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Effects of the anuran tadpole assemblage and nutrient enrichment on freshwater snail abundance (Physella sp.).

INTRODUCTION

The composition of a community can have an impact on the outcome of community-level interactions. In some cases, community composition can increase or alter the intensity of negative interactions, such as competition and predation. For example, community composition changes the intensity of competition in grassland plants (Elmendorf and Moore, 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 composition can also influence positive interactions among species. For example, certain combinations of shredder insects show facilitation compared to other combinations of shredders (Dangles et al., 2011) or the presence of an herbivore may facilitate the invasion of certain plant species into a community (Madrigal et al., 2011). Thus, variation in the composition of one aspect 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 of community-level interactions (e.g., Brose and Tielborger, 2005; Hughes and Grabowski, 2006; Werner and Peacor, 2006). One potentially important aspect of the environment that can influence the effect of community context is the allochthonous input of nutrients. In aquatic ecosystems agricultural run-off is a major source of allochthonous nutrient enrichment (Foley et al., 2005; Holland et al., 2005; Broussard and Turner, 2009). Nutrient enrichment has the potential to alter the quantity or quality of primary producers, with consequences for the entire food web (e.g., Anderson and Polis, 2004; DeAngelis and Mulholland, 2004; Cottingham et al., 2004). Further, the interaction of community context and nutrient enrichment can result in significant effects on several components of aquatic ecosystems (e.g., Leibold and Wilbur, 1992).

Several previous studies have provided evidence for competitive interactions between snails and tadpoles (e.g., Bronmark et al., 1991; Holomuzki and Hemphill, 1996; Lefcort et al., 1999; Rohr and Crumrine, 2005). The presence of interactions between snails and tadpoles 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 and periphyton (Harris, 1995). In particular, Holomuzki and Hemphill (1996) found that both Physella snails and Anaxyrus americanus tadpoles were negatively affected by each other, with reproduction reduced in Physella and development and biomass reduced in A. americanus. In contrast, 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 could have 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 impact on snail populations might differ such that assemblages of tadpoles with more A. americanus would 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 influence primary productivity in aquatic ecosystems might also influence the interactions between snails and tadpoles. As indicated above, anthropogenic nutrient enrichment is one factor that can affect primary 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 between tadpoles and snails by altering the quality and/or quantity of primary producers.

Using mesocosms designed to mimic local ponds, we manipulated the composition of the larval amphibian assemblage consisting of two anuran tadpoles, gray treefrogs (Hyla versicolor), and American toads (Anaxyrus americanus) and simulated anthropogenic nutrient enrichment by adding nitrate and phosphate to examine their effects on freshwater snails (Physella sp.). Due to 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 threshold concentration in Anaxyrus than in Hyla (Seale and Beckvar, 1980); greater use of phytoplankton in the water column in Hyla than in Anaxyrus, (Beiswinger, 1977; Wilbur and Alford, 1986)], we predicted that variation in the presence and density of H. versicolor and A. americanus tadpoles would 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. versicoIor. We also expected that higher snail abundance at the end of the experiment would result in lowered tadpole performance (e.g., survivorship, growth, and development) and that A. americanus would be more affected than H. versicolor. Indeed, as mentioned above, A. americanus tadpoles showed slowed development and lower biomass in the presence of Physella snails (Holomuzki and Hemphill, 1996), whereas snails (Pseudosuccinea) had no effect on H. versicolor tadpoles (Kiesecker and Skelly, 2001), suggesting greater potential for competition between snails and A. americanus than between snails and H. versicolor. Given the effects that nutrient enrichment may have on primary producers, we predicted that nutrient enrichment would directly or indirectly positively affect snail abundance. We also predicted that nutrient enrichment would reduce any negative effects of tadpole manipulations on snail abundance.

METHODS

We collected several egg masses representing clutches from multiple females (>3) of Anaxyrus americanus and Hyla versicolor from a small pond on the Denison University Biological Reserve located in Licking Co., Ohio, USA (40[degrees]5'N, 82[degrees]31'W) and incubated them in aged tapwater at 17-19 C in the laboratory. After hatching, tadpoles were maintained in plastic containers (54 cm x 35 cm x 16 cm) and fed ground Purina Rabbit Chow 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 = 36) filled with 800 L (depth = 44 cm) of well water (conductivity = 453 mS, dissolved oxygen = 9.56 mg [L.sup.-1], nitrate-N = 2 ppm, phosphate-P < 1 ppm, ammonium-N [less than or equal to] 0.1 ppm, hardness = 180 ppm) to establish our experimental communities. Mesocosms were placed in an open field so that all mesocosms received the same natural light regime. Mesocosms were filled from 14-22 May 2003 and on 22 May we added 50 g of Purina Rabbit Chow pellets and 8 L of deciduous leaf litter [mostly ([approximately equals] 70%) maple leaves, Acer spp., with some oak leaves, Quercus spp.] to provide a nutrient source and structure to the mesocosm. Mesocosms were inoculated with zooplankton and phytoplankton concentrates from local ponds on 23 May 2003 and again on 27 May 2003. Colonization of mesocosms by macroinvertebrates and other amphibians was prevented by attaching a cover of fiberglass window screen (1 mm mesh) to each cattletank. Since the local pond where we collected the Anaxyrus americanus and Hyla versicolor egg masses also has Lithobates catesbeianus, we added 40 tadpoles of L. catesbeianus (mean mass = 0.007 [+ or -] 0.0003 g; density = 50 [m.sup.-3]) to each mesocosm on 6 Jun. 2003. In addition, given the very large egg masses and numbers of tadpoles produced by L. catesbeianus, we included a higher density of these tadpoles than the other tadpoles.

We used a 3 x 2 x 2 fully factorial experimental design (replicated three times) that included three anuran tadpole assemblage composition treatments (Hyla versicolor only, Anaxyrus americanus only, both H. versicolor and A. americanus) at two densities [low = total of 18 tadpoles (density = 22.5 [m.sup.-3]); high = total of 36 tadpoles (density = 45 [m.sup.-3])], with two nutrient treatments (no enrichment vs. enrichment). For treatments with both species of tadpoles we introduced an equal number of each species. Because the primary intent of this experiment was to examine interactions between the species of tadpoles (Smith and Burgett, 2012), there was no "control" treatment that lacked all tadpoles. However, this particular design does allow us to examine how changes in the density and composition of a tadpole assemblage may affect snail abundance. We added tadpoles of A. americanus (mean mass = 0.008 [+ or -] 0.0004 g) and H. versicolor (mean mass = 0.010 [+ or -] 0.001 g) to mesocosms on 23 May 2003. We added 15 snails to each mesocosm on 27 May 2003 (density = 19 [m.sup.-3]). Tadpole and snail densities in local ponds ranged from 26-176.4 [m.sup.-3] for hylids, 0.38-58.4 [m.sup.-3] for bufonids, 0.46-57.5 [m.sup.-3] for ranids, and 58.8-468.9 [m.sup.-3] for snails (Smith et al., 2003a, b). To enriched mesocosms we added nutrients (8 mg [L.sup-1] N[O.sub.3] and 2 mg [L.sup.-1] P[O.sub.4]) every 14 d starting on 2 Jun. 2003 to simulate periodic run-off events. These concentrations are 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 metamorphs and tadpoles of Hyla versicolor (not all had metamorphosed by the time the experiment was terminated) from each mesocosm. All snails were generally similar in size at the end of the experiment, and thus we did not weigh them and instead used abundance of snails in our analyses. For A. americanus, we allowed metamorphosis to occur, removing metamorphs daily when both forelimbs had emerged (Gosner Stage 42). We housed the metamorphs in the laboratory in plastic containers with access to water but not food until the tail was resorbed, and then weighed them. The number of days to metamorphosis was counted from the starting date of the experiment to the day when the mil was fully resorbed. For H. versicolor, we allowed tadpoles to undergo metamorphosis and treated the metamorphs in the same way as for A. americanus. However, not all of the H. versicolor tadpoles had metamorphosed by the time the experiment was terminated. We thus removed all surviving Gray Treefrog tadpoles and counted them (for inclusion in survivorship estimates and proportion metamorphosing but not in the mass analysis). After draining the mesocosms, we scraped the periphyton from a specific area (15.5 cm x 22.8 cm) on the south-facing interior wall of each mesocosm. Since the area scraped was from the same area on all mesocosms, they all received the same amount of incident sunlight throughout the experiment. We then allowed the periphyton to air dry at room temperature until constant mass was achieved, and we used this final periphyton dry mass as our estimate of periphyton productivity.

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

RESULTS

There was a significant, complex three-way interaction that influenced the number of Physella sp. in the mesocosms at the end of the experiment (3-way interaction; Fig. 1; [F.sub.2,23] = 3.78, P = 0.038). At low density, there was little difference in snail abundance among the assemblage composition and nutrient enrichment treatments. However, at high density, the mixed assemblage composition with nutrient enrichment had significantly more Physella sp. than the other treatments. There was also a significant assemblage composition effect with higher snail abundance in the mixed assemblage composition treatment ([F.sub.2,23] = 4.28, P = 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 = 23, [r.sup.2] = 0.007, P = 0.69). There was a significant negative relationship between the mean days to metamorphosis and the abundance of Physella sp. such that earlier metamorphosis by A. americanus was associated with greater abundances of Physella sp. [Fig. 2B; N = 23, [r.sup.2] = 0.21, P = 0.030; mean days to metamorphosis = 32.11-0.0013 (Physella)]. There was no relationship between the number of Physella sp. and mean A. americanus metamorph mass (Fig. 2C; N = 23, [r.sup.2] = 0.06, P = 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 = 23, [r.sup.2] = 0.18, P = 0.043; survivorship = 0.52 + 0.00017(Physella)]. The proportion of H. versicolor that metamorphosed was positively related to the number of Physella sp. [Fig. 3B; N = 22, [r.sup.2] = 0.35, P = 0.0038; proportion metamorphosing = 0587 + 0.00024(Physella)]. The mean number of days to metamorphosis for H. versicolor was negatively related to the number of Physella sp. at the end of the experiment [Fig. 3C; N = 21, [r.sup.2] = 0.27, P = 0.016; mean days to metamorphosis = 45.57-0.0031 (Physella)]. The mean mass of H. versicolor metamorphs was not related to the number of Physella sp. at the end of the experiment (Fig. 3D; N = 20, [r.sup.2] = 0.15, P = 0.089).

[FIGURE 1 OMITTED]

High density mesocosms (regardless of tadpole assemblage composition or enrichment treatment) had lower periphyton dry mass than low density mesocosms [low density: 0.638 [+ or -] 0.123 g (N = 18), high density: 0.354 [+ or -] 0.096 g (N = 17); [F.sub.1,23] = 5.42, P < 0.0001]. Periphyton dry mass at the end of the experiment was lower in enrichment than no enrichment treatments [control: 0.794 [+ or -] 0.104 g (N = 18), enriched: 0.189 [+ or -] 0.068 (N = 17); [F.sub.1,23] = 22.4, P < 0.0001]. No other factor of interaction term was significant (see Fig. 4).

DISCUSSION

Differences in the tadpole assemblages, both in terms of tadpole density and the composition of the tadpole assemblage, in our experimental mesocosms interacted with nutrient enrichment to affect snail (Physella sp.) abundance. This significant interaction primarily reflects the very high mean abundance of snails in the high density, nutrient addition treatments with tadpoles of both Anaxyrus americanus and Hyla versicolor. The patterns of snail abundance to some extent parallels the observed mean periphyton dry mass at the end of the experiment (see Fig. 4). Although the interaction was not statistically significant and the peak is not very high in the periphyton dry mass, the similarity between the 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 would have predicted. Our results suggest further research on this question is warranted, especially explorations 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 the experiment and the mean number of days to metamorphosis in Anaxyrus americanus may suggest that increasing numbers of Physella sp. may have somehow accelerated the development of A. americanus tadpoles. We also found no effect of Physella abundance at the end of the experiment on A. americanus survivorship and metamorph mass. Our results contrast 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 Physella snails. However, the densities used in our experiment were lower than those used in Holomuzki and Hemphill (1996). It may be that the direction of the effects of Physella snails on A. americanus tadpole development may be dependent on the density of snails and/or tadpoles.

[FIGURE 2 OMITTED]

[FIGURE 3 OMITTED]

We also observed positive relationships between snail abundance and the proportion of Hyla versicolor tadpoles that metamorphosed and their survivorship, and a negative relationship 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 positively reacting to the same conditions. Because Hyla and Anaxyrus tadpoles likely use the periphyton resource differently (e.g., bufonids tend to have higher consumption rates and assimilation rates than hylids, Richardson, 2002; Anaxyrus uses benthic algae more than Hyla, and Hyla use algae in the water column more than Anaxyrus, Beiswinger, 1977; Wilbur and Alford, 1985), they may have different effects on snails. For example, Hyla may regenerate or relocate nutrients to the ecosystem differently than Anaxyrus (e.g., Hyla may relocate nutrients from the open water column to the benthos) and thus have a positive effect 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 mechanism inducing the contrasting relationships between snail abundance and A. americanus and H. versicolor tadpoles; however, our results do suggest further examination of these potential relationships would be interesting.

[FIGURE 4 OMITTED]

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

In conclusion, our results suggest that changes in tadpole assemblages in association with other environmental alterations can have effects on diverse components of the broader community, including snails. Such effects are potentially important because changes in amphibian 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 in distributions of timing of breeding due to habitat changes or climate change, could induce greater impacts on the broader aquatic community and ecosystem. For example, anuran tadpoles reduce primary productivity and inorganic sediments in tropical streams (Connelly et 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 the productivity of shredders in tropical streams (Colon-Gaud et al., 2009, 2010), and increase 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 Howard Hughes Medical Institute, and an Amphibian Research and Monitoring Initiative/Declining Amphibian Populations 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 earlier version of this manuscript.

SUBMITTED 22 JULY 2011

ACCEPTED 10 FEBRUARY 2012

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GEOFFREY R. SMITH, (1) AMBER A. BURGETT (2), AND JESSICA E. RETTIG

Department of Biology, Denison University, Granville, Ohio 43023

(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
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