Zoo Biology 9999 : 1–6 (2014)

RESEARCH REVIEW

Tadpole Nutritional Ecology and Digestive Physiology: Implications For Captive Rearing of Larval Anurans Gregory S. Pryor* Francis Marion University, Florence, South Carolina The adaptive tadpole stage allows anurans to exploit food resources in two vastly different environments, and the transition from aquatic larvae to terrestrial carnivores is both dramatic and complex. As seen in many other members of the freshwater aquatic community, the nutritional requirements and characteristic feeding strategies of anuran larvae (tadpoles) are extremely diverse, ranging from herbivory to carnivory and including predation and cannibalism, oophagy, coprophagy, filter‐feeding, and hindgut microbial fermentation. Whereas tadpoles as a group are commonly considered herbivorous or omnivorous, many are specialists; understanding species‐specific dietary habits is critical for captive rearing projects in zoos and amphibian habitat conservation efforts. Practical applications of this review also encompass studies of amphibian declines, herpetoculture, ecology and evolution, and comparative gastrointestinal morphology and physiology. Zoo Biol. XX: © 2014 Wiley Periodicals, Inc. 1–6, 2014.

Keywords: anuran larvae; dietary habits; feeding strategies; amphibian declines; captive breeding

INTRODUCTION Understanding anuran larvae (tadpole) nutrition and digestion is critical for successful anuran captive rearing programs, yet for most species, very little is known about the nutrient requirements for optimal growth, metamorphosis, and survival of larvae. Unfortunately, the vast majority of frog species have never been bred or raised in captivity, and knowledge of rearing their tadpoles is entirely lacking. Given the widespread and ongoing declines in amphibian populations, there is indeed a dire “sense of urgency” in these regards [Altig et al., 2007], particularly when dealing with threatened and endangered tropical species. The main focus of this review will be a summary of known dietary strategies, nutritional ecology, and digestive physiology of tadpoles. Synopses of published captive rearing experiments and husbandry programs will also be provided. For certain species of anuran larvae (tadpoles), characteristic dietary strategies such as herbivory, cannibalism, predation, oophagy, and filter‐feeding have been reported based on observations of foraging behavior and gut contents [reviewed in McDiarmid and Altig, 1999; Altig et al., 2007]. Tadpoles also have been loosely classified into feeding guilds based on oral and body morphology [Orton, 1953;

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Starrett, 1973; Inger, 1986; Altig and Johnston, 1989]. Although such “ecomorphological guilds” of tadpoles have been described [Table 1 and McDiarmid and Altig, 1999], their nutritional ecology—that is, the contributions and significance of ingested food items to the nutrient requirements of tadpoles —remains generally uninvestigated and poorly understood. The basic anatomical characteristics of the gastrointestinal tracts of some common species of tadpoles also have been described [Hourdry et al., 1996; reviewed in Viertel and Richter, 1999], but most attention on tadpole digestive physiology has been focused on oral morphology. Gut morphology varies among and within species [e.g., herbivores have longer intestines than carnivores, and gut length and mass increases within a species when more plant matter is  Correspondence to: Gregory S. Pryor, Francis Marion University, Florence, SC 29502‐0547. E‐mail: [email protected]

Received 06 January 2014; Accepted 11 June 2014

DOI: 10.1002/zoo.21152 Published online XX Month Year in Wiley Online Library (wileyonlinelibrary.com).

2 Pryor TABLE 1. Familial summary of feeding strategies and ecomorphology of anuran larvae Familya

General tadpole feeding strategy

Ecomorphological guild

Arthroleptidae

Exotrophic or endotrophic

Ascaphidae Brachycephalidae Bufonidae

Exotrophic Endotrophic Exotrophic or endotrophic

Centrolenidae Dendrobatidae

Exotrophic Exotrophic or endotrophic

Discoglossidae Heleophrynidae Hemisotidae Hylidae

Exotrophic Exotrophic Exotrophic Exotrophic or endotrophic

Hyperoliidae

Exotrophic

Leiopelmatidae Leptodactylidae

Endotrophic Exotrophic or endotrophic

Megophryidae Microhylidae Myobatrachidae

Exotrophic or endotrophic Exotrophic or endotrophic Exotrophic or endotrophic

Pelobatidae Pelodytidae Pipidae Pseudidae Ranidae

Exotrophic Exotrophic Exotrophic or endotrophic Exotrophic Exotrophic or endotrophic

Rhacophoridae

Exotrophic or endotrophic

Rhinodermatidae Rhinophrynidae Sooglossidae

Endotrophic Exotrophic Endotrophic

Lotic: neustonic, suctorial Lentic: benthic Lotic: suctorial n/a Lotic: benthic, suctorial Lentic: benthic Lotic: burrower Lotic: benthic, neustonic Lentic: benthic Lentic: benthic Lotic: suctorial Lentic: nektonic Lotic: wide variety Lentic: wide variety Lotic: benthic Lentic: benthic, nektonic n/a Lotic: wide variety Lentic: wide variety Lotic: neustonic, benthic Lentic: suspension Lotic: benthic Lentic: benthic, nektonic, carnivorous Lentic: benthic, carnivorous Lentic: benthic Lentic: suspension, carnivorous Lentic: benthic, nektonic Lotic: wide variety Lentic: wide variety Lotic: benthic, suctorial Lentic: benthic, nektonic n/a Lentic: suspension n/a

Feeding strategies divided into exotrophic (non‐egg food consumption) and endotrophic (parental egg or egg yolk consumption). Ecomorphological guild terminology includes lotic (rapid freshwater) and lentic (still freshwater) habitats, and benthic (bottom‐feeding), neustonic (feeding on microbes at surface layer of water), nektonic (feeding on free swimming aquatic organisms), suctorial (sucking and/or adherent feeding), suspension (filter‐feeding), and oophagous (feeding on anuran egg or egg yolk) habits. Table based on abridged data from McDiarmid and Altig [1999]. a Family Allophrynidae not included in table because tadpoles have not yet been described.

included in the diet; Altig and Kelly, 1974], but in general, the stomach is enlarged and acidic; the midgut is long, narrow, and coiled; and the colon is short and wide. Overall gut lengths of wild‐caught Rana catesbeiana tadpoles can be nearly a meter long, or 20 times the snout‐to‐vent length (G. Pryor, unpub. data). Radical changes in gut length and width occur during metamorphosis, as do digestive enzyme activities and nutrient transport systems [reviewed in Bjorndal, 1997; Viertel and Richter, 1999]. Broad generalizations regarding the nutritional ecology and digestive physiology of the vast majority of tadpole species can be made only tentatively. For example, most tadpoles are considered primarily herbivorous [McDiarmid and Altig, 1999], but several studies have shown that growth, development, and survivorship are improved in these tadpoles when higher‐protein animal material is included in their diets [Li and Lin, 1935; Nagai et al., 1971; Crump, 1990]. Commonly used commercial diets for tadpoles (e.g., Nasco Zoo Biology

Frog Brittle [Nasco, Fort Atkinson, WI 53538] and Zoo Med Aquatic Frog and Tadpole Food [Petco, San Diego, CA 92121]) contain almost 50% animal protein in the form of fish and/or porcine meat meal. Furthermore, “herbivorous” tadpoles will preferentially select diets containing more animal material [Taylor et al., 1995]. Because animal tissue is digested and absorbed more rapidly and thoroughly than refractory plants or algae, the nutritional importance of animal components of wild tadpole diets likely has been underestimated. Much of the uncertainty surrounding tadpole nutritional ecology stems from inherent difficulties in inferring the nutritional importance of ingested food items from the gut or fecal contents of tadpoles. The small sizes of tadpoles and the finely comminuted nature of their ingesta and feces limit even basic descriptions of the apparent digestion of various dietary items. Among the gut contents analyzed from wild tadpoles, microorganisms have been the most readily

Tadpole nutritional ecology and digestive physiology

identified components. Protozoa, blue‐green algae (cyanobacteria), diatoms, filamentous and suspended green algae, microcrustaceans, and bacteria appear to be common food items [Li and Lin, 1935; Savage, 1952; Jenssen, 1967; Nathan and James, 1972; Hendricks, 1973; Test and McCann, 1976; Seale, 1980; Seale and Beckvar, 1980; Altig et al., 2007]. Whereas some authors maintain that these microorganisms are randomly ingested [Farlowe, 1928; Jenssen, 1967; Seale and Beckvar, 1980], others assert that certain microorganisms are fed on selectively by tadpoles [Test and McCann, 1976]. Some of these microbes are apparently digested and assimilated. For example, isotopic analyses of centrolenid tadpoles in Panama suggest that detritus‐associated microbes are more important, nutritionally, than the other benthic materials consumed [Whiles et al., 2006]. In another study of tadpoles in Panamanian streams, biovolumes of diatoms were higher in tadpole exclosures than in control treatments [Ranvestel et al., 2004]. Regardless of whether or not aquatic microbes are digested or pass through the gut intact, the extraordinary filter‐feeding ability of many tadpole species suggests they are well‐suited for microphagy [Kenny, 1969; Wassersug, 1972, 1980; Seale, 1982]. A diversity of endemic microorganisms is found living within the digestive tracts of tadpoles, including aerobic and anaerobic bacteria, ciliates, and nematodes [Li and Lin, 1935; Savage, 1952; Battaglini and Boni, 1967; Nathan and James, 1972; Adamson, 1981; Schorr et al., 1990; Bjorndal, 1997; Pryor and Greiner, 2004; Pryor and Bjorndal, 2005a; Pryor, 2008]. The nutritional and digestive contributions of most of these microbes in tadpoles remain unknown, but some can contribute metabolizable nutrients (e.g., fermentation byproducts) to their tadpole hosts [Pryor and Bjorndal, 2005a]. In these regards, they can be likened to the symbiotic microbes inside many other vertebrate herbivores [reviewed in Stevens and Hume, 1995]. The oxyurid gut nematode Gyrinicola batrachiensis has been shown to play a significant beneficial role in the development and timing of metamorphosis in R. catebeiana tadpoles [Pryor and Bjorndal, 2005a,b] due to nutritional gains; the energetic contributions, in the form of microbial fermentation byproducts, are more than doubled when these nematodes are present. Also reported from the guts of tadpoles are detritus, plant fibers, pollen, a variety of freshwater invertebrates, fungi, viruses, fecal material, and heterospecific and conspecific tadpoles [Costa and Balasubramanian, 1965; Heyer, 1973; Steinwascher, 1978; Sabnis and Kuthe, 1980; Diaz‐ Paniagua, 1985; Inger, 1986; Harrison, 1987; Sekar, 1992; Pryor and Bjorndal, 2005b]. High digestibilities of plant matter by tadpoles have been reported [i.e., mean percent assimilation of organic matter ranged from 54% to 86%: Altig and McDearman, 1975], but the nutritional importance of plants remains uncertain because of methodological problems in this study [reviewed in Bjorndal, 1997; McDiarmid and Altig, 1999]. I have reared hundreds of Southeastern ranid, hylid, and bufonid tadpoles from egg stage to metamorphosis

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using plant‐based rabbit food fed ad libitum (Classic Blend Rabbit Food, L/M Animal Farms, Inc., Pleasant Plain, OH). Furthermore, in the stomach contents of wild‐caught R. catesbeiana tadpoles from Florida, the aquatic plant Najas guadalupensis was often observed intact, but was fragmented and emptied of its cellular contents in the hindgut (G. Pryor pers. obs.). Further research in plant digestion by tadpoles is sorely needed. Several comparative studies of captive tadpoles fed green and blue–green algae clearly indicate that not all algal species are equally digestible and nutritionally valuable [reviewed in Pryor, 2003]. For example, growth rates of R. catesbeiana tadpoles were highest when fed nitrogen‐ fixing Anabaena, presumably due to its high protein content [Pryor, 2003]. Correspondingly, populations of these tadpoles have been associated with major reductions in bloom‐ forming Anabaena [Seale, 1980]. Reinforcing the importance of microbial dietary components, Cladophora algae with attached epiphytic diatoms resulted in better ranid tadpole growth than cleaned Cladophora [Kupferberg et al., 1994; Kupferberg, 1997a]. The bacteria, protozoa, and detritus attached to filamentous algae are likely valuable food sources to tadpoles. The benefit of higher protein diets (i.e., both natural and artificial diets) to tadpoles seems evident. Animal and protozoan dietary components are higher in protein than plant‐based dietary components, and many studies support the link between these high‐protein dietary supplements and better tadpole growth and/or development. For example, Pandian and Marian [1985] showed that tubifex worm‐ supplemented plant‐based diets resulted in shorter larval periods and faster development than unsupplemented plant‐ based diets in R. catesbeiana. Nathan and James [1972] found that dietary supplementation with protozoans decreased time to metamorphosis in Bufo tadpoles. Carnivorous morphs of Scaphiopus tadpoles (S. bombifrons, S. intermontanus, and S. multiplicatus) grow and develop more quickly than omnivorous morphs [Pfennig, 1990]. In field experiments, Kupferberg [1997b] showed ranid tadpole growth is positively correlated with the percentage of dietary protein in their algal diet; the epiphytic diatoms attached to algae that tadpoles feed upon are high in protein because of nitrogen‐ fixing cyanobacterial symbionts, and they result in improved tadpole growth and development over cleaned algae. In fact, epiphyte‐covered Cladophora algae produced as rapid growth as high‐protein commercial reptile food (35% protein) in Rana boylii tadpoles [Kupferberg, 1997b]. Caution is warranted in attributing more rapid tadpole growth exclusively to higher dietary protein levels, because carbohydrates, fats, and energy in general can also be critical determinants of growth. The nutritional significance of detritivory and coprophagy in tadpoles should not be underestimated. Some hylid tadpoles can survive, develop, and metamorphose properly when fed only detritus [Kupferberg et al., 1994]. Conspecific coprophagy was evident in captive R. catesbeiana tadpoles Zoo Biology

4 Pryor observed by Pryor and Bjorndal [2005b], even when other food was available ad libitum. Steinwascher [1978] showed that R. catesbeiana tadpoles grew more slowly when denied access to their feces. In R. pipiens tadpoles, not only was growth slowed by prevention of coprophagy, but feces deposited after reingestion had lower energy content than feces deposited after a single passage through the gut [Gromko et al., 1973]. These studies indicate that herbivorous ranid tadpoles benefit from the increased digestibilities and nutritional gains associated with coprophagy. The nutritional value of pollen to tadpoles remains undetermined, although Wagner [1986] showed selective consumption of conifer pollen by Hyla regilla tadpoles. In preliminary experiments (G. Pryor, unpub. data), I examined over a thousand Pinus pollen grains collected from the midguts of hylid tadpoles in South Carolina and compared them to control pollen samples collected from the same pond. Alexander’s stain was used to discern between viable and unviable/empty pollen grains [Alexander, 1969]. Control samples averaged 86% viability, whereas samples from tadpoles averaged 21% viability. While these data suggest digestion of high‐protein pollen grain contents by tadpoles, further replication among species are needed before substantial conclusions can be made. The endotrophic anurans—those that derive their nutrition from parental eggs—include approximately 1,000 species in 13 families [Table 1 and McDiarmid and Altig, 1999]. Briefly, these anurans exhibit vivipary, ovovivipary, direct development, paravivipory, exovivipary, or nidicolous forms. Because their nutrition during development is entirely based on parental egg sources [mostly vitellogenic yolk: Altig and Johnston, 1989], typical tadpole characteristics, including mouthparts and complete gastrointestinal tracts, are often reduced or absent in this group. CAPTIVE REARING PROGRAMS Tadpole nutrition and digestion has obvious importance in anuran husbandry and captive rearing programs, yet most frog species have never been raised in captivity, and information on how to rear tadpoles is lacking in the peer‐ reviewed literature. Internal reports and anecdotal accounts exist, but can be difficult to obtain. In response to the World Association of Zoos and Aquarium’s plea in 2005 for the development of more ex situ amphibian breeding programs, more facilities have engaged in this endeavor. Perhaps the most comprehensive and up‐to‐date source of husbandry protocols for such ex situ programs can be found online, through Amphibian Ark [Amphibian Ark Progress of Programs, 2013]. A summary of each of the 134 listed programs —of which approximately half have successfully raised tadpoles through metamorphosis—is not feasible here, but a few examples will be discussed. One example of a captive rearing program report is that at the Mountain View Conservation Center and the Greater Vancouver Zoo (report prepared by Gielens [2008]). This

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report describes a 1‐year attempt to raise tadpoles of Rana pretiosa, a critically endangered anuran in Canada. Briefly, more than 3000 eggs were collected from the wild and reared in two Canadian facilities (artificial habitat setup described in detail in the report). Boiled and pureed romaine lettuce was the primary diet provided, although some tanks of tadpoles also received frozen bloodworms as a supplement. The tanks were described as growing “dense with vegetation” [no details of flora provided; Gielens, 2008], which the tadpoles also consumed. Furthermore, dead tadpoles were readily eaten by conspecifics. No data were provided in regards to whether bloodworm‐supplemented tadpoles grew or developed more rapidly than the unsupplemented tadpoles, as would be predicted based on the higher protein content of bloodworms. At the end of one year of captive rearing, approximately 40% of the original eggs had developed into releasable frogs, nonreleasable (small) frogs, or unmetamorphosed tadpoles. An American captive rearing program for R. pretiosa was also described by Abrahamse [2009]. In this report, the protocol for artificial habitat setup and maintenance differed from the Canadian protocol. In particular, more naturalistic environments were provided that included algae, leaf litter, and moss‐ and grass‐covered logs pads (see details in the report). The diet offered was a 50/50 mixture of boiled and pureed kale and romaine lettuce, and powdered high‐protein (60% protein) Spirulina. One‐eighth of a teaspoon of the Spirulina was added to every two tablespoons of thawed kale‐ lettuce puree. Freeze‐dried bloodworms were offered initially, but tadpole affinity for them was low and the bloodworms were subsequently removed from the diet. Unfortunately, no details of growth, development, or survivorship were provided in the report. Regarding tropical anuran species, Omaha’s Henry Doorly Zoo in Nebraska, USA collaborated with Johannesburg Zoo in South Africa to create a captive rearing program and tadpole maintenance facility [Van Der Spuy and Krebs, 2008]. In this study, five non‐threatened anuran species (Amietophrynus gutturalis, Breviceps adspersus, Cacosternum boettgeri, Heleophryne natalensis, and Hyperolius marmoratus) were collected from the wild and brought into captivity for breeding of adults and/or rearing of collected tadpoles at the Johannesburg Zoo Amphibian Conservation Center. Strict hygiene practices were used in the field, and natural habitat parameters were measured for reference. These species were chosen because they had similar habitat requirements as five threatened, endangered, or vulnerable species. Artificial habitats at the center were meticulously recreated and maintained as close to the original habitats as possible. However, no details of diets were provided and no data regarding growth, metamorphosis, or survivorship were presented [see details in Van Der Spuy and Krebs, 2008]. The above examples of captive rearing programs point out a clear need for establishing consistent and detailed reports among institutions. Whereas the abiotic conditions

Tadpole nutritional ecology and digestive physiology

(e.g., temperature, water quality, lighting) of artificial habitats are commonly presented, major shortcomings are evident in descriptions of diets, growth and metamorphosis data, and survivorship of tadpoles. DISCUSSION Knowledge of the nutrition and digestive abilities of tadpoles has potential applications in studies of ecology, evolution, and conservation. For example, because tadpoles typically occur at high densities and have high feed intake, their influence at the ecosystem level can be considerable. A large percentage of the algal biomass in the freshwater ecosystem passes through tadpoles [Seale, 1980, 1982]. Tadpoles have been shown to shift nutrients from aquatic systems into terrestrial systems upon metamorphosis [Seale, 1980], replenish nutrients in some temporary pools [Osborne and McLachlan, 1985], increase primary productivity [Kupferberg, 1997a], and alter species compositions within aquatic habitats [McDiarmid and Altig, 1999]. Despite such major influence within freshwater ecosystems, the mechanisms by which tadpoles process their diets and the nutritional importance of various food items to tadpoles are still largely uninvestigated and remain unknown. Understanding tadpole digestion, especially gastrointestinal fermentation, contributes to a broader understanding of the origins and diversity of herbivore‐microbe symbioses. Considering that amphibians represent the oldest, ancestral terrestrial vertebrates [Duellman and Trueb, 1994], their symbioses are potentially ancient. Further details of gastrointestinal fermentation in tadpoles will be informative in the study of the evolution of fermentative digestion in vertebrates. From a conservation perspective, a better understanding of the larval food and habitat requirements of invasive and endangered anuran species is critical. For example, R. catesbeiana is a widespread invasive species that displaces native frogs in areas of its introduction [Hayes and Jennings, 1986; Kiesecker and Blaustein, 1998]. The mechanisms underlying this displacement are unknown, but some authors have implicated competitive interactions between R. catesbeiana tadpoles and native tadpoles for food resources [Kiesecker et al., 2001]. Relevant to studies of amphibian declines, the loss of herbivorous tadpoles may be causing algal overgrowth and altered food web dynamics and energy flow in some streams and ponds in tropical montane regions [Ranvestel et al., 2004]. CONCLUSIONS The nutritional ecology and digestive physiology of tadpoles remain, for the most part, enigmatic and uninvestigated. Most studies to date have focused on oral morphology, observations of feeding behavior, and gut content analyses of common species of anuran larvae. Dietary protein seems to be a pivotal nutrient that results in better tadpole growth and development. Further investigation is warranted

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in the nutritional requirements of tadpoles, the digestibilities and assimilation of various food items, and the roles of endemic gastrointestinal symbionts. Adding to the World Association of Zoos and Aquarium’s call for more ex situ tadpole rearing programs, and mirroring the plea of Altig et al. [2007], more detailed descriptions of captive and wild tadpole feeding, nutrition, and digestion are desperately needed in anticipation of “rapid‐response” measures that will need to be taken for anuran species in imminent danger. This is particularly true for tropical anuran species, which are experiencing the most catastrophic population declines. REFERENCES Abrahamse A. 2009. Oregon Spotted Frog (Rana pretiosa) captive rearing protocol. Report prepared by Northwest Trek Wildlife Park and The Oregon Spotted Frog Rearing Subgroup. Adamson ML. 1981. Gyrinicola batrachiensis (Walton, 1929) n.comb. (Oxyuroidea; Nematoda) from tadpoles in eastern and central Canada. Can J Zool 59:1344–1350. Alexander MP. 1969. Differential staining of aborted and nonaborted pollen. Stain Technol 44:117–122. Altig R, Johnston GF. 1989. Guilds of anuran larvae: relationships among developmental modes, morphologies, and habitats. Herpetol Monogr 3: 81–109. Altig R, Kelly JP. 1974. Indices of feeding in anuran tadpoles as indicated by gut characteristics. Herpetologica 30:200–203. Altig R, McDearman W. 1975. Percent assimilation and clearance times of five anuran tadpoles. Herpetologica 31:67–69. Altig R, Whiles MR, Taylor CL. 2007. What do tadpoles really eat? Assessing the trophic status of an understudied and imperiled group of consumers in freshwater habitats. Freshw Biol 52:386–395. Amphibian Ark Progress of Programs [Internet]. Conservation Breeding Specialist Group [cited 2013 Dec 16]. Available from http://www. amphibianark.org/resources/progress‐of‐programs/ Battaglini P, Boni. P. 1967. Indigenous microbial flora and the large intestine in tadpoles. Experientia 23:950–951. Bjorndal KA. 1997. Fermentation in reptiles and amphibians. In: Mackie RI, White BA, editors. Gastrointestinal microbiology: Volume 1, gastrointestinal ecosystems and fermentations. New York: Chapman & Hall. p 199– 230 Costa HH, Balasubramanian S. 1965. The food of the tadpoles of Rhacophorous cruciger cruciger (Blyth). Ceylon J Sci 5:105–109. Crump ML. 1990. Possible enhancement of growth in tadpoles through cannibalism. Copeia 1990:560–564. Diaz‐Paniagua C. 1985. Larval diets related to morphological characters of five anuran species in the biological reserve of Donaña (Huelva, Spain). Amphibia‐Reptilia 6:307–322. Duellman WE, Trueb L. 1994. Biology of amphibians. Baltimore, MD: Johns Hopkins University Press. Farlowe V. 1928. Algae of ponds as determined by an examination of the intestinal contents of tadpoles. Biol Bull 55:443–448. Gielens A. 2008. Oregon Spotted Frog: captive husbandry program at Mountain View Conservation Center and the Greater Vancouver Zoo. Report prepared for Public Works and Government Services Canada. Gromko MH, Mason FS, Smith‐Gill. SJ. 1973. Analysis of the crowding effect in Rana pipiens tadpoles. J Exp Zool 186:63–72. Harrison JD. 1987. Food and feeding relations of common frog and common toad tadpoles (Rana temporaria and Bufo bufo) at a pond in mid‐Wales. Herpetol J 1:141–143. Hayes MP, Jennings MR. 1986. Decline of ranid frog species in western North America: are bullfrogs (Rana catesbeiana) responsible? J Herpetol 20:490–509. Hendricks FS. 1973. Intestinal contents of Rana pipiens Schreber (Ranidae) larvae. Southwest Nat 18:99–101. Heyer WR. 1973. Ecological interactions of frog larvae at a seasonal tropical location in Thailand. J Herpetol 7:337–361. Hourdry J, L’Hermite A, Ferrand R. 1996. Changes in the digestive tract and feeding behavior of anuran amphibians during metamorphosis. Physiol Zool 69:219–251.

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6 Pryor Inger RF. 1986. Diets of tadpoles living in a Bornean rain forest. Alytes 5:153–164. Jenssen TA. 1967. Food habits of the green frog, Rana clamitans, before and during metamorphosis. Copeia 1967:214–218. Kenny JS. 1969. Feeding mechanisms in anuran larvae. J Zool 157:225–246. Kiesecker JM, Blaustein AR. 1998. Effects of introduced bullfrogs and smallmouth bass on microhabitat use, growth, and survival of native red‐ legged frogs (Rana aurora). Conserv Biol 12:776–787. Kiesecker JM, Blaustein AR, Miller CL. 2001. Potential mechanisms underlying the displacement of native red‐legged frogs by introduced bullfrogs. Ecology 82:1964–1970. Kupferberg SJ. 1997a. Facilitation of periphyton production by tadpole grazing: functional differences between species. Freshw Biol 37:427–439. Kupferberg SJ. 1997b. The role of larval diet in anuran metamorphosis. Am Zool 37:146–159. Kupferberg SJ, Marks JC, Power ME. 1994. Effects of variation in natural algal and detrital diets on larval anuran (Hyla regilla) life‐history traits. Copeia 1994:446–457. Li JC, Lin CS. 1935. Studies of the “rain frog” Kaloula borealis II: the food and feeding of the embryos and adults. Peking Nat Hist Bull 10:45–53. McDiarmid RW, Altig R. 1999. Tadpoles: the biology of anuran larvae. Chicago, IL: University of Chicago Press. Nagai Y, Nagai S, Nishikawa T. 1971. The nutritional efficiency of cannibalism and an artificial feed for the growth of tadpoles of Japanese toad (Bufo vulgaris sp.). Agric Biol Chem 35:697–703. Nathan JM, James VG. 1972. The role of protozoa in the nutrition of tadpoles. Copeia 1972:669–679. Orton GL. 1953. The systematics of vertebrate larvae. Syst Zool 2:63–75. Osborne PL, McLachlan AJ. 1985. The effect of tadpoles on algal growth in temporary, rain‐filled rock pools. Freshw Biol 15:77–87. Pandian TJ, Marian MP. 1985. Predicting anuran metamorphosis and energetics. Physiol Zool 58:538–552. Pfennig DW. 1990. The adaptive significance of an environmentally‐cued developmental switch in an anuran tadpole. Oecologia 85:101–107. Pryor GS. 2003. Growth rates and digestive abilities of bullfrog tadpoles (Rana catesbeiana) fed algal diets. J Herpetol 37:560–566. Pryor GS. 2008. Anaerobic bacteria isolated from the gastrointestinal tracts of bullfrog tadpoles (Rana catesbeiana). Herpetol Conserv Biol 3: 176–181. Pryor GS, Bjorndal KA. 2005a. Symbiotic fermentation, digesta passage, and gastrointestinal morphology in bullfrog tadpoles (Rana catesbeiana). Physiol Biochem Zool 78:201–215. Pryor GS, Bjorndal KA. 2005b. Effects of the nematode Gyrinicola batrachiensis on development, gut morphology, and fermentation in bullfrog tadpoles (Rana catesbeiana): a novel mutualism. J Exp Zool 303A:704–712. Pryor GS, Greiner EC. 2004. Expanded geographical range, new host accounts, and observations of the nematode Gyrinicola batrachiensis (Oxyuroidea: pharyngodonidae) in tadpoles. J Parasitol 90:189–191.

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Ranvestel AW, Lips KR, Pringle CM, et al. 2004. Neotropical tadpoles influence stream benthos: evidence for ecological consequences of decline in amphibian populations. Freshw Biol 49:274–285. Sabnis JH, Kuthe KSM. 1980. Observations of food and growth of Bufo melanostictus tadpole. J Bombay Nat Hist Soc 77:21–25. Savage RM. 1952. Ecological, physiological, and anatomical observations on some species of anuran tadpoles. Proc Zool Soc Lond 122:467–514. Schorr MS, Altig R, Diehl WJ. 1990. Populational changes of the enteric protozoans Opalina spp. and Nyctotherus cordiformes during the ontogeny of anuran tadpoles. J Protozool 37:479–481. Seale DB. 1980. Influence of amphibian larvae on primary production, nutrient flux, and competition in a pond ecosystem. Ecology 61:1531– 1552. Seale DB. 1982. Obligate and facultative suspension feeding in anuran larvae: feeding regulation in Xenopus and Rana. Biol Bull 162:214–231. Seale DB, Beckvar N. 1980. The comparative ability of anuran larvae (genera: Hyla, Bufo, and Rana) to ingest suspended blue‐green algae. Copeia 1980:495–503. Sekar AG. 1992. A study of the food habits of six anuran tadpoles. J Bombay Nat Hist Soc 89:9–16. Starrett PH. 1973. Evolutionary patterns in larval morphology. In: Vial JL, editor. Evolutionary biology of the anurans: contemporary research on major problems. Columbia, MO: University of Missouri Press. p 251–271. Steinwascher K. 1978. The effect of coprophagy on the growth of Rana catesbeiana tadpoles. Copeia 1978:130–134. Stevens CE, Hume ID. 1995. Comparative physiology of the vertebrate digestive system. 2nd edition. Cambridge, UK: Cambridge University Press. Taylor CL, Altig R, Boyle CR. 1995. Can anuran tadpoles choose among foods that vary in quality? Alytes 13:81–86. Test FH, McCann RG. 1976. Foraging behavior of Bufo americanus tadpoles in response to high densities of micro‐organisms. Copeia 1976:576–578. Van Der Spuy SD, Krebs J. 2008. Collaboration for amphibian conservation: the establishment of the Johannesburg Zoo Amphibian Conservation Center in South Africa with assistance from Omaha’s Henry Doorly Zoo, USA. Int Zoo Yearbook 42:165–171. Viertel B, Richter S. 1999. Anatomy: viscera and endocrines. In: McDiarmid RW, Altig R, editors. Tadpoles: the biology of anuran larvae. Chicago, IL: University of Chicago Press. p 92–148 Wagner WE. 1986. Tadpoles and pollen: observations on the feeding behavior of Hyla regilla larvae. Copeia 1986:802–804. Wassersug R. 1972. The mechanism of ultraplanktonic entrapment in anuran larvae. J Morphol 137:279–288. Wassersug R. 1980. Internal oral features of larvae from eight anuran families: functional, systematic, evolutionary, and ecological considerations. Univ Kans Museum Nat Hist Misc Publ 68:1–146. Whiles MR, Lips KR, Pringle CM, et al. 2006. The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. Front Ecol Environ 4:27–34.

Tadpole nutritional ecology and digestive physiology: Implications for captive rearing of larval anurans.

The adaptive tadpole stage allows anurans to exploit food resources in two vastly different environments, and the transition from aquatic larvae to te...
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