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Are Seeds Consumed by Crocodilians Viable? A Test of the Crocodilian Saurochory Hypothesis
Adam E. Rosenblatt, Scott Zona, Michael R. Heithaus, and Frank J. Mazzotti

Southeastern Naturalist, Volume 13, Issue 3 (2014): N26–N29

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2014 Southeastern Naturalist Notes Vol. 13, No. 3 N26 A.E. Rosenblatt, S. Zona, M.R. Heithaus, and F.J. Mazzotti Are Seeds Consumed by Crocodilians Viable? A Test of the Crocodilian Saurochory Hypothesis Adam E. Rosenblatt1,3,*, Scott Zona1, Michael R. Heithaus1, and Frank J. Mazzotti2 Abstract - Many animal species are important dispersers of seeds; however, relatively little attention has been paid to the seed-dispersal capabilities of reptiles, and almost nothing is known about the seed-dispersal capabilities of crocodilians. This lack of information is surprising given that seeds have been found in the stomach contents of a majority of crocodilian species. Here we present the first experimental investigation of the seed-dispersal potential of a crocodilian. Using a comparative germination experiment, we tested the viability of Annona glabra (Pond-apple Tree) seeds recovered from the stomach of an Alligator mississippiensis (American Alligator [Alligator]) captured in the Florida Coastal Everglades. We found that seeds from the Alligator’s stomach were nonviable under ideal germination conditions and that fresh, non-digested Pond-apple seeds exposed to the same germination conditions were highly viable. The seeds recovered from the Alligator’s stomach were nonviable because they were likely destroyed by stomach acids. Thus, Alligators are likely not dispersers of Pond-apple seeds and may instead act as seed predators. Further research is needed to test the potential of crocodilians as dispersers of other types of seeds from different plant families. Seeds are dispersed by a wide variety of mammals, birds, and insects, leading to changes in plant demography and distribution and, in some cases, evolution of animal–plant mutualisms (Howe and Smallwood 1982). However, seed dispersal by reptiles, or saurochory, has typically received much less attention than seed dispersal by other vertebrates (Traveset 1998). Yet reptiles can be important dispersers of seeds. For example, many terrestrial and aquatic chelonians disperse seeds across terrestrial and riparian landscapes (reviewed in Moll and Jansen 1995), and 280 species of lizards (Squamata) are known to consume fleshy fruits, with 25% of the species tested showing enhanced germination of seeds that pass through their digestive systems (reviewed in Valido and Olesen 2007). One omission from the seed-dispersal literature is the order Crocodylia. Indeed, we know of no studies that have experimentally examined seed consumption, excretion, or dispersal by any crocodilians even though a recent comprehensive review of frugivory in crocodilians found that more than 70% of species for which diet data exist regularly had seeds in their stomach contents or have been directly observed consuming fruit (Platt et al. 2013). Crocodilians clearly have potential to act as seed dispersers, but evaluation of this potential requires experimentation, especially concerning viability of seeds ingested by crocodilians (Platt et al. 2013). Using stomach contents collected from wild Alligator mississippiensis Daudin (American Alligator, hereafter Alligator) we conducted a simple comparative germination experiment to test viability of seeds ingested by crocodilians. We collected stomach-contents samples from 54 adult Alligators inhabiting the Shark River Estuary in the Florida Coastal Everglades (25°25'N, 81°00'W; for full description of the study site see Rosenblatt and Heithaus 2011) from 2009–2011 using the hose-Heimlich technique (Fitzgerald 1989, Nifong et al. 2012, Rice et al. 2005). Twelve (22%) of the individuals had seeds in their 1Department of Biological Sciences, Florida International University, Miami, FL. 2Fort Lauderdale Research and Education Center, University of Florida, Davie, FL. 3Present address - School of Forestry and Environmental Studies, Yale University, New Haven, CT. *Corresponding author - arose007@ Manuscript Editor: Scott Markwith Notes of the Southeastern Naturalist, Issue 13/3, 2014 N27 2014 Southeastern Naturalist Notes Vol. 13, No. 3 A.E. Rosenblatt, S. Zona, M.R. Heithaus, and F.J. Mazzotti stomachs. The seeds came from three plants: Rhizophora mangle L. (Red Mangrove), Chrysobalanus icaco L. (Coco Plum), and Annona glabra L. (Pond-apple). Consumption of Pond-apple fruits by crocodilians was documented almost 100 years ago (Guppy 1917, Standley 1922). Pond-apple seeds were by far the most abundant seeds consumed, with one individual’s stomach containing 1286 seeds. We chose to test viability of Pond-apple seeds recovered from Alligator-stomach contents because this species provided us with a relatively large sample size of seeds and because other vertebrate species are known to consume and disperse viable Pond-apple seeds (Setter and Patane 2011, Setter et al. 2002, Westcott et al. 2008). Typically, seed dispersal in Pond-apple is diplochorous: if not consumed when ripe (leading to endozoochory), Pond-apple fruits quickly disintegrate and release their large seeds, which disperse by floatation (hydrochory; Setter and P atane 2011). An adult male Alligator (tag number: FWC 52611; 232 cm total length) that contained Pond-apple seeds in its stomach was captured on 19 November 2010. We placed 20 of the seeds in a plastic bag filled with approximately 100 mL of water, because Pond-apple seeds normally disperse by hydrochory, and transported the seeds to the Florida International University (FIU) greenhouse. On 2 December 2010, we planted all 20 seeds (evenly spaced) in a 15-cm tall by 15-cm diameter pot that contained a commercial potting medium (Fafard 4; Conrad Fafard Inc., Agawam, MA) consisting of sphagnum peat-moss, processed pine bark, and vermiculite. The seeds were irrigated 3–5 times per week because Pond-apple seeds require moist soil for germination (Swarbrick 1993). Despite the ideal growing conditions we provided, none of the seeds germinated and we terminated the experiment on 29 September 2011 (302 days after planting). We dug up the seeds at the end of the experiment and found that they were rotten and quickly disintegrated upon handling. This finding suggests that the Pond-apple seeds were not lying dormant, as has been reported for seeds that have passed through the guts of other reptiles, such as Terrapene carolina bauri Taylor (Florida Box Turtle; Liu et al. 2004). As a post hoc control, on 29 September 2011, we planted 40 fresh Pond-apple seeds (collected directly from 1 ripe fruit taken from a Pond-apple tree in the Shark River Estuary) in the FIU greenhouse in two 15-cm tall by 15-cm diameter pots (20 seeds per pot, evenly spaced) containing the Fafard 4 potting medium. The control seeds were irrigated following the same protocol used for the seeds ingested by the Alligator, and by 21 November 2011 (54 days after planting) more than 75% of the seeds had germinated and we terminated the experiment. The difference in germination rates between the control and Alligator-ingested seeds was likely not caused by the fact that the 2 seed batches were planted at different times of the year because Pond-apple seeds are able to germinate year-round in Florida (S. Zona, pers. observ.). The results from this simple experiment show that fresh Pond-apple seeds are highly viable and readily germinate, as has been shown in other studies (Setter et al. 2004, 2008), whereas Pond-apple seeds that have been ingested by Alligators are likely rendered nonviable. Thus, Alligators may act as predators, not dispersers, of Pond-apple seeds and likely do not play a role in Pond-apple demography or distribution. We hypothesize that the Pond-apples’ porous seedcoat (Guppy 1917) combined with the highly acidic conditions in the Alligator’s stomach (pH = less than 2; Coulson and Hernandez 1964) likely rendered the experimental seeds nonviable. Also, Alligators can retain hard or indigestible food items in their stomachs for weeks or even hundreds of days (Garnett 1985, Nifong et al. 2012), thereby allowing the seeds to potentially be exposed to the acidic conditions for long time periods. In contrast, other species that consume Pond-apple seeds and excrete them in a viable form, like Casuarius casuarius L. (Southern Cassowary), 2014 Southeastern Naturalist Notes Vol. 13, No. 3 N28 A.E. Rosenblatt, S. Zona, M.R. Heithaus, and F.J. Mazzotti have gentle digestive systems that do not significantly impact seeds either chemically or mechanically (Setter et al. 2002, Stocker and Irvine 1983). The results of our study suggested that Alligators are likely not dispersers of Pond-apple seeds and may instead act as seed predators. However, much more research is necessary because our sample size was small and we focused on only one type of seed in one species of crocodilian. Crocodilians are known to consume seeds from 46 genera of plants representing 33 families (Platt et al. 2013). If any of the other seed types possess hard seed coats or exhibit short gut-retention times, then crocodilians could still play a role in their seed dispersal. Acknowledgments. This material is based upon work supported by the National Science Foundation through the Florida Coastal Everglades Long-Term Ecological Research program under Grant No. DBI-0620409. Additional funding was provided by Florida International University (FIU). We thank Everglades National Park (ENP), P. Matich, D. Burkholder, R. Sarabia, K. Gastrich, and A. Fritz for assistance with field work. All procedures were carried out under permits from ENP (permit EVER-00093) and FIU’s Institutional Animal Care and Use Committee (permit 09-013). Literature Cited Coulson, R., and T. Hernandez. 1964. Biochemistry of the alligator. Louisiana State University Press, Baton Rouge, LA. 138 pp. Fitzgerald, L. 1989. 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Pond-apple (Annona glabra): A new and aggressive weed of wetlands in tropical Queensland. Proceedings of the 10th Australian Weeds Conference 10:217–219. Traveset, A. 1998. Effect of seed passage through vertebrate frugivores’ guts on germination: A review. Perspectives in Plant Ecology, Evolution, and Systematics 1/2:151–190. Valido, A., and J.M. Olesen. 2007. The importance of lizards as frugivores and seed dispersers. Pp. 124–147, In A. Dennis, E.W. Schupp, R.A. Green, and D.A. Westcott (Eds.). Seed dispersal: Theory and its Application in a Changing World. CABI Publishing, Wallingford, UK. 720 pp. Westcott, D., M. Setter, M.G. Bradford, A. McKeown, and S. Setter. 2008. Cassowary dispersal of the invasive Pond-apple in a tropical rainforest: The contribution of subordinate dispersal modes in invasion. Diversity and Distributions 14:432–439.