Hostname: page-component-cd9895bd7-jkksz Total loading time: 0 Render date: 2024-12-28T05:03:46.190Z Has data issue: false hasContentIssue false
  • English
  • Français

Non-invasive genetic sampling reveals diet shifts, but little difference in endoparasite richness and faecal glucocorticoids, in Belizean felids inside and outside protected areas

Published online by Cambridge University Press:  10 May 2016

J. Bernardo Mesa-Cruz ,
Janine L. Brown ,
Lisette P. Waits  and
Marcella J. Kelly
J. Bernardo Mesa-Cruz*
Affiliation:
Department of Fish and Wildlife Conservation, Virginia Polytechnic and State University 100 Cheatham Hall, Blacksburg, VA, 24061USA Center for Species Survival, Smithsonian Conservation Biology Institute 1500 Remount Rd, Front Royal, VA, 22630USA
Janine L. Brown
Affiliation:
Center for Species Survival, Smithsonian Conservation Biology Institute 1500 Remount Rd, Front Royal, VA, 22630USA
Lisette P. Waits
Affiliation:
Department of Fish and Wildlife Sciences, University of Idaho875 Perimeter Drive, Moscow, ID, 83844USA
Marcella J. Kelly
Affiliation:
Department of Fish and Wildlife Conservation, Virginia Polytechnic and State University 100 Cheatham Hall, Blacksburg, VA, 24061USA
*
1Corresponding author. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract:

Many Neotropical felids are threatened with extinction due to direct effects of habitat destruction and/or human persecution. However, indirect and synergistic effects of human-felid conflict remain under-studied and potentially include increased stress and diet shifts that may negatively impact felid health. We hypothesized that faecal glucocorticoid metabolites (FGM) and endoparasite species richness (ESR) would be higher, and diet would shift, for felids outside protected areas where conflict occurs. In north-western Belize, a scat-detector dog located 336 faecal samples, identified to species and individual using DNA analyses. DNA amplification success was substantially higher within protected areas than outside. We detected jaguar, puma, ocelot, jaguarundi and domestic cat. FGMs were higher in puma and jaguarundi than in other felids, while ESR was similar across felids with domestic cats exhibiting the highest number of genera. Diet partitioning occurred among felids, but domestic cats may compete with ocelot and jaguarundi for small prey. Outside of protected areas, large cats shifted their diet to smaller prey and livestock remains were not found. Contrary to our hypotheses, FGM and ESR did not differ inside versus outside protected areas, but sample sizes were low in human-modified areas. We provide a baseline on wild felid adrenal activity, endoparasites and diet and suggest improvements to increase sample sizes outside protected areas. Our research provides a template for expanding non-invasive sampling approaches more widely across the range of Neotropical felids.

Resumen:

Muchas de las especies de félidos neotropicales están amenazadas con extinción debido a efectos directos como destrucción del hábitat y/o persecución por parte de los humanos. Sin embargo, efectos indirectos y sinergísticos del conflicto con humanos permanecen poco estudiados y potencialmente incluyen incremento en estrés y cambios de dieta que pueden impactar negativamente la salud de los félidos. Hipotetisamos que los metabolitos de glucocorticoides fecales (FGM) y la riqueza de especies endoparásitas (ESR) serian mas altas, y cambios en dieta, serian observados en félidos en áreas sin protección donde existe conflicto. En el noroeste de Belice, un perro detector de heces localizo 336 muestras, identificadas con análisis de ADN hasta especie e individuo. El éxito de amplificación de ADN fue sustancialmente mas alto dentro de las áreas protegidas. Detectamos jaguar, puma, ocelote, jaguarundí, y gato domestico. FGMs fueron mas altos en pumas y jaguarundí, mientras que el ESR fue similar en todos los félidos, pero el gato domestico presento números mas altos de endoparásitos. Se observaron dietas particionadas en estos félidos, aunque el gato domestico podría estar compitiendo con ocelotes y jaguarundís por presas de tamaño pequeño. Fuera de las áreas protegidas, los félidos grandes cambiaron su dieta con presas mas pequeñas y remanentes de animales de granja no fueron evidenciados en las heces. En contradicción con nuestra hipótesis, FGM y ESR no fueron diferentes dentro o fuera de áreas protegidas, aunque el tamaño de muestra fue bajo en áreas modificadas por humanos. Ofrecemos parámetros de base en actividad adrenal, endoparásitos y dieta, y sugerimos alternativas para incrementar el tamaño de muestra fuera de las áreas protegidas. Nuestro trabajo provee un marco para expandir el uso de técnicas no invasivas a través del rango de distribución de félidos neotropicales.

Keywords

Belizedietendoparasitesfaecal glucocorticoidshabitat modificationjaguarjaguarundimolecular scatologyocelotpuma
Type
Research Article
Information
Journal of Tropical Ecology , Volume 32 , Issue 3 , May 2016 , pp. 226 - 239
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ARANDA, M., SANCHEZ-CORDERO, V. & SÁNCHEZ-CORDERO, V. 1996. Prey spectra of Jaguar (Panthera onca) and Puma (Puma concolor) in tropical forests of Mexico. Studies on Neotropical Fauna and Environment 31:65–67.CrossRefGoogle Scholar
BACA IBARRA, I. I. & SANCHEZ-CORDERO, V. 2004. Catálogo de pelos de guardia dorsal en mamíferos del estado de Oaxaca, México. Anales del Instituto de Biología. Serie Zoología 75:383–437.Google Scholar
BERTO, B., FLAUSINO, W., MCINTOSH, D., TEIXEIRA-FILHO, W. & LOPES, C. 2011. Coccidia of New World passerine birds (Aves: Passeriformes): a review of Eimeria Schneider, 1875 and Isospora Schneider, 1881 (Apicomplexa: Eimeriidae). Systematic Parasitology 80:159–204.CrossRefGoogle ScholarPubMed
BONIER, F., QUIGLEY, H. & AUSTAD, S. N. 2004. A technique for non-invasively detecting stress response in cougars. Wildlife Society Bulletin 32:711–717.CrossRefGoogle Scholar
BROQUET, T. & PETIT, E. 2004. Quantifying genotyping errors in noninvasive population genetics. Molecular Ecology 13:3601–3608.CrossRefGoogle ScholarPubMed
CARVAJAL-VILLARREAL, S., CASO, A., DOWNEY, P., MORENO, A., TEWES, M. E. & GRASSMAN, L. I. 2012. Spatial patterns of the margay (Leopardus wiedii; Felidae, Carnivora) at “El Cielo” Biosphere Reserve, Tamaulipas, Mexico. Mammalia 76:237–244.CrossRefGoogle Scholar
CASCELLI DE AZEVEDO, F. C. 2008. Food habits and livestock depredation of sympatric jaguars and pumas in the Iguaçu National Park area, South Brazil. Biotropica 40:494–500.Google Scholar
CONFORTI, V., MORATO, R. G., AUGUSTO, A. M., DE OLIVEIRA SOUSA, L., DE AVILA, D. M., BROWN, J. L. & REEVES, J. J. 2012. Noninvasive monitoring of adrenocortical function in captive jaguars (Panthera onca). Zoo Biology 31:426–441.CrossRefGoogle ScholarPubMed
DEMAY, S., BECKER, P., EIDSON, C., RACHLOW, J., JOHNSON, T. & WAITS, L. 2013. Evaluating DNA degradation rates in faecal pellets of the endangered pygmy rabbit. Molecular Ecology Resources 13:654–662.CrossRefGoogle ScholarPubMed
DIAS, E. A., NICHI, M. & GUIMARÃES, M. A. B. V. 2008. Comparison of two commercial kits and two extraction methods for fecal glucocorticoid analysis in ocelots (Leopardus pardalis) submitted to ACTH challenge. Pesquisa Veterinaria Brasileira 28:329–334.Google Scholar
DILLON, A. & KELLY, M. J. 2007. Ocelot Leopardus pardalis in Belize: the impact of trap spacing and distance moved on density estimates. Oryx 41:469–477.Google Scholar
DOBSON, H. & SMITH, R. 2000. What is stress, and how does it affect reproduction? Animal Reproduction Science 60–61:743–752.CrossRefGoogle ScholarPubMed
DOVE, C. J. & KOCH, S. L. 2010. Microscopy of feathers: a practical guide for forensic feather identification. Journal of American Society of Trace Evidence Examiners 1:15–61.Google Scholar
ENGILIS, A. J., COLE, R. E. & CARO, T. 2012. Small mammal survey of Chiquibul forest reserve, Maya mountains, Belize, 2001. Occasional papers, Museum Texas Tech University 308:1–24.Google Scholar
EVANNO, G., REGNAUT, S. & GOUDET, J. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology 14:2611–2620.Google Scholar
FANSON, K. V, WIELEBNOWSKI, N. C., SHENK, T. M. & LUCAS, J. R. 2012. Comparative patterns of adrenal activity in captive and wild Canada lynx (Lynx canadensis). Journal of Comparative Physiology B 182:57–65.Google Scholar
FARRELL, L. E., ROMAN, J. & SUNQUIST, M. E. 2000. Dietary separation of sympatric carnivores identified by molecular analysis of scats. Molecular Ecology 9:1583–1590.CrossRefGoogle ScholarPubMed
FARRIS, Z. J., GERBER, B. D., KARPANTY, S., MURPHY, A., ANDRIANJAKARIVELO, V., RATELOLAHY, F. & KELLY, M. J. 2015. When carnivores roam: temporal patterns and overlap among Madagascar's native and exotic carnivores. Journal of Zoology 296:45–57.Google Scholar
FOSTER, R. J., HARMSEN, B. J. & DONCASTER, C. P. 2010. Habitat use by sympatric jaguars and pumas across a gradient of human disturbance in Belize. Biotropica 42:724–731.Google Scholar
GARCÍA, F. J. & SÁNCHEZ-GONZÁLEZ, E. 2013. Morfometría geométrica craneal en tres especies de roedores arborícolas neotropicales (Rodentia: Cricetidae: Rhipidomys) en Venezuela. Therya 4:57–178.Google Scholar
GOODWIN, G. 1969. Mammals from the state of Oxataca, Mexico, in the American museum of natural history. Bulletin of the American Natural History Museum 141:1–270.Google Scholar
INSKIP, C. & ZIMMERMANN, A. 2009. Human-felid conflict: a review of patterns and priorities worldwide. Oryx 43:18–34.Google Scholar
KAYS, R. W. & DEWAN, A. A. 2004. Ecological impact of inside/outside house cats around a suburban nature preserve. Animal Conservation 7:273–283.Google Scholar
KELLY, M., NOSS, A., DI BITETTI, M., MAFFEI, L., ARISPE, R., PAVIOLO, A., DE AGUDELO, C. & DI BLANCO, Y. 2008. Estimating puma densities from camera trapping across three study sites: Bolivia, Argentina, and Belize. Journal of Mammalogy 89:408–418.Google Scholar
KELLY, M., BETSCH, J., WULTSCH, C., MESA, B. & MILLS, L. 2012. Noninvasive sampling for carnivores. Pp. 47–69 in Boitani, L. & Powell, R. (eds.). Carnivore ecology and conservation: a handbook of techniques. Oxford University Press, New York.Google Scholar
KOOLHAAS, J. M., KORTE, S. M., DE BOER, S. F., VAN DER VEGT, B. J., VAN REENEN, C. G., HOPSTER, H., DE JONGA, I.C., RUIS, M. A. W. & BLOKHUIS, H. J. 1999. Coping styles in animals: current status in behavior and stress-physiology. Neuroscience and Biobehavioral Reviews 23:925–935.Google Scholar
KRUK, M., HALÁSZ, J., MEELIS, W. & HALLER, J. 2004. Fast positive feedback between the adrenocortical stress response and a brain mechanism involved in aggressive behavior. Behavioral Neuroscience 118:1062–1070.Google Scholar
LAFFERTY, K. D. 1997. Environmental parasitology: what can parasites tell us about human impacts on the environment;? Parasitology Today 13:251–255.Google Scholar
LAUNDRÉ, J. W. & HERNÁNDEZ, L. 2010. What we know about cougars in Latin America. Pp. 60–76 in Hornocker, M. & Negri, S. (eds.). Cougar: ecology and conservation. The University of Chicago Press, Chicago.Google Scholar
LONG, R. A., DONOVAN, T. M., MACKAY, P., ZIELINSKI, W. J. & BUZAS, J. S. 2007. Effectiveness of scat detection dogs for detecting forest carnivores. Journal of Wildlife Management 71:2018–2025.CrossRefGoogle Scholar
LOPEZ, J., CEVARIO, S. & O'BRIEN, S. 1996. Complete nucleotide sequences of the domestic cat (Felis catus) mitochondrial genome and a transposed mtDNA tandem repeat (Numt) in the nuclear genome. Genomics 33:229–246.Google Scholar
LOSS, S. R., WILL, T. & MARRA, P. P. 2013. The impact of free-ranging domestic cats on wildlife of the United States. Nature Communications 4:1–7.Google Scholar
LUNGU, A., RECORDATI, C., FERRAZZI, V. & GALLAZZI, D. 2007. Image analysis of animal hair: morphological features useful in forensic veterinary medicine. Lucrări Ştiinţifice Medicină Veterinară; 40:439–446.Google Scholar
MACCARI, S. & MORLEY-FLETCHER, S. 2007. Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32:S10–S15.CrossRefGoogle ScholarPubMed
MEDINA, F. M., BONNAUD, E., VIDAL, E., TERSHY, B. R., ZAVALETA, E. S., DONLAN, C. J., KEITT, B. S., CORRE, M., HORWATH, S. V. & NOGALES, M. 2011. A global review of the impacts of invasive cats on island endangered vertebrates. Global Change Biology 17:3503–3510.Google Scholar
MESA-CRUZ, J. B., BROWN, J. L. & KELLY, M. J. 2014. Effect of natural environmental conditions in Belize on fecal glucocorticoid metabolite concentrations in jaguars (Panthera onca). Conservation Physiology 2:cou039.Google Scholar
MORATO, R. G., BUENO, M. G., MALMHEISTER, P., VERRESCHI, I. T. N. & BARNABE, R. C. 2004. Changes in the fecal concentrations of cortisol and androgen metabolites in captive male jaguars (Panthera onca) in response to stress. Brazilian Journal of Medical and Biological Research 37:1903–1907.Google Scholar
MOREIRA, N., BROWN, J. L., MORAES, W., SWANSON, W. F. & ROYAL, F. 2007. Effect of housing and environmental enrichment on adrenocortical activity, behavior and reproductive cyclicity in the female tigrina (Leopardus tigrinus) and margay (Leopardus wiedii). Zoo Biology 26:441–460.Google Scholar
MUEHLENBEIN, M. P. 2006. Intestinal parasite infections and fecal steroid levels in wild chimpanzees. American Journal of Physical Anthropology 30:546–550.Google Scholar
NOVACK, A. J., MAIN, M. B., SUNQUIST, M. E. & LABISKY, R. F. 2005. Foraging ecology of jaguar (Panthera onca) and puma (Puma concolor) in hunted and non-hunted sites within the Maya Biosphere Reserve, Guatemala. Journal of Zoology 267:167–178.Google Scholar
NSUBUGA, A., ROBBINS, M., ROEDER, A., MORIN, P., BOESCH, C. & VIGILANT, L. 2004. Factors affecting the amount of genomic DNA extracted from ape faeces and the identification of an improved sample storage method. Molecular Ecology 13:2089–2094.CrossRefGoogle ScholarPubMed
PATTON, S. & RABINOWITZ, A. 1986. A coprological survey of parasites of wild neotropical Felidae. Journal of Parasitology 72:517–520.Google Scholar
PEAKALL, R. & SMOUSE, P. E. 2012. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28:2537–2539.Google Scholar
PECON SLATTERY, J. & O'BRIEN, S. J. 1998. Patterns of Y and X chromosome DNA sequence divergence during the Felidae radiation. Genetics 148:1245–1255.Google Scholar
PILGRIM, K. L., MCKELVEY, K. S., RIDDLE, A. E. & SCHWARTZ, M. K. 2005. Felid sex identification based on noninvasive genetic samples. Molecular Ecology Notes 5:60–61.CrossRefGoogle Scholar
PIÑEIRO, A., BARJA, I., OTERO, G. P., SILVÁN, G. & ILLERA, J. C. 2015. No effects of habitat, prey abundance and competitor carnivore abundance on fecal cortisol metabolite levels in wildcats (Felis silvestris) Annales Zoologici Fennici 52:90–102.Google Scholar
POLISAR, J., MAXIT, I., SCOGNAMILLO, D., FARRELL, L., SUNQUIST, M. E. & EISENBERG, J. F. 2003. Jaguars, pumas, their prey base, and cattle ranching: ecological interpretations of a management problem. Biological Conservation 109:297–310.Google Scholar
PRITCHARD, J. K., STEPHENS, M. & DONNELLY, P. 2000. Inference of population structure using multilocus genotype data. Genetics 155:945–959.Google Scholar
RABINOWITZ, A. R. 1986a. Jaguar predation on domestic livestock in Belize. Wildlife Society Bulletin 14:170–174.Google Scholar
RABINOWITZ, A. R. 1986b. Ecology and behaviour of the jaguar (Panthera onca) in Belize, Central America. Journal of Zoology 210:149–159.CrossRefGoogle Scholar
ROMANO, M. C., RODAS, A. Z., VALDEZ, R. A, HERNÁNDEZ, S. E., GALINDO, F., CANALES, D. & BROUSSET, D. M. 2010. Stress in wildlife species: noninvasive monitoring of glucocorticoids. Neuroimmunomodulation 17:209–212.CrossRefGoogle ScholarPubMed
SANTINI, A., LUCCHINI, V., FABBRI, E. & RANDI, E. 2007. Ageing and environmental factors affect PCR success in wolf (Canis lupus) excremental DNA samples. Molecular Ecology Notes 7:955–961.CrossRefGoogle Scholar
SAPOLSKY, R., ROMERO, L. M. & MUNCK, A. 2000. How do glucocorticoids influence stress responses? Integrating permissive, suppresive, stimulatory, and preparative actions. Endocrine Reviews 21:55–89.Google Scholar
SGOIFO, A., DE BOER, S., HALLER, J. & KOOLHAAS, J. 1996. Individual differences in plasma catecholamine and corticosterone stress responses of wild-type rats: relationship with aggression. Physiology and Behavior 60:1403–1407.Google Scholar
SILVER, S. C., OSTRO, L. E. T., MARSH, L. K., MAFFEI, L., NOSS, A. J., KELLY, M. J., WALLACE, R. B., GÓMEZ, H. & AYALA, G. 2004. The use of camera traps for estimating jaguar Panthera onca abundance and density using capture/recapture analysis. Oryx 38:148–154.CrossRefGoogle Scholar
SUNQUIST, M. E. & SUNQUIST, F. 2002. Wild cats of the world. University of Chicago Press, London. 452 pp.Google Scholar
UPTON, S., MCALLISTER, C., BRILLHART, D., DUSZYNSKI, D. & WASH, C. 1992. Cross-transmission studies with Eimeria arizonensis-like oocysts (Apicomplexa) in new world rodents of the genera Baiomys, Neotoma, Onychomys, Peromyscus, and Reithrodontomys (Muridae). Journal of Parasitology 78:406–413.Google Scholar
WASSER, S. K., DAVENPORT, B., RAMAGE, E. R., HUNT, K. E., PARKER, M., CLARKE, C. & STENHOUSE, G. 2004. Scat detection dogs in wildlife research and management: application to grizzly and black bears in the Yellowhead Ecosystem, Alberta, Canada. Canadian Journal of Zoology 82:475–492.Google Scholar
WULTSCH, C., WAITS, L. & KELLY, M. 2014. Noninvasive individual and species identification of jaguars (Panthera onca), pumas (Puma concolor) and ocelots (Leopardus pardalis) in Belize, Central America using cross-species microsatellites and fecal DNA. Molecular Ecology Resources 14:1171–1182.Google Scholar
WULTSCH, C., WAITS, L. P., HALLERMAN, E. M. & KELLY, M. J. 2015. Optimizing collection methods for noninvasive genetic sampling of Neotropical felids. Wildlife Society Bulletin 39:403–412.Google Scholar
YOUNG, K. M., WALKER, S. L., LANTHIER, C., WADDELL, W. T., MONFORT, S. L. & BROWN, J. L. 2004. Noninvasive monitoring of adrenocortical activity in carnivores by fecal glucocorticoid analyses. General and Comparative Endocrinology 137:148–165.Google Scholar
ZAJAC, A. & CONBOY, G. 2012. Veterinary clinical parasitology. (Eighth edition). Wiley-Blackwell, Ames. 354 pp.Google Scholar
ZHAO, H., XU, H., XU, X. & YOUNG, D. 2007. Predatory stress induces hippocampal cell death by apoptosis in rats. Neuroscience Letters 421:115–120.Google Scholar