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Effects of the Anuran Tadpole Assemblageand Nutrient Enrichment on Freshwater SnailAbundance (Physella sp.)Author(s): Geoffrey R. Smith, Amber A. Burgett, and Jessica E.RettigSource: The American Midland Naturalist, 168(2):341-351. 2012.Published By: University of Notre DameDOI: http://dx.doi.org/10.1674/0003-0031-168.2.341URL: http://www.bioone.org/doi/full/10.1674/0003-0031-168.2.341

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Effects of the Anuran Tadpole Assemblage and NutrientEnrichment on Freshwater Snail Abundance (Physella sp.)

GEOFFREY R. SMITH,1 AMBER A. BURGETT2, AND JESSICA E. RETTIGDepartment of Biology, Denison University, Granville, Ohio 43023

ABSTRACT.—Alterations of aquatic ecosystems, such as nutrient enrichment and changes incommunity composition, can potentially have effects that pervade the entire community. Weinvestigated the effects of nutrient enrichment and changes in the presence and density of twospecies of tadpoles, American toad (Anaxyrus americanus) and Gray treefrog (Hyla versicolor), onfreshwater snail abundance (Physella sp.). At low tadpole density, there was no difference in theabundance of Physella sp. among treatments. At high tadpole density, treatments with bothspecies of tadpoles present and nutrient enrichment had a higher abundance of Physella than allother treatment combinations. Mesocosms with high tadpole densities had lower periphyton drymass than those with low overall tadpole density. At the end of the experiment, increasedabundance of Physella was related to earlier metamorphosis in A. americanus and H. versicolor andhigher proportions of H. versicolor metamorphosing and surviving. Nutrient enrichment did notindependently affect snails. Our results suggest that changes in the composition and density oftadpole assemblages can interact with nutrient enrichment to drive variation in freshwater snailabundances, indicating that ongoing declines in amphibian populations combined withcontinued anthropogenic nutrient enrichment of freshwater ecosystems may have complexeffects on freshwater snail populations.

INTRODUCTION

The composition of a community can have an impact on the outcome of community-levelinteractions. In some cases, community composition can increase or alter the intensity ofnegative interactions, such as competition and predation. For example, communitycomposition changes the intensity of competition in grassland plants (Elmendorf andMoore, 2007), and predator identity and diversity can affect how predation impacts prey(e.g., oysters, O’Connor et al., 2008; herbivores, Otto et al., 2008). Community compositioncan also influence positive interactions among species. For example, certain combinationsof shredder insects show facilitation compared to other combinations of shredders (Dangleset al., 2011) or the presence of an herbivore may facilitate the invasion of certain plantspecies into a community (Madrigal et al., 2011). Thus, variation in the composition of oneaspect of a community can have impacts for the other species in the community.

In addition, the abiotic context of a community can alter the outcome or influence ofcommunity-level interactions (e.g., Brose and Tielborger, 2005; Hughes and Grabowski,2006; Werner and Peacor, 2006). One potentially important aspect of the environment thatcan influence the effect of community context is the allochthonous input of nutrients. Inaquatic ecosystems agricultural run-off is a major source of allochthonous nutrientenrichment (Foley et al., 2005; Holland et al., 2005; Broussard and Turner, 2009). Nutrientenrichment has the potential to alter the quantity or quality of primary producers, withconsequences for the entire food web (e.g., Anderson and Polis, 2004; DeAngelis andMulholland, 2004; Cottingham et al., 2004). Further, the interaction of community context

1 Corresponding author: Telephone: (740) 587-9847; FAX: (740) 587-6417; e-mail: smithg@denison.edu

2 Present Address: Department of Biology, Wittenberg University, Springfield, Ohio 45501

Am. Midl. Nat. (2012) 168:341–351

341

and nutrient enrichment can result in significant effects on several components of aquaticecosystems (e.g., Leibold and Wilbur, 1992).

Several previous studies have provided evidence for competitive interactions betweensnails and tadpoles (e.g., Bronmark et al., 1991; Holomuzki and Hemphill, 1996; Lefcortet al., 1999; Rohr and Crumrine, 2005). The presence of interactions between snails andtadpoles is not surprising given that they may feed on similar resources (e.g., periphyton),although there may be some subtle differences in their use of phytoplankton andperiphyton (Harris, 1995). In particular, Holomuzki and Hemphill (1996) found that bothPhysella snails and Anaxyrus americanus tadpoles were negatively affected by each other, withreproduction reduced in Physella and development and biomass reduced in A. americanus. Incontrast, Hyla versicolor tadpoles were not affected by the presence of Pseudosuccinea snails(Kiesecker and Skelly, 2001), suggesting H. versicolor tadpoles may not compete with snails.Thus, it appears that alterations in the composition of the anuran tadpole assemblage couldhave ramifications for snail populations. For example, if the relative abundance of A.americanus and H. versicolor tadpoles were to vary, one might expect the competitive impacton snail populations might differ such that assemblages of tadpoles with more A. americanuswould have a greater impact on snails than those assemblages with more H. versicolor.

Since snails and tadpoles may compete over a common algal resource, factors that influenceprimary productivity in aquatic ecosystems might also influence the interactions between snails andtadpoles. As indicated above, anthropogenic nutrient enrichment is one factor that can affectprimary productivity in aquatic ecosystems by altering the quantity or quality of primary producers.It might therefore be expected that such nutrient enrichment could alter the ineractions betweentadpoles and snails by altering the quality and/or quantity of primary producers.

Using mesocosms designed to mimic local ponds, we manipulated the composition of thelarval amphibian assemblage consisting of two anuran tadpoles, gray treefrogs (Hyla versicolor),and American toads (Anaxyrus americanus) and simulated anthropogenic nutrient enrichmentby adding nitrate and phosphate to examine their effects on freshwater snails (Physella sp.). Dueto differences in feeding rates and use of feeding habitat by these two genera of tadpoles [e.g.,generally higher consumption rate by Anaxyrus than Hyla (Richardson, 2002); lower thresholdconcentration in Anaxyrus than in Hyla (Seale and Beckvar, 1980); greater use of phytoplanktonin the water column in Hyla than in Anaxyrus, (Beiswinger, 1977; Wilbur and Alford, 1986)], wepredicted that variation in the presence and density of H. versicolor and A. americanus tadpoleswould affect snail abundance via their differential effects on primary producers. In particular,we predicted that A. americanus would have greater effects on snail abundance than H. versicolor.We also expected that higher snail abundance at the end of the experiment would result inlowered tadpole performance (e.g., survivorship, growth, and development) and that A.americanus would be more affected than H. versicolor. Indeed, as mentioned above, A. americanustadpoles showed slowed development and lower biomass in the presence of Physella snails(Holomuzki and Hemphill, 1996), whereas snails (Pseudosuccinea) had no effect on H. versicolortadpoles (Kiesecker and Skelly, 2001), suggesting greater potential for competition betweensnails and A. americanus than between snails and H. versicolor. Given the effects that nutrientenrichment may have on primary producers, we predicted that nutrient enrichment woulddirectly or indirectly positively affect snail abundance. We also predicted that nutrientenrichment would reduce any negative effects of tadpole manipulations on snail abundance.

METHODS

We collected several egg masses representing clutches from multiple females (.3) ofAnaxyrus americanus and Hyla versicolor from a small pond on the Denison University

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Biological Reserve located in Licking Co., Ohio, USA (40u59N, 82u319W) and incubatedthem in aged tapwater at 17–19 C in the laboratory. After hatching, tadpoles weremaintained in plastic containers (54 cm 3 35 cm 3 16 cm) and fed ground Purina RabbitChow ad libitum until they were transferred to mesocosms at Gosner stage 25 (Gosner, 1960).Snails (Physella sp.) were collected from the same small pond as the egg masses.

We used 1135 L cattletanks (N 5 36) filled with 800 L (depth 5 44 cm) of well water(conductivity 5 453 mS, dissolved oxygen 5 9.56 mg L21, nitrate-N 5 2 ppm, phosphate-P, 1 ppm, ammonium-N # 0.1 ppm, hardness 5 180 ppm) to establish our experimentalcommunities. Mesocosms were placed in an open field so that all mesocosms received thesame natural light regime. Mesocosms were filled from 14–22 May 2003 and on 22 May weadded 50 g of Purina Rabbit Chow pellets and 8 L of deciduous leaf litter [mostly (<70%)maple leaves, Acer spp., with some oak leaves, Quercus spp.] to provide a nutrient source andstructure to the mesocosm. Mesocosms were inoculated with zooplankton and phytoplank-ton concentrates from local ponds on 23 May 2003 and again on 27 May 2003. Colonizationof mesocosms by macroinvertebrates and other amphibians was prevented by attaching acover of fiberglass window screen (1 mm mesh) to each cattletank. Since the local pondwhere we collected the Anaxyrus americanus and Hyla versicolor egg masses also has Lithobatescatesbeianus, we added 40 tadpoles of L. catesbeianus (mean mass 5 0.007 6 0.0003 g; density5 50 m23) to each mesocosm on 6 Jun. 2003. In addition, given the very large egg massesand numbers of tadpoles produced by L. catesbeianus, we included a higher density of thesetadpoles than the other tadpoles.

We used a 3 3 2 3 2 fully factorial experimental design (replicated three times) thatincluded three anuran tadpole assemblage composition treatments (Hyla versicolor only,Anaxyrus americanus only, both H. versicolor and A. americanus) at two densities [low 5 total of18 tadpoles (density 5 22.5 m23); high 5 total of 36 tadpoles (density 5 45 m23)], with twonutrient treatments (no enrichment vs. enrichment). For treatments with both species oftadpoles we introduced an equal number of each species. Because the primary intent of thisexperiment was to examine interactions between the species of tadpoles (Smith andBurgett, 2012), there was no ‘‘control’’ treatment that lacked all tadpoles. However, thisparticular design does allow us to examine how changes in the density and composition of atadpole assemblage may affect snail abundance. We added tadpoles of A. americanus (meanmass 5 0.008 6 0.0004 g) and H. versicolor (mean mass 5 0.010 6 0.001 g) to mesocosms on23 May 2003. We added 15 snails to each mesocosm on 27 May 2003 (density 5 19 m23).Tadpole and snail densities in local ponds ranged from 26–176.4 m23 for hylids, 0.38–58.4 m23 for bufonids, 0.46–57.5 m23 for ranids, and 58.8–468.9 m23 for snails (Smith et al.,2003a, b). To enriched mesocosms we added nutrients (8 mg L21 NO3 and 2 mg L21 PO4)every 14 d starting on 2 Jun. 2003 to simulate periodic run-off events. These concentrationsare within the range of concentrations observed in ponds in agricultural regions of the USA(e.g., Sims et al., 1998; Rouse et al., 1999).

The experiment was terminated after 52 d on 14 Jul. 2003. At the end of the experiment,we collected and counted the snails, metamorphs of Anaxyrus americanus and metamorphsand tadpoles of Hyla versicolor (not all had metamorphosed by the time the experiment wasterminated) from each mesocosm. All snails were generally similar in size at the end of theexperiment, and thus we did not weigh them and instead used abundance of snails in ouranalyses. For A. americanus, we allowed metamorphosis to occur, removing metamorphsdaily when both forelimbs had emerged (Gosner Stage 42). We housed the metamorphs inthe laboratory in plastic containers with access to water but not food until the tail wasresorbed, and then weighed them. The number of days to metamorphosis was counted from

2012 SMITH ET AL.: TADPOLE ASSEMBLAGE EFFECTS ON SNAIL ABUNDANCE 343

the starting date of the experiment to the day when the tail was fully resorbed. For H.versicolor, we allowed tadpoles to undergo metamorphosis and treated the metamorphs inthe same way as for A. americanus. However, not all of the H. versicolor tadpoles hadmetamorphosed by the time the experiment was terminated. We thus removed all survivingGray Treefrog tadpoles and counted them (for inclusion in survivorship estimates andproportion metamorphosing but not in the mass analysis). After draining the mesocosms,we scraped the periphyton from a specific area (15.5 cm 3 22.8 cm) on the south-facinginterior wall of each mesocosm. Since the area scraped was from the same area on allmesocosms, they all received the same amount of incident sunlight throughout theexperiment. We then allowed the periphyton to air dry at room temperature until constantmass was achieved, and we used this final periphyton dry mass as our estimate of periphytonproductivity.

Prior to using parametric analyses, we confirmed that their assumptions were met. Weused ANOVAs to analyze treatment effects on snail abundance and periphyton dry mass. Bythe end of the experiment, the mesocosms varied in several measures of tadpole growth andsurvivorship. To examine the potential effects of snails on each species of tadpole, weregressed tadpole survivorship, metamorph mass, and time to metamorphosis on snailabundance. All statistical analyses were conducted on mesocosm means. We removed onemesocosm (high density, Anaxyrus americanus and Hyla versicolor, Enrichment) from ouranalyses because of a bloom of red algae early in the experiment.

RESULTS

There was a significant, complex three-way interaction that influenced the number ofPhysella sp. in the mesocosms at the end of the experiment (3-way interaction; Fig. 1; F2,23 5

3.78, P 5 0.038). At low density, there was little difference in snail abundance among theassemblage composition and nutrient enrichment treatments. However, at high density, themixed assemblage composition with nutrient enrichment had significantly more Physella sp.than the other treatments. There was also a significant assemblage composition effect withhigher snail abundance in the mixed assemblage composition treatment (F2,23 5 4.28, P 5

0.026). No other treatment or interaction was significant (all P . 0.065).At the end of the experiment, there was no relationship between the number of Physella

sp. and Anaxyrus americanus survivorship (Fig. 2A; N 5 23, r2 5 0.007, P 5 0.69). There was asignificant negative relationship between the mean days to metamorphosis and theabundance of Physella sp. such that earlier metamorphosis by A. americanus was associatedwith greater abundances of Physella sp. [Fig. 2B; N 5 23, r2 5 0.21, P 5 0.030; mean days tometamorphosis 5 32.11–0.0013(Physella)]. There was no relationship between the numberof Physella sp. and mean A. americanus metamorph mass (Fig. 2C; N 5 23, r2 5 0.06, P 5

0.25).The survivorship of Hyla versicolor (metamorphs and surviving tadpoles) was positively

related to the number of Physella sp. at the end of the experiment [Fig. 3A; N 5 23, r2 5

0.18, P 5 0.043; survivorship 5 0.52 + 0.00017(Physella)]. The proportion of H. versicolor thatmetamorphosed was positively related to the number of Physella sp. [Fig. 3B; N 5 22, r2 5

0.35, P 5 0.0038; proportion metamorphosing 5 0587 + 0.00024(Physella)]. The meannumber of days to metamorphosis for H. versicolor was negatively related to the number ofPhysella sp. at the end of the experiment [Fig. 3C; N 5 21, r2 5 0.27, P 5 0.016; mean days tometamorphosis 5 45.57–0.0031(Physella)]. The mean mass of H. versicolor metamorphs wasnot related to the number of Physella sp. at the end of the experiment (Fig. 3D; N 5 20, r2 5

0.15, P 5 0.089).

344 THE AMERICAN MIDLAND NATURALIST 168(2)

High density mesocosms (regardless of tadpole assemblage composition or enrichmenttreatment) had lower periphyton dry mass than low density mesocosms [low density: 0.6386 0.123 g (N 5 18), high density: 0.354 6 0.096 g (N 5 17); F1,23 5 5.42, P , 0.0001].Periphyton dry mass at the end of the experiment was lower in enrichment than noenrichment treatments [control: 0.794 6 0.104 g (N 5 18), enriched: 0.189 6 0.068 (N 5

17); F1,23 5 22.4, P , 0.0001]. No other factor or interaction term was significant (seeFig. 4).

DISCUSSION

Differences in the tadpole assemblages, both in terms of tadpole density and thecomposition of the tadpole assemblage, in our experimental mesocosms interacted withnutrient enrichment to affect snail (Physella sp.) abundance. This significant interactionprimarily reflects the very high mean abundance of snails in the high density, nutrientaddition treatments with tadpoles of both Anaxyrus americanus and Hyla versicolor. Thepatterns of snail abundance to some extent parallels the observed mean periphyton drymass at the end of the experiment (see Fig. 4). Although the interaction was not statisticallysignificant and the peak is not very high in the periphyton dry mass, the similarity betweenthe three-way interaction plots for snail abundance and periphyton dry mass is clear.However, it is not clear why this particular pattern was observed, and it is not what we wouldhave predicted. Our results suggest further research on this question is warranted, especiallyexplorations of how tadpoles and snails interact with their resources.

Our results also suggest that snails had some effects on the tadpoles in our experiment.For example, the negative relationships between the number of Physella sp. at the end of theexperiment and the mean number of days to metamorphosis in Anaxyrus americanus maysuggest that increasing numbers of Physella sp. may have somehow accelerated thedevelopment of A. americanus tadpoles. We also found no effect of Physella abundance at theend of the experiment on A. americanus survivorship and metamorph mass. Our resultscontrast with the results of the experiment conducted by Holomuzki and Hemphill (1996)that found development was slowed in A. americanus tadpoles in the presence of Physellasnails. However, the densities used in our experiment were lower than those used in

FIG. 1.—The effect of the interaction of nutrient enrichment treatment, tadpole density, andcommunity composition on the abundance of Physella sp. Anaxyrus 5 only A. americanus tadpoles, Mix 5

both A. americanus and H. versicolor tadpoles, and Hyla 5 only H. versicolor tadpoles. Circles denote lowtadpole density treatments and squares denote high tadpole density treatments. Open symbols denoteno nutrient addition treatments and closed symbols denote nutrient addition treatments. In cases wherethe error bars are not visible, they are smaller than the symbol. Means are given 6 1 SE

2012 SMITH ET AL.: TADPOLE ASSEMBLAGE EFFECTS ON SNAIL ABUNDANCE 345

346 THE AMERICAN MIDLAND NATURALIST 168(2)

Holomuzki and Hemphill (1996). It may be that the direction of the effects of Physella snailson A. americanus tadpole development may be dependent on the density of snails and/ortadpoles.

We also observed positive relationships between snail abundance and the proportion ofHyla versicolor tadpoles that metamorphosed and their survivorship, and a negativerelationship between snail abundance and the days to metamorphosis of H. versicolor.These relationships suggest that snails and H. versicolor are either facilitating each other or

r

FIG. 2.—The relationships between the abundance of Physella snails and (A) survivorship, (B) meannumber of days to metamorphosis, and (C) mean metamorph mass of Anaxyrus americanus tadpoles

FIG. 3.—The relationships between the abundance of Physella snails and (A) survivorship, (B)proportion metamorphosing, (C) mean number of days to metamorphosis, and (D) mean metamorphmass of Hyla versicolor tadpoles

2012 SMITH ET AL.: TADPOLE ASSEMBLAGE EFFECTS ON SNAIL ABUNDANCE 347

positively reacting to the same conditions. Because Hyla and Anaxyrus tadpoles likely use theperiphyton resource differently (e.g., bufonids tend to have higher consumption rates andassimilation rates than hylids, Richardson, 2002; Anaxyrus uses benthic algae more thanHyla, and Hyla use algae in the water column more than Anaxyrus, Beiswinger, 1977; Wilburand Alford, 1985), they may have different effects on snails. For example, Hyla mayregenerate or relocate nutrients to the ecosystem differently than Anaxyrus (e.g., Hyla mayrelocate nutrients from the open water column to the benthos) and thus have a positiveeffect on the resources used by the snails, as has been observed for tadpoles and isopods(Iwai and Kagaya, 2007). Our experiment does not allow us to establish the mechanisminducing the contrasting relationships between snail abundance and A. americanus and H.versicolor tadpoles; however, our results do suggest further examination of these potentialrelationships would be interesting.

Nutrient enrichment on its own did not affect snail abundance in our experiment;however, it did interact with tadpole assemblage composition and density. In previousexperiments, snail biomass or abundance increased with nutrient enrichment (e.g.,Hershey, 1992; Wojdak, 2005; Johnson et al., 2007), but sometimes the response wasdelayed (Hershey, 1992), absent (Fernandez-Alaez et al., 2004) or even negative (e.g.,Daldorph and Thomas, 1991; Armitage and Fong, 2004). Our results indicate that theeffects of anthropogenic nutrient enrichment on snails may depend upon the backgroundcommunity in which the snails are found.

In conclusion, our results suggest that changes in tadpole assemblages in association withother environmental alterations can have effects on diverse components of the broadercommunity, including snails. Such effects are potentially important because changes inamphibian assemblages through global amphibian declines (e.g., Alford and Richards, 1999;Stuart et al., 2004), or in changes in the anuran tadpole assemblage due to changes indistributions or timing of breeding due to habitat changes or climate change, could inducegreater impacts on the broader aquatic community and ecosystem. For example, anurantadpoles reduce primary productivity and inorganic sediments in tropical streams (Connellyet al., 2008), clear sediments in temperate ponds and lakes (Wood and Richardson, 2010),cause shifts in the composition of scraper and grazer assemblages of macroinvertebrates and

FIG. 4.—The effect of the interaction of nutrient enrichment treatment, tadpole density, andcommunity composition on periphyton dry mass. Anaxyrus 5 only A. americanus tadpoles, Mix 5 both A.americanus and H. versicolor tadpoles, and Hyla 5 only H. versicolor tadpoles. Circles denote low tadpoledensity treatments and squares denote high tadpole density treatments. Open symbols denote nonutrient addition treatments and closed symbols denote nutrient addition treatments. In cases wherethe error bars are not visible, they are smaller than the symbol. Means are given 6 1 SE

348 THE AMERICAN MIDLAND NATURALIST 168(2)

the productivity of shredders in tropical streams (Colon-Gaud et al., 2009, 2010), andincrease the quality of organic seston in tropical streams (Colon-Gaud et al., 2008).

Acknowledgments.—Funding was provided in part by the Sherman Fairchild Foundation, the HowardHughes Medical Institute, and an Amphibian Research and Monitoring Initiative/Declining AmphibianPopulations Task Force seed grant. Assistance during the experiment was provided by M. Tribue, W.Smith, and L. Smith. We thank two anonymous reviewers for their helpful comments on an earlierversion of this manuscript.

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SUBMITTED 22 JULY 2011 ACCEPTED 10 FEBRUARY 2012

2012 SMITH ET AL.: TADPOLE ASSEMBLAGE EFFECTS ON SNAIL ABUNDANCE 351