydroperiod length ofwetlands for A. opacum, allowing this species to takeadvantage of a ‘‘priority effect’’ (Alford and Wilbur1985, Wilbur and Alford 1985).

Developing expectations of larval amphibianassemblage structure

The application of general models of communitystructure in lentic systems to larval amphibian assem-blages in southeastern coastal plain wetlands suggeststhat models of lentic community structure can serve astemplates for development of sampling plans for de-fining conditions in minimally disturbed systems. Weused general models to develop expectations of larvalamphibian assemblage structure for four groups of wet-lands at the SRS. Our methods consisted of quantita-tively sampling (i.e., determining relative frequency ofoccurrence) fish and larval amphibians at wetlands dur-ing the period of the year when they are most likelyto occur. Gascon (1991) successfully applied this meth-od in quantifying the distributions of anurans in tropicalwetlands and McDiarmid (1994) suggested ‘‘samplinglarvae may be a more efficient and quicker method forinventorying species at a site than sampling adults.’’However, this method is likely to miss species withshort larval periods and low breeding success (e.g.,small chance of larvae making it to metamorphosis).This appears to be the case in our sampling. We col-

lected three of the five species determined to success-fully reproduce in one wetland with a drift fence com-pletely surrounding it (D. Scott, unpublished data). Atotal of three individuals of the two species we missedwere collected at the drift fence while greater than tenindividuals of each species we did collect were col-lected at the drift fence. Thus, our methods underes-timate species richness, but do provide a relative mea-sure that can be used in biological monitoring and as-sessment.

We only sampled wetlands for one year; however,wetland hydrology and amphibian assemblage structurevary greatly from year to year at the SRS (Pechmannet al. 1989, Semlitsch et al. 1996). Year to year vari-ation in hydrology can be a critical factor in assessingchanges in amphibian populations at an individual wet-land (Pechmann et al. 1991, Pechmann and Wilbur1994), but may be less critical for developing expec-tations of larval amphibian structure at SRS referencesites. By substituting space for time, variation in as-semblage structure across important environmentalgradients can be estimated. We chose wetlands for sam-pling so as to include the range of hydroperiods ex-hibited by wetlands at the SRS. We assumed that sam-pling an individual wetland for a number of yearswould produce similar results. Comparison of our re-sults with those from a single site, sampled over anumber of years, suggests this assumption is valid.Semlitsch et al. (1996) reported on drift fence samplingof metamorphs over a 16-yr period at Rainbow Bay,an isolated wetland on the SRS. Hydroperiods at Rain-bow Bay ranged from 3 d to 365 d during the 16 yr ofstudy, but fish were never present. Species richnessranged from 0–15 and was positively correlated (r 50.84, P , 0.001) with hydroperiod (measured in num-ber of days water was present) at Rainbow Bay. Forour spatial survey, richness ranged from 0–12 speciesand was also positively correlated (r 5 0.88, P , 0.001)with hydroperiod (measured with drying scores) amongwetlands without fish. Substituting space for time maybe an option for developing expectations at the SRS,where hydroperiod length is highly correlated with var-iation in larval amphibian assemblage structure. How-ever, in other regions where amphibian breeding activ-ities are influenced more by other characteristics of thehydrological cycle, such as the distribution of rainfallduring the breeding season, space may not be a goodsubstitute for time.

Characterizing wetland hydroperiods is difficult. Ouruse of drying scores represents a compromise betweenobtaining precise data (e.g., the number of days a wet-land holds water a year) and the logistical constrainsof gathering such data. The strong relationship betweenassemblage structure and our drying scores suggeststhis measure is adequate for characterizing hydroper-iods on the upper southeastern Coastal Plain. We adviserestricting measures of hydroperiod to the year of sam-pling because of the large degree of hydroperiod var-


iation among years and the documented correlation ofassemblage variation with hydroperiod variation (Pech-mann et al. 1989, Semlitsch et al. 1996).

In conclusion, Hart (1994) suggested that incorpo-rating ecological constructs into the design of biolog-ical monitoring programs would increase the efficiencyand accuracy of these programs. We were able to usegeneral models of lentic community structure that haveemerged from numerous observational and experimen-tal studies (Wellborn et al. 1996) to design a samplingprogram that accounted for significant natural variationin larval amphibian assemblage structure. This varia-tion can now be incorporated into future models ofexpected larval amphibian assemblage structure. Hart(1994) also suggested that biological monitoring pro-grams could provide data for testing ecological con-structs. Our study provided a specific test of the abilityof lentic community models developed in temporatesystems to predict patterns in southeastern depressionwetlands. Overall, our results suggest that ecologicalconstructs can be applied in solving ‘‘real-world’’ prob-lems. Our findings, along with those of others who haveused the results of experiments to develop models thataccurately predict patterns in nature (e.g., Resetaritsand Fauth 1998), argue for closer ties between basicand applied research.

ACKNOWLEDGMENTS

We thank J. W. Ackerman for help with fieldwork. We thankI. L. Brisbin, Jr. and J. W. Gibbons for reviews of earlierdrafts of the manuscript that greatly improved the final ver-sion. Ronn Altig graciously assisted with the identificationof ranid tadpoles. This research was supported by FinancialAssistance Award Number DE-FC09-96SR18546 from theU.S. Department of Energy to the University of Georgia Re-search Foundation (J. W. Snodgrass and A. L. Bryan, Jr.) andthe Consortium for Risk Evaluation with Stakeholder Partic-ipation through the Department of Energy AI DE-FC01-95EW55084 (J. W. Snodgrass and J. Burger).

LITERATURE CITED

Alford, R. A., and H. M. Wilbur. 1985. Priority effects inexperimental pond communities: competition between Bufoand Rana. Ecology 66:1097–1105.

Altig, R. 1970. A key to the tadpoles of the continental UnitedStates and Canada. Herpetologica 26:180–207.

Bradford, D. F. 1989. Allotopic distribution of native frogsand introduced fishes in high Sierra Nevada lakes of Cal-ifornia: implication of the negative effect of fish introduc-tion. Copeia 1989:775–778.

Bronmark, C., and P. Edenhamn. 1994. Does the presence offish affect the distribution of tree frogs (Hyla arborea)?Conservation Biology 8:841–845.

Collins, J. P., and H. M. Wilbur. 1979. Breeding habits andhabitats of amphibians of the Edwin S. George Reserve,Michigan, with notes on the local distribution of fishes.Occasional Papers, Museum of Zoology, University ofMichigan 686:1–34.

Gascon, C. 1991. Population- and community-level analysesof species occurrences of central Amazonian rainforest tad-poles. Ecology 72:1731–1746.

Gibbons, J. W., and R. D. Semlitsch. 1991. Guide to thereptiles and amphibians of the SRS. University of GeorgiaPress, Athens, Georgia, USA.

Hart, D. D. 1994. Building a stronger partnership between

ecological research and biological monitoring. Journal ofthe North American Benthological Society 13:110–116.

Healy, W. R. 1974. Population consequences of alternativelife histories in Notophthalmus v. viridescens. Copeia 1974:221–229.

Hecnar, S. J., and R. T. M’Closkey. 1997. The effects ofpredatory fish on amphibian species richness and distri-bution. Biological Conservation 79:123–131.

Heyer, W. R., R. W. McDiarmid, and D. L. Weigmann. 1975.Tadpoles, predation and pond habitats in the tropics.BioTropica 7:100–111.

Karr, J. R., and E. W. Chin. 1997. Biological monitoring andassessment: using multimetric indexes effectively. Envi-ronmental Protection Agency Paper 235-R97–001, Uni-versity of Washington, Seattle, Washington, USA.

Kirkman, L. K., R. F. Lide, G. Wein, and R. R. Sharitz. 1996.Vegetation change and land-use legacies of depression wet-lands of the western Coastal Plain of South Carolina: 1951–1992. Wetlands 16:564–576.

Lide, R. F., V. G. Meentemeyer, J. E. Pinder, III, and L. M.Beatty. 1995. Hydrology of a Carolina bay located on theupper Coastal Plain of western South Carolina. Wetlands15:47–57.

Marchant, R., A. Hirst, R. H. Norris, R. Butcher, L. Metzeling,and D. Tiller. 1997. Classification and prediction of ma-croinvertebrate assemblages from running waters in Vic-toria, Australia. Journal of the North American Benthol-ogical Society 16:664–681.

Matthews, W. J. 1998. Patterns in freshwater fish ecology.Chapman & Hall, New York, New York, USA.

McDiarmid, R. W. 1994. Amphibian diversity and naturalhistory: an overview. Pages 5–15 in W. R. Heyer, M. A.Donnelly, R. W. McDiarmid, L. C. Hayek, and M. S. Foster,editors. Measuring and monitoring biological diversity:standard methods for amphibians. Smithsonian Institution,Washington, D.C., USA.

Newman, M. C., and J. F. Schalles. 1990. The water chem-istry of Carolina bays: a regional survey. Archives FurHydrobiologia 118:147–168.

Noble, G. K., and M. K. Brady. 1933. Observations on thelife history of the marbled salamander Ambystoma opacumGravenhorst. Zoologica 11:89–132.

Parsons, M., and R. H. Norris. 1996. The effects of habitat-specific sampling on biological assessment of water qualityusing a predictive model. Freshwater Biology 36:419–434.

Pechmann, J. H. K., D. E. Scott, J. W. Gibbons, and R. D.Semlitsch. 1989. Influence of wetland hydroperiod on di-versity and abundance of metamorphosing juvenile am-phibians. Wetlands Ecology and Management 1:3–11.

Pechmann J. H. K., D. E. Scott, R. D. Semlitsch, J. P. Cald-well, L. J. Vitt, and J. W. Gibbons. 1991. Declining am-phibian populations: the problem of separating human im-pacts from natural fluctuations. Science 253:892–895.

Pechmann, J. H. K., and H. M. Wilbur. 1994. Putting de-clining amphibian populations in perspective: natural fluc-tuations and human impacts. Herpetologica 50:65–84.

Resetarits, W. J., Jr., and J. E. Fauth. 1998. From cattle tanksto Carolina bays: the utility of model systems for under-standing natural communities. Pages 133–151 in W. J. Re-setarits Jr. and J. Bernardo, editors. Experimental ecology:issues and perspectives. Oxford University Press, NewYork, New York, USA.

Reynoldson, T. B., R. C. Bailey, K. E. Day, and R. H. Norris.1995. Biological guidelines for freshwater sediment basedon BEnthic Assessment of SedimenT (the BEAST) usinga multivariate approach for predicting biological state. Aus-tralian Journal of Ecology 20:198–219.

Reynoldson, T. B., R. H. Norris, V. H. Resh, K. E. Day, andD. M. Rosenberg. 1997. The reference condition: a com-parison of multimetric and multivariate approaches to as-


sess water-quality impairment using benthic macroinver-tebrates. Journal of the North American Benthological So-ciety 16:833–852.

Schalles, J. F., R. R. Sharitz, J. W. Gibbons, G. J. Leversee,and J. N. Knox. 1989. Carolina bays of the Savannah RiverPlant. National Environmental Research Park Program, Sa-vannah River Ecology Laboratory, Aiken, South Carolina,USA.

Schalles, J. F., and D. J. Shure. 1989. Hydrology, communitystructure, and productivity patterns of a dystrophic Carolinabay wetland. Ecological Monographs 59:365–385.

Schneider, D. W., and T. M. Frost. 1996. Habitat durationand community structure in temporary ponds. Journal ofthe North American Benthological Society 15:64–86.

Semlitsch, R. D. 1985. Reproductive strategy of a faculta-tively paedomorphic salamander Ambystoma talpoideum.Oecologia (Berlin) 65:305–313.

Semlitsch, R. D., D. E. Scott, J. H. K. Pechmann, and J. W.Gibbons. 1996. Structure and dynamics of an amphibiancommunity: evidence from a 16-year study of a naturalpond. Pages 217–248 in M. L. Cody and J. Smallwood,editors. Long-term studies of vertebrate communities. Ac-ademic Press, Orlando, Florida, USA.

Snodgrass, J. W., A. L. Bryan, Jr., R. Lide, and G. Smith.1996. Factors affecting the occurrence and structure of fishassemblages in isolated wetlands of the upper coastal plain,U.S.A. Canadian Journal of Fisheries Aquatic Sciences 53:443–454.

ter Braak, C. J. F. 1986. Canonical correspondence analysis:

a new eigenvector technique for multivariate direct gradientanalysis. Ecology 67:1167–1179.

ter Braak, C. J. F. 1988. CANOCO—a FORTRAN programfor canonical community ordination. Microcomputer Pow-er, Ithaca, New York, USA.

Tonn, W. M., and J. J. Magnuson. 1982. Patterns in the fishcomposition and richness of fish assemblages in northernWisconsin lakes. Ecology 63:1149–1166.

Travis, J. 1981. A key to the tadpoles of North Carolina.Brimleyana 6:119–127.

Wellborn, G. A., D. K. Skelly, and E. E. Werner. 1996. Mech-anisms creating community structure across a freshwaterhabitat gradient. Annual Review of Ecology & Systematics27:337–363.

Wiggins, G. B., R. J. MacKay, and I. M. Smith. 1980. Evo-lutionary and ecological strategies of animals in annualtemporary pools. Archiv fur Hydrobiologia, Supplement58:97–206.

Wilbur, H. M. 1984. Complex life cycles and communityorganization in amphibians. Pages 195–224 in P. W. Price,C. N. Slobodchikoff, and W. S. Gaud, editors. A new ecol-ogy: novel approaches to interactive systems. John Wiley,New York, New York, USA.

Wilbur, H. M., and R. S. Alford. 1985. Priority effects inexperimental pond communities: response of Hyla to Bufoand Rana. Ecology 66:1106–1114.

Wright, J. F. 1995. Development and use of a system forpredicting the macroinvertebrate fauna in flowing waters.Australian Journal of Ecology 20:181–197.

Zar, J. H. 1984. Biostatistical analysis. Second edition. Pren-tice Hall, Englewood Cliffs, New Jersey, USA.


APPENDIX ATotal number of individuals of 25 species collected from 22 depression wetlands on the upper coastal plain of South

Carolina.

Species

Wetland number

Short hydroperiod

99 172 92 10 189 17

Medium hydroperiod

27 168 66 78 87

Ambystoma opacum 5 68 20 2 36 145 44 39 11Eurycea quadridigitata 1 5 2 2Pseudacris ornata 6 160 29 22Pseudacris nigrita 19 61 14Gastrophryne carolinensis 6 14 12 12 14Hyla femoralis 47 39 756 64Notophthalmus viridescens‡ 7 6 1 4 8 1 19 4Pseudacris crucifer 25 150 2 2 123 233 2 47Ambystoma talpoideum§ 1 3 4 71 107 25 41 39Bufo terrestris 65 286 1455 386Rana utricularia 37 43 4 856 525 743 245 147Hyla gratiosaRana clamitansRana grylioAcris gryllusRana catesbeianaAmphiuma means‡Siren intermedia‡Acris crepitansSiren lacertina‡Pseudacris triseriataRana virgatipesAmbystoma tigrinumHyla chrysoscelisScaphiopus holbrooki

1

1

6

1

5

1310

RichnessTotalDrying score

(1990 and 1997, 1997)

313

2, 1

7143

3, 1

223

4, 1

346

5, 2

3187

5, 1

5159

6, 2

91101

6, 3

10875

6, 4

122307

6, 4

91868

8, 3

71962

8, 4

Notes: All individuals were larval forms unless otherwise noted. Wetlands are grouped based on relative hydroperiod andthe presence or absence of fish. Total numbers collected and number of occurrences for each species are given at the right.Drying scores and total number of species and individuals collected in each wetland are given at the bottom. Drying scoresincluding 1990 and 1997 wetland visits and for 1997 visits only are included.

‡ Counts for these species include larva and adult stages and both were used in analyses.§ Counts include larva and paedomorphic adults and both were used in analyses.

APPENDIX BTotal number of fish collected in the six wetlands with fish populations, listed by species.

Species

Wetland number

40 77 139 142 143 147 Total

Acantharchus pomotisErimyzon sucettaEsox americanusLepomis marginatusNotemigonus crysoleucasAmeiurus natalisCentrarchus macropterusGambusia holbrookiLepomis gulosusEnneacanthus gloriosusFundulus lineolatusUmbra pygmae

Total

6012101110

103

12931

721

1113

302

3945

9

93

333

171

62234

1

351

59

32

57

741

58

236

46

46

32091753310

1180241

174

1104

1131


APPENDIX A. Extended.

Wetland number

Long hydroperiod (no fish)

31 176 83 123 3

Long hydroperiod (fish)

147 77 143 40 139 142Total

collected

No. ofoccur-ences

1

477

1

3

43

2645243

412

380

3410

316

20

111

2

57

42208137

80

6

211693

1

8

158329

1

5629

1

2

12

37113

2179449

920104651

126140362831

104

1064357

141314

915

62

1

5

791

7, 5

3

9

8381

8, 5

11524

55

9589

8, 5

87

49

997

8, 5

17238

1

12512

10, 5

559

48

233

1

12258

8, 5

1

30

16

10

91669

8, 5

1

1

3

1

46

9, 5

12

16

5104

10, 5

931

1

617

10, 5

106

187

174

956

10, 5

22751

1053513122228

2251

1310

2512 464

11667454422111

development of expectations of larval amphibian assemblage structure in southeastern depression...

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