Diet Composition and Overlap between Recently Metamorphosed

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Diet Composition and Overlap between Recently Metamorphosed Rana areolata and Rana sphenocephala: Implications for a Frog of Conservation Concern John A. Crawford1, Donald B. Shepard2, and Christopher A. Conner3 Interspecific competition for resources is predicted to be high in dense populations of closely related species and should lead either to species partitioning resources along one or more niche axes, or exclusion of the competitively inferior species. Between 19 June and 19 July 2003, we collected 71 recently metamorphosed Rana areolata (Crawfish Frogs) and 69 recently metamorphosed R. sphenocephala (Southern Leopard Frogs) from a single pond in northeastern Oklahoma and compared their morphology and diet. We found that recently metamorphosed R. areolata and R. sphenocephala are morphologically similar. Further, diets of both species were similar: hemipterans predominated, prey items were similarly sized, and dietary niche breadths overlapped, but R. areolata had significantly lower volumes of prey in their stomachs. Because of the high risk of desiccation, especially in Great Plains populations, newly metamorphosed Rana are not expected to disperse far from their natal ponds. During this first season, Rana also experience rapid growth. Dietary restrictions directly influence growth rate, which in turn are known to have major consequences during later life stages, ultimately affecting fitness. Rana areolata is a species of conservation concern across its range. Competitive interactions with other species of Rana have been proposed to be contributing to declines in R. areolata. Our results indicate that competitive interactions with R. sphenocephala have the potential to negatively affect prey consumption, and ultimately fitness, in R. areolata.

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NTERSPECIFIC competition frequently results in species segregating along one or more niche axes or exclusion of the competitively inferior species (Pianka, 1994). The life history of many anuran species involves large numbers of individuals during early life stages and multiple species often breed synchronously in the same habitats (Duellman and Trueb, 1986). Many studies have examined interspecific food resource competition in frog tadpoles (Wilbur, 1982; Bardsley and Beebee, 2001; Smith et al., 2004) and dietary segregation within assemblages of adult anurans (Toft, 1980; Lima and Magnusson, 1998; Caldwell and Vitt, 1999; Parmelee, 1999), but few have focused on dietary overlap among recently metamorphosed frogs of different species (Werner et al., 1995). For species that breed in lentic habitats, large masses of recently metamorphosed frogs often disperse synchronously from their natal pond into adjacent terrestrial habitat (Semlitsch et al., 1996). When metamorphosis of syntopic species coincides, recently metamorphosed frogs of multiple species can co-occur at high densities (Semlitsch et al., 1996). Under such dense conditions and because of their similar small size, and thus similar gape limitations, recently metamorphosed individuals of different species may compete for prey. Further, competition is expected to be highest among closely related species because they usually have similar morphologies and diets (Toft, 1985). Rana sphenocephala (Southern Leopard Frogs) are one of the most common aquatic frogs throughout the southeastern and south-central United States (Butterfield et al., 2005). Rana areolata (Crawfish Frogs) also occur in the southcentral United States and their distribution is entirely overlapped by that of R. sphenocephala (Lannoo, 2005). Both species often breed synchronously in the same habitats, but 1

R. areolata appear to have declined in many parts of their range, which has resulted in some level of conservation status in several states (Redmer, 2000; Parris and Redmer, 2005). Competitive interactions with other species of Rana have been proposed to be contributing to the decline of R. areolata (Parris and Redmer, 2005), but supporting evidence is limited. Interspecific competition for resources among tadpoles has been shown to negatively impact R. areolata (Parris and Semlitsch, 1998), but the extent to which R. areolata interact with other Rana in the terrestrial habitat, where the majority of their lives are spent, is unknown. Because of high risk of desiccation, especially in Great Plains populations, individuals of species that metamorphose during summer months are not expected to disperse far from their natal ponds until the following year (Semlitsch, 2008). Thus, conditions in which recently metamorphosed individuals of different species co-occur in dense numbers are likely to last the remainder of their first season. During this first season, most anurans in temperate regions experience rapid growth (Duellman and Trueb, 1986). Diet during early life stages will directly influence growth rate, and early growth rate trajectories can have major consequences for adults that ultimately affect fitness (Madsen and Shine, 2000; Leary et al., 2005). Due to similarities in size at and timing of metamorphosis in R. areolata and R. sphenocephala, the potential for competitive interactions in the terrestrial habitat should be highest during the post-metamorphic period. Here we examine the diets of syntopic, recently metamorphosed R. areolata and R. sphenocephala, calculate dietary niche breadths for each species, and determine the degree of dietary overlap. We also examine morphological differences and test whether species differ in mean prey size and total

Division of Biological Sciences, University of Missouri, 105 Tucker Hall, Columbia, Missouri 65211. Present address: School of Medicine–TH, Indiana University, 135 Holmstedt Hall, Terre Haute, Indiana 47809; E-mail: [email protected]. Send reprint requests to this address. 2 Sam Noble Oklahoma Museum of Natural History and Department of Zoology, University of Oklahoma, 2401 Chautauqua Avenue, Norman, Oklahoma 73072; E-mail: [email protected]. 3 Division of Biological Sciences, University of Missouri, 105 Tucker Hall, Columbia, Missouri 65211; E-mail: [email protected]. Submitted: 30 July 2008. Accepted: 7 May 2009. Associate Editor: M. J. Lannoo. DOI: 10.1643/CH-08-125 F 2009 by the American Society of Ichthyologists and Herpetologists

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prey volume. If R. areolata and R. sphenocephala compete for prey items, then we should observe significant dietary segregation (diet composition or prey size) or indication that prey consumption in one species was negatively affected by the other species (i.e., reduced total prey volume). MATERIALS AND METHODS Between 19 June and 19 July 2003, we collected 71 recently metamorphosed Rana areolata and 69 recently metamorphosed R. sphenocephala from the Camp Gruber Joint Maneuver Training Center, Muskogee County, Oklahoma (35u459N, 95u099W). All individuals were collected from a 2.25-ha area around a pond from which they were dispersing. To capture frogs, we constructed and installed 20 Y-shaped drift fence arrays in the habitat around their natal pond (fences ranged 50–600 m from the pond edge). Each array consisted of a central pitfall trap (approx. 19-L bucket) and three 10-m black plastic fences radiating outward with a wire-mesh funnel trap on each side of the end of each fence. We checked traps at least once daily and always in the morning (between 0800 and 1000 h), which was the only time of day frogs were encountered. Frogs were never found in traps during evening checks. Frogs were transported back to our field laboratory and euthanized within 2–4 h of capture. We gave each frog a uniquely numbered tag, removed the stomach, and placed it in 95% ethanol in an individually labeled plastic tube. We preserved frogs in 10% formalin and subsequently transferred them to 70% ethanol for storage. All specimens were deposited in the Sam Noble Oklahoma Museum of Natural History at the University of Oklahoma, Norman, Oklahoma, USA (OMNH 39630–39700, 39713, 39716–39748, 39751–39785). For each frog stomach, we counted, identified, and measured the maximum length and width of each prey item. Prey items were identified to order or family when possible. We estimated the volume of intact prey items using the formula for a prolate spheroid,

 4 length width 2 V~ p 3 2 2 in the program BugRun, which is a 4th DimensionH-based analysis that produces dietary summaries including numeric and volumetric percentages for pooled stomachs, calculates mean prey size (length, width, and volume) for each frog, estimates stomach volume based on total prey volume, and calculates niche breadth using the inverse of Simpson’s (1949) diversity measure (Pianka, 1973, 1986), b~

1 , n P p2i

i~1

where p is the proportional utilization of each prey type i and n is the total number of prey categories. Niche breadth values (b) vary from 1 (exclusive use of a single prey type) to n (even use of all prey). We also calculated the percentage of occurrence (%Freq) of each prey type (number of stomachs containing prey type i divided by the total number of stomachs with prey). To determine the relative contribution of each prey type, we calculated an Importance Index using the equation I~

%nz%Volz%Freq , 3

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where %N is the numeric percentage, %Vol is the volumetric percentage, and %Freq is the percentage of occurrence. We calculated dietary overlap between R. areolata and R. sphenocephala using Importance Index values and Pianka’s overlap index (Pianka, 1973), which varies from 0 (no overlap) to 1 (complete overlap). To investigate the presence of non-random patterns in dietary niche overlap, we used the Niche Overlap Module of EcoSim (Gotelli and Entsminger, 2003). Data for such analysis consist of a matrix in which each species is a row, each diet category is a column, and the cells, in our case, were the Importance Index values. The matrix is reshuffled to produce random patterns that would be expected in the absence of underlying structure. Based on simulations, an expected mean under the null hypothesis of no structure is calculated and compared to the observed overlap. A P-value # 0.05 indicates that the observed overlap is less than would be expected from random and suggests niche segregation. A P-value . 0.05 simply indicates a failure to reject the null hypothesis. We performed 1000 randomizations under the following options in EcoSim: ‘‘Pianka’s niche overlap index,’’ ‘‘randomization algorithm two,’’ ‘‘retained zero states,’’ and ‘‘relaxed niche breadth.’’ For each individual with identifiable prey in the stomach, we measured (after preservation) the frog’s snout–vent length (SVL), head width, head length, and head height (60.01 mm) using digital calipers. To test for differences in head dimensions between R. areolata and R. sphenocephala, we conducted a MANCOVA with species as the class, head width, head length, and head height as dependent variables, and SVL as the covariate. We tested if mean prey size (volume) and total prey volume of individual frogs were related to frog SVL and whether they differed between species using ANCOVA with species as the class variable, prey size or total prey volume as dependent variables, and SVL as the covariate. We tested for class by covariate interactions, but removed them from the final models if they were not significant. All morphological and prey size variables were loge-transformed prior to analyses to meet assumptions of normality. Means are presented throughout as 6SD. RESULTS A total of 127 prey items representing 13 prey categories were recovered from 53 Rana areolata, and a total of 143 prey items representing 13 prey categories were recovered from 62 R. sphenocephala (Table 1). A significantly higher number of R. areolata had empty stomachs (n 5 18) than R. sphenocephala (n 5 7; x2 5 4.84, df 5 1, P 5 0.03). Numerically, the diet of R. areolata was dominated by hemipterans, collembolans, and beetles, and the diet of R. sphenocephala was dominated by hemipterans, spiders, and beetles (Table 1). Volumetrically, the diet of R. areolata was dominated by hemipterans, and the diet of R. sphenocephala was dominated by spiders and hemipterans (Table 1). Based on the Importance Index, hemipterans and beetles were the most important prey items for R. areolata, whereas hemipterans and spiders were the most important prey items for R. sphenocephala (Table 1). Niche breadths for volumetric data were similar for the two species (Table 1). The observed niche overlap using Importance Indices was 0.844 and was not significantly less than the mean expected overlap (0.468) generated from simulations (P . 0.99), thus indicating a lack of niche segregation.

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Table 1. Diet Summary for Recently Metamorphosed Rana areolata (n 5 53) and R. sphenocephala (n 5 62). n is the total number of items of that prey category, Vol is total prey volume (mm3) of that prey category, Freq is the number of stomachs that contained that prey category, and I is the Importance Index, which is the average of %n, %Vol, and %Freq.

R. areolata Prey type Ants Beetles Caterpillars Cockroaches Collembollans Diplurans Dipterans Earwigs Gastropods Hemipterans Bees/wasps Isopods Mayflies Nematodes Odonates Orthopterans Spiders Unknown SUMS Niche breadths

n 3 18 1 2 40 0 0 2 2 46 1 0 0 1 2 2 7 0 127 —

%n

Vol

%Vol

2.36 18.45 0.39 14.17 439.95 9.25 0.79 314.16 6.61 1.57 584.33 12.29 31.50 5.24 0.11 0.00 0.00 0.00 0.00 0.00 0.00 1.57 79.07 1.66 1.57 10.47 0.22 36.22 2013.74 42.36 0.79 108.91 2.29 0.00 0.00 0.00 0.00 0.00 0.00 0.79 10.47 0.22 1.57 366.00 7.70 1.57 251.32 5.29 5.51 551.88 11.61 0.00 0.00 0.00 — 4753.99 — 3.91 — 4.34

R. sphenocephala Freq %Freq 3 15 1 2 1 0 0 2 2 34 1 0 0 1 2 2 6 0 — —

5.66 2.80 28.30 17.24 1.89 3.10 3.77 5.88 1.89 11.17 0.00 0.00 0.00 0.00 3.77 2.33 3.77 1.85 64.15 47.58 1.89 1.66 0.00 0.00 0.00 0.00 1.89 0.97 3.77 4.35 3.77 3.54 11.32 9.48 0.00 0.00 — — — —

Mean SVL of recently metamorphosed R. areolata and R. sphenocephala did not significantly differ (F1,112 5 0.001, P 5 0.98; Table 2). Head width (F1,110 5 6.31, P 5 0.01), head length (F1,110 5 4.40, P 5 0.04), and head height (F1,110 5 9.89, P 5 0.002) all increased at a faster rate with respect to SVL (i.e., a significant class by covariate interaction) in R. areolata than in R. sphenocephala. Individual prey items averaged 5.24 6 4.40 mm in length, 2.43 6 1.58 mm in width, and 37.43 6 57.02 mm3 in volume for R. areolata (n 5 127). For R. sphenocephala, individual prey items averaged 8.34 6 3.95 mm in length, 3.05 6 1.67 mm in width, and 62.5 6 91.36 mm3 in volume (n 5 143). Mean prey size (volume) for individual frogs was related to SVL (F1,111 5 5.09, P 5 0.03) and did not significantly differ between species (F1,111 5 1.91, P 5 0.17; Table 2). Total prey volume for individual frogs was also significantly related to SVL (F1,111 5 5.75, P 5 0.02) and was significantly higher in R. sphenocephala (F1,111 5 5.04, P 5 0.03; Table 2).

Table 2. Means (6SD) of Morphological Variables, Prey Size, and Total Prey Volume for Recently Metamorphosed Rana areolata and R. sphenocephala Containing Prey.

R. areolata n Snout–vent length (mm) Head width (mm) Head length (mm) Head height (mm) Mean prey size (mm3) Mean total prey volume (mm3)

31.01 10.35 11.91 5.73 51.88

53 6 1.90 6 0.80 6 0.81 6 0.42 6 37.43

89.70 6 94.01

R. sphenocephala 31.16 10.37 12.01 5.77 75.80

I

62 6 3.48 6 1.06 6 1.25 6 0.51 6 86.04

146.05 6 158.44

n

%n

6 21 0 0 0 1 9 4 1 44 0 7 15 0 7 5 22 1 143 —

4.20 14.69 0.00 0.00 0.00 0.70 6.29 2.80 0.70 30.77 0.00 4.90 10.49 0.00 4.90 3.50 15.38 0.70 — 6.11

Vol

%Vol

134.82 1.51 382.49 4.28 0.00 0.00 0.00 0.00 0.00 0.00 6.28 0.07 453.36 5.07 293.34 3.28 4.19 0.05 2067.15 23.13 0.00 0.00 407.76 4.56 422.02 4.72 0.00 0.00 530.94 5.94 881.87 9.87 3324.86 37.20 28.27 0.32 8937.35 — — 4.65

Freq %Freq 4 14 0 0 0 1 7 4 1 31 0 7 5 0 7 5 17 1 — —

I

6.45 4.05 22.58 13.85 0.00 0.00 0.00 0.00 0.00 0.00 1.61 0.79 11.29 7.55 6.45 4.18 1.61 0.79 50.00 34.63 0.00 0.00 11.29 6.92 8.06 7.76 0.00 0.00 11.29 7.38 8.06 7.14 27.42 26.67 1.61 0.88 — — — —

DISCUSSION Interspecific competition for resources should be high in dense populations of closely related species with similar morphologies and is predicted to lead to species partitioning resources along one or more niche axes or exclusion of the competitively inferior species (Jaeger, 1972, 1980; Toft, 1985; Griffis and Jaeger, 1998). In our study, supporting evidence for interspecific competition would therefore consist of either dietary segregation or a result suggesting that one species has a negative effect on prey consumption in the other species. We found that recently metamorphosed Rana areolata and R. sphenocephala overlapped greatly in diet and exhibited no segregation. However, we found that R. areolata had a significantly lower total volume of prey in their stomachs and a higher number of empty stomachs compared to R. sphenocephala. Because both species of frogs were of similar size and ate similar prey types and sizes, the latter results suggest that the amount of prey consumed by recently metamorphosed R. areolata was negatively affected by the presence of R. sphenocephala. This effect could be an artifact of using individuals sampled from pitfall traps, if, for example, R. sphenocephala continued to eat in the traps while R. areolata ceased foraging, or R. areolata consumed more soft-bodied prey (e.g., earthworms) that were digested faster than hard-bodied prey. However, these scenarios seem unlikely given that frogs in our study were in pitfall traps for at most 12 hours, and prior studies have shown that individuals in pitfall traps checked every day do not significantly differ from conspecifics collected outside of traps in diet composition or volume of prey consumed (Costa et al., 2008). Whether consuming less food following metamorphosis has long-term fitness consequences for R. areolata that could negatively impact populations is unclear. Post-metamorphic dispersal where species are co-occurring at high densities

Crawford et al.—Ranid dietary overlap

likely lasts for at least the first year (Semlitsch, 2008) and may be long enough to have prolonged effects considering this is the period of most rapid growth for anurans (Duellman and Trueb, 1986; Leary et al., 2005). Reduced prey consumption in R. areolata could also be due to some unknown intrinsic or extrinsic factor. For example, predation is typically high on recently metamorphosed frogs (Arnold and Wassersug, 1978), and individuals may decrease foraging activity in response to predators. It is possible that R. areolata have a stronger response to predators which decreases foraging activity, and thus total volume of prey in their stomachs, independent of whether other species of Rana are present. Comparison of our stomach volumes with populations of R. areolata where R. sphenocephala are absent could provide additional insight; however, due to complete range overlap with R. sphenocephala, and synchronous breeding in the same habitats, such a situation would be difficult to find. It seems unlikely that small insect prey would be a limited resource given their high abundance in most natural habitats. Whether species segregate along some other niche axis during post-metamorphic dispersal is also unknown. Hofer et al. (2004) found that ecologically similar species of amphibians co-occurred more often than expected by chance, which was attributed to shared resource requirements associated with reproduction. The constraint of needing access to suitable breeding sites likely outweighs any negative effects of competitive interactions that would otherwise be avoided through resource partitioning. Because of their similar small size, recently metamorphosed frogs of different species may have similar diets because gape limitations restrict them to certain prey types. We found that mean SVL of recently metamorphosed R. areolata and R. sphenocephala did not significantly differ and that they ate similar types of prey. Similarly, Werner et al. (1995) found high dietary overlap in recently metamorphosed R. catesbeiana (Bullfrogs) and R. clamitans (Green Frogs), and that the potential for competitive interactions over food decreased as the disparity between size classes increased. In the narrow range of body sizes examined in our study, we found no difference in mean prey size between R. areolata and R. sphenocephala. However, we found that head morphological variables (length, width, and height) all increased at a faster rate relative to SVL in R. areolata than in R. sphenocephala. This difference in allometric growth would translate to larger gape size in R. areolata as they grow and allow them to ingest a larger range of prey sizes and types, which may decrease dietary overlap with R. sphenocephala over time. Ultimately, the potential for competitive interactions will be lessened because of the habitat differences exhibited by adult R. areolata and R. sphenocephala (Butterfield et al., 2005; Parris and Redmer, 2005). Post-metamorphic size of R. areolata is similar to the size of other Rana with which they co-occur, such as R. sphenocephala, R. blairi (Plains Leopard Frogs), and R. clamitans (Butterfield et al., 2005; Crawford et al., 2005; Parris and Redmer, 2005; Pauley and Lannoo, 2005; this study). Because these species are similarly sized, closely related, and use common breeding sites, it is possible that they all overlap significantly in diet, at least during early life stages (larvae and recently metamorphosed individuals). Whether competitive interactions with other Rana are contributing to the decline of R. areolata remains unclear. Although R. areolata may or may not be limited by a single strong competitor, the collective impact of several weak

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competitors (an effect known as diffuse competition) might have negative consequences on populations (Morin, 1999). To fully understand the impacts of competitive interactions of R. sphenocephala (and other Rana) on R. areolata studies such as this one should be replicated across the range of R. areolata. Ultimately, any negative effects of interspecific competition on R. areolata are compounded by other, more important, factors. For example, habitat loss and alteration not only directly impact populations, but they can also significantly decrease the abundance and change the composition of available invertebrate prey (Schowalter et al., 2003; Wightman and Germaine, 2006). The spread of R. catesbeiana, which has been shown to have detrimental effects on other ranid species (Hammerson, 1982; Hecnar and M’Closkey, 1997; Pearl et al., 2004), may also negatively impact populations of R. areolata. For species of conservation concern, such as R. areolata, it is vital to undertake studies of the synergistic mechanisms that regulate population sizes in order to conserve populations faced with multiple threats. ACKNOWLEDGMENTS We thank J. Caldwell, J. Porter, and L. Vitt for assistance installing the drift fence arrays, J. Caldwell and L. Vitt for field assistance and the use of their 1977 Winnebago, J. Caldwell, M. Lannoo, L. Vitt, and the OU ZEEB journal club for commenting on an earlier version of the manuscript, and Sgt. T. Lawrence and staff at Camp Gruber Range Control for logistical assistance. JAC acknowledges partial support from a GAANN fellowship through the University of Missouri. This research was conducted during a concurrent project supported by a contract from the U.S. Army to G. Schnell, N. McCarty, W. Shelton, J. Caldwell, and L. Vitt. All work was performed under Scientific Permit #3403 from the Oklahoma Department of Wildlife Conservation to DBS and University of Oklahoma Animal Care and Use Committee protocol #R04-016. LITERATURE CITED Arnold, S. J., and R. J. Wassersug. 1978. Differential predation on metamorphic anurans by garter snakes (Thamnophis): social behavior as a possible defense. Ecology 59:1014–1022. Bardsley, L., and T. J. C. Beebee. 2001. Strength and mechanisms of competition between common and endangered anurans. Ecological Applications 11:453–463. Butterfield, B. P., M. J. Lannoo, and P. Nanjappa. 2005. Southern leopard frog (Rana sphenocephala), p. 586–587. In: Amphibian Declines: The Conservation Status of United States Species. M. J. Lannoo (ed.). University of California Press, Berkeley. Caldwell, J. P., and L. J. Vitt. 1999. Dietary asymmetry in leaf litter frogs and lizards in a transitional northern Amazonian rain forest. Oikos 84:383–397. Costa, G. C., D. O. Mesquita, and G. R. Colli. 2008. The effect of pitfall trapping on lizard diets. Herpetological Journal 18:45–48. Crawford, J. A., L. E. Brown, and C. W. Painter. 2005. Plains leopard frog (Rana blairi), p. 532–534. In: Amphibian Declines: The Conservation Status of United States Species. M. J. Lannoo (ed.). University of California Press, Berkeley.

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