Predation on Caecilians (Caecilia orientalis)
Transcription
Predation on Caecilians (Caecilia orientalis)
Herpetological Review, 2008, 39(2), 162–164. © 2008 by Society for the Study of Amphibians and Reptiles Predation on Caecilians (Caecilia orientalis) by Barred Hawks (Leucopternis princeps) Depends on Rainfall HAROLD F. GREENEY and RUDY A. GELIS Yanayacu Biological Station, Cosanga, Napo, Ecuador and W. CHRIS FUNK Department of Biology, Colorado State University Fort Collin, Colorado 80523-1878, USA e-mail: Chris.Funk@colostate.edu Caecilians are limbless, subterranean or aquatic amphibians found throughout much of the tropics (Duellman and Trueb 1994; Himstedt 1996). Although amphibians are declining dramatically (Stuart et al. 2004), the conservation status of caecilians is largely unknown due to lack of information on their ecology and natural history (Gower and Wilkinson 2005). A handful of studies have documented caecilian life histories (e.g., Funk et al. 2004; Gans 1961; Kupfer et al. 2005; Malonza and Measey 2005; Parker 1936, 1958; Sanderson 1937; Sarasin and Sarasin 1887–1890; Taylor 1968; Wake 1980). Nevertheless, 114 out of 172 species (66%) of caecilians remain too poorly known for an accurate status assess- 162 ment, and thus are listed as “Data Deficient” by the IUCN (2006). Perhaps because of their elusive nature, there is an increasing interest in the biology of caecilians (Kupfer et al. 2006; Measey and Herrel 2006). Predator-prey interactions are widely recognized to have important effects on population dynamics (e.g., Krebs et al. 1995; Lotka 1925; Volterra 1926), but in the case of caecilians, little is even known about which taxa act as predators. Snakes are considered the main predators of caecilians (Duellman and Trueb 1994; Kupfer et al. 2003), although some other predators such as turtles (Zamprogno and Zamprogno 1998), spiders (Boistel and Pauwels 2002), and ants (Measey 2004) have been documented preying on caecilians. Identifying predators of amphibians is important in the context of amphibian declines, because predation may tip already declining populations over the edge toward extinction (Corn 1993; Parker et al. 2000). Here we show that a tropical hawk acts as an important predator of the caecilian Caecilia orientalis and that this unexpected ecological interaction depends strongly on weather. Methods.—We filmed a Barred Hawk (Leucopternis princeps) nest using a hidden camera from 15 February–8 May 2004 and 7– 28 January 2005 for a total of 599 h in the private reserve of Cabañas San Isidro, next to Yanayacu Biological Station (00°35'S, 77°53'W; 1950 m elev.). During most days of filming, the nest was filmed continuously during daylight hours (from morning to evening) when the hawks were active. The Barred Hawk is a rare, large hawk (total length = 52–61 cm) found from northern Peru to Costa Rica (700–2200 m; Ridgely and Greenfield 2001). The 1700 ha reserve comprises a mosaic of primary and secondary growth in humid, montane, evergreen forest about 3 km W of the town of Cosanga in the Napo Province of northeastern Ecuador (for a more complete site description, see Greeney et al. 2006). Each year, the same Barred Hawk pair raised a single chick in the same nest. The nest was located on a rocky ledge 5 m from a rushing waterfall. The blind was installed 3.5 m above and 10 m from the nest, on the opposite side of a stream. All videos were transcribed at a later date. In addition to recording prey brought to the nest, we recorded whether it rained during each hour-long time interval. Since video quality was excellent, most taxa were clearly identifiable, but seven unknown taxa were excluded from the analysis. Because caecilians surface primarily during heavy rains and snakes are active at Yanayacu when it is clear and sunny, we hypothesized that Barred Hawks would bring more caecilians to the nest, but fewer snakes, when it was raining. We tested this in 2004 using a Fisher’s exact test. This was the second Barred Hawk nest ever documented (Muela and Valdez 2003) and the first closely monitored to document feeding behavior. Details of the breeding ecology of these Barred Hawks are being prepared separately for an ornithological journal (R. A. Gelis and H. F. Greeney, unpubl. ms.). Results.—To our surprise, a caecilian species (Caecilia orientalis) was the main prey item brought to the nest by two Barred Hawk parents to feed a single chick brooded each year (Fig. 1; videos available upon request). Caecilia orientalis is a large caecilian (total length = 31–62.5 cm) found in the Andes of Ecuador and Colombia and is the only caecilian known from this site (Funk et al. 2004; IUCN 2006). Prey items delivered to nestlings included 50 caecilians (48.1% of diet), 36 snakes (34.6%; Atractus occipitoalbus and two unidentified colubrid species), five giant Herpetological Review 39(2), 2008 FIG. 1. (A) Barred Hawk (Leucopternis princeps) with caecilian (Caecilia orientalis) in talons (left). The white chick is seen in background (upper right). A color version of this photo is available upon request. (B) Proportion of Barred Hawk diet in 2004 and 2005 composed of different taxa. (C) Barred Hawks bring significantly more caecilians than snakes to the nest when it is raining (P < 0.00001, N = 58). earthworms (4.8%), three young birds (2.9%), three small mammals (2.9%), and seven unknown animals (6.7%) (Fig. 1B). Caecilia orientalis vouchers from this site are available in the Museo de Zoología at the Pontificia Universidad Católica del Ecuador (QCAZ 21417–21419). As predicted, we found that Barred Hawks brought significantly more caecilians than snakes to the nest during hour-long time intervals when it was raining (Fisher’s exact test, P < 0.00001, N = 58; Fig. 1C). Discussion.—It is surprising that an aerial predator, the Barred Hawk, was able to find subterranean prey such as caecilians. A previous report states that birds may occasionally prey on caecilians (Wake 1983), but this report did not provide specific bird species names or details of this predator-prey interaction. During several years of research at Yanayacu, caecilians were rarely encountered on the surface in the day even when it was raining (Funk et al. 2004). Thus it is unknown how Barred Hawks are able to consistently find these elusive amphibians. These results suggest that Caecilia orientalis may actually be fairly common, as has been found for some other caecilian species (Measey 2004), yet C. orientalis is reported as “uncommon in Ecuador” by the Global Amphibian Assessment (IUCN 2006). Because of the rarity and huge ranges of Barred Hawks, we were only able to find and intensively monitor one pair over two years. It will likely take several years of intensive searching to find additional Barred Hawk nests. Nonetheless, the dominance of caecilians in this pair’s diet and consistent use of these amphibians over two years suggests that caecilian predation by Barred Hawks will likely be widespread at sites with abundant caecilian populations. Rainfall has increased at some sites in Ecuador over the last 40 years (Haylock et al. 2006), although rainfall trends at Yanayacu are unknown. If predation on caecilians is typical for Barred Hawks, changes in rainfall could alter this predator-prey interaction and potentially impact populations of both species. Climate change has already been implicated in amphibian declines in Ecuador and elsewhere in the Neotropics (Blaustein and Dobson 2006; Pounds et al. 2006). Predicting the ecological impacts of climate change, however, will require a better understanding of trophic interactions and the influence of weather on these interactions as documented here. Determining the effect of predators on caecilian populations will also require a much better understanding of caecilian population dynamics. Studying the population ecology of these fossorial amphibians has proven difficult in the past due to low detectability, a paucity of methods for individually marking caecilians, and the rareness of some caecilians species. However, at Yanayacu Biological Station and some other sites (Bustamante 2005; Measey 2004; Péfaur et al. 1987), caecilians can be abundant and thus potentially amenable to study. New methods have also recently been developed for marking caecilians for capture-recapture estimation of vital rates and demographic parameters (Gower et al. 2006; Measey et al. 2001, 2003). Use of these methods in combination with population modeling (Biek et al. 2002) and molecular genetic markers (Beebee 2005; Funk et al. 2005) should help illuminate the demography, ecology, and conservation status of these fascinating animals. Acknowledgments.—We thank Carmen Bustamante for permission to conduct research on the San Isidro Reserve. We also thank J. Beatty, L. Coloma, D. Gower, J. Matthews, J. Measey, and A. Sheldon for comments on the manuscript. Funding was provided by Matt Kaplan, John V. and Ruth Ann Moore, a Pamela and Alexander F. Skutch Award, and a Declining Amphibian Populations Task Force Seed Grant. This study was conducted in compliance with Ecuadorian laws. This is publication number 59 of the Yanayacu Natural History Research Group. LITERATURE CITED BEEBEE, T. J. C. 2005. Conservation genetics of amphibians. Heredity 95:423–427. BIEK, R., W. C. FUNK, B. A. MAXELL, AND L. S. MILLS. 2002. What is missing in amphibian decline research: Insights from ecological sensitivity analysis. Conserv. Biol. 16:728–734. BLAUSTEIN, A. R., AND A. DOBSON. 2006. A message from the frogs. Nature 439:143–144. BOISTEL, R., AND O. S. G. PAUWELS. 2002. Oscaecilia zweifeli (Zweifel’s caecilian). Predation. Herpetol. Rev. 33:120–121. Herpetological Review 39(2), 2008 163 BUSTAMANTE, M. R. 2005. La cecilia más grande del mundo. Ecuador Terra Incognita 33:34–36. CORN, P. S. 1993. Bufo boreas (boreal toad). Predation. Herpetol. Rev. 24:57. DUELLMAN, W. E., AND L. TRUEB. 1994. Biology of Amphibians. Johns Hopkins University Press, Baltimore, Maryland. FUNK, W. C., M. S. BLOUIN, P. S. CORN, B. A. MAXELL, D. S. PILLIOD, S. AMISH, AND F. W. ALLENDORF. 2005. Population structure of Columbia spotted frogs (Rana luteiventris) is strongly affected by the landscape. Mol. Ecol. 14:483–496. ––––––, G. FLETCHER-LAZO, F. NOGALES-SORNOSA, AND D. ALMEIDAREINOSO. 2004. First description of a clutch and nest site for the genus Caecilia (Gymnophiona: Caeciliidae). Herpetol. Rev. 35:128–130. GANS, C. 1961. The first record of egg laying in the caecilian Siphonops paulensis Boettger. Copeia 1961:490–491. GOWER, D. J., AND M. WILKINSON. 2005. Conservation biology of caecilian amphibians. Conserv. Biol. 19:45–55. ––––––, O. V. OOMMEN, AND M. WILKINSON. 2006. Marking amphibians with alpha numeric fluorescent tags: caecilians lead the way. Herpetol. Rev. 37:302. GREENEY, H. F., R. C. DOBBS, G. I. C. DIAZ, S. KERR, AND J. G. HAYHURST. 2006. Breeding biology of the green-fronted lancebill (Doryfera ludovicae) in eastern Ecuador. Ornitol. Neotrop. 17:321–331. HAYLOCK, M. R., T. C. PETERSON, L. M. ALVES, T. AMBRIZZI, Y. M. T. ANUNCIACAO, J. BAEZ, V. R. BARROS, M. A. BERLATO, M. BIDEGAIN, G. CORONEL, V. CORRADI, V. J. GARCIA, A. M. GRIMM, D. KAROLY, J. A. MARENGO, M. B. MARINO, D. F. MONCUNILL, D. NECHET, J. QUINTANA, E. REBELLO, M. RUSTICUCCI, J. L. SANTOS, I. TREBEJO, AND L. A. VINCENT. 2006. Trends in total and extreme South American rainfall in 1960– 2000 and links with sea surface temperature. J. Clim. 19:1490–1512. H IMSTEDT , W. 1996. Die Blindwühlen. Westarp-Wissenschaften, Magdeburg. IUCN, CONSERVATION INTERNATIONAL, AND NATURESERVE. 2006. Global Amphibian Assessment (http://www.globalamphibians.org). KREBS, C. J., S. BOUTIN, R. BOONSTRA, A. R. E. SINCLAIR, J. N. M. SMITH, M. R. T. DALE, K. MARTIN, AND R. TURKINGTON. 1995. Impact of food and predation on the snowshoe hare cycle. Science 269:1112–1115. KUPFER, A., D. J. GOWER, AND W. HIMSTEDT. 2003. Field observations on the predation of the caecilian amphibian, genus Ichthyophis (Fitzinger, 1826), by the red-tailed pipe snake Cylindrophis ruffus (Laurenti, 1768). Amphibia-Reptilia 24:212–215. ––––––, H. MÜLLER, M. M. ANTONIAZZI, C. JARED, H. GREVEN, R. A. NUSSBAUM, AND M. WILKINSON. 2006. Parental investment by skin feeding in a caecilian amphibian. Nature 440:926–929. ––––––, J. NABHITABHATA, AND W. HIMSTEDT. 2005. Life history of amphibians in the seasonal tropics: habitat, community and population ecology of a caecilian (genus Ichthyophis). J. Zool. (Lond.) 266:237– 247. LOTKA, A. J. 1925. Elements of Physical Biology. Williams and Wilkins Co., Baltimore, Maryland. MALONZA, P. K., AND G. J. MEASEY. 2005. Life history of an African caecilian: Boulengerula taitanus Loveridge 1935 (Caeciilidae Amphibia Gymnophiona). Trop. Zool. 18:49–66. MEASEY, G. J. 2004. Are caecilians rare? An East African perspective. J. East Afr. Nat. Hist. 93:1–21. ––––––, D. J. GOWER, O.V. OOMMEN, AND M. WILKINSON. 2001. Permanent marking of a fossorial caecilian, Gegeneophis ramaswamii (Amphibia: Gymnophiona: Caeciliidae). J. South Asian Nat. Hist. 5:109– 115. ––––––, ––––––, ––––––, AND ––––––. 2003. A mark-recapture study of the caecilian amphibian Gegeneophis ramaswamii (Amphibia: Gymnophiona: Caeciliidae) in southern India. J. Zool. (Lond.) 261:129– 133. ––––––, AND A. HERREL. 2006. Rotational feeding in caecilians: putting a spin on the evolution of cranial design. Biol. Lett. 2:485–487. 164 MUELA, A., AND U. VALDEZ. 2003. First report of the nest of the Barred Hawk (Leucopternis princeps) in Panama. Ornitol. Neotrop. 14:267– 268. PARKER, H. W. 1936. The caecilians of the Mamfe Division, Cameroons. Proc. Zool. Soc. Lond. 1936:135–163. ––––––. 1958. Caecilians of Seychelles Islands with description of a new subspecies. Copeia 1958:71–76. PARKER, J., S. H. ANDERSON, AND F. J. LINDZEY. 2000. Bufo baxteri (Wyoming toad). Predation. Herpetol. Rev. 31:167–168. PÉFAUR, J. E., R. PÉREZ, N. SIERRA, AND F. GODOY. 1987. Density reappraisal of caeciliids in the Andes of Venezuela. J. Herpetol. 21:335– 337. POUNDS, J. A., M. R. BUSTAMANTE, L. A. COLOMA, J. A. CONSUEGRA, M. P. L. FOGDEN, P. N. FOSTER, E. LA MARCA, K. L. MASTERS, A. MERINOVITERI, R. PUSCHENDORF, S. R. RON, G. A. SANCHEZ-AZOFEIFA, C. J. STILL, AND B. E. YOUNG. 2006. Widespread amphibian extinctions from epidemic disease driven by global warming. Nature 439:161–167. RIDGELY, R. S., AND P. J. GREENFIELD. 2001. Birds of Ecuador. Cornell University Press, Ithaca, New York. SANDERSON, I. T. 1937. Animal Treasure. Viking Press, New York. SARASIN, P., AND F. SARASIN. 1887–90. Ergebnisse Naturwissenschaftlichen. Forschungen auf Ceylon in den Jahren 1884–1886. Zur Entwicklungsgeschichte u. Anat. der Ceylonische Blindwuhle Ichthyophis glutinosus. C. W. Kreidel’s Verlag, Wiesbaden. STUART, S. N., J. S. CHANSON, N. A. COX, B. E. YOUNG, A. S. L. RODRIGUES, D. L. FISCHMAN, AND R. W. WALLER. 2004. Status and trends of amphibian declines and extinctions worldwide. Science 306:1783–1786. TAYLOR, E. H. 1968. The Caecilians of the World. University of Kansas Press, Lawrence, Kansas. VOLTERRA, V. 1926. Variazioni e fluttuazioni del numero d’individui in specie animali conviventi. Memorie della Reale Accademia dei Lincei 2:31–113. WAKE, M. H. 1980. Reproduction, growth, and population structure of the Central American caecilian Dermophis mexicanus. Herpetologica 36:244–256. ––––––. 1983. Gymnopis multiplicata, Dermophis mexicanus, and Dermophis parviceps (soldas, suelda con suelda, dos cabezas, caecilians). In D. Janzen (ed.), Costa Rican Natural History, pp. 400–401. University of Chicago Press, Chicago, Illinois. ZAMPROGNO, C., AND G. F. ZAMPROGNO. 1998. Siphonops hardyi (Hardy’s caecilian). Predation. Herpetol. Rev. 29:166. Xantusia sierrae (Sierra Night Lizard): USA: California: Kern Co., foothills of Greenhorn Mountains. Illustration by Jackson Shedd. Herpetological Review 39(2), 2008