View Item 

Show simple item record

Isotopic niche partitioning in two sympatric howler monkey species

dc.contributor.authorFlores‐escobar, Elizabeth
dc.contributor.authorSanpera, Carolina
dc.contributor.authorJover, Lluís
dc.contributor.authorCortés‐ortiz, Liliana
dc.contributor.authorRangel‐negrín, Ariadna
dc.contributor.authorCanales‐espinosa, Domingo
dc.contributor.authorDias, Pedro Américo D.
dc.date.accessioned2020-07-02T20:33:17Z
dc.date.availableWITHHELD_13_MONTHS
dc.date.available2020-07-02T20:33:17Z
dc.date.issued2020-07
dc.identifier.citationFlores‐escobar, Elizabeth ; Sanpera, Carolina; Jover, Lluís ; Cortés‐ortiz, Liliana ; Rangel‐negrín, Ariadna ; Canales‐espinosa, Domingo ; Dias, Pedro Américo D. (2020). "Isotopic niche partitioning in two sympatric howler monkey species." American Journal of Physical Anthropology 172(3): 438-446.
dc.identifier.issn0002-9483
dc.identifier.issn1096-8644
dc.identifier.urihttps://hdl.handle.net/2027.42/155926
dc.description.abstractObjectivesEcological similarity between species can lead to interspecific trophic competition. However, when ecologically similar species coexist, they may differ in foraging strategies and habitat use, which can lead to niche partitioning. As the body tissues of consumers contain a stable isotope signature that reflects the isotopic composition of their diet, stable isotope analysis is a useful tool to study feeding behavior. We measured the isotopic niche width, which is a proxy for trophic niche width, of mantled (Alouatta palliata) and black (A. pigra) howler monkeys. Specifically, studied populations in allopatry and sympatry to assess whether these species showed niche partitioning.Materials and MethodsBetween 2008 and 2012, we collected hair samples from 200 subjects (113 black and 87 mantled howler monkeys) and used continuous flow isotope ratio mass spectrometry to estimate δ13C and δ15N. We described the isotopic niche width of each species in allopatry and sympatry with the Bayesian estimation of the standard ellipse areas.ResultsIn allopatry, isotopic niche width and isotopic variation were similar in both species. In sympatry, black howler monkeys had a significantly broader isotopic niche, which was mainly determined by high δ15N values, and included the majority of mantled howler monkeys’ isotopic niche. The isotopic niche of mantled howler monkeys did not differ between sympatry and allopatry.ConclusionsThe coexistence of these ecologically similar species may be linked to trophic niche adjustments by one species, although the particular features of such adjustments (e.g., dietary, spatial, or sensory partitioning) remain to be addressed.
dc.publisherJohn Wiley & Sons, Inc.
dc.subject.othertrophic niche
dc.subject.othercoexistence
dc.subject.otherAlouatta
dc.subject.otherstable isotope analysis
dc.subject.otherstandard ellipse area
dc.subject.othersympatry
dc.titleIsotopic niche partitioning in two sympatric howler monkey species
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelAnthropology
dc.subject.hlbtoplevelSocial Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/155926/1/ajpa24028.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/155926/2/ajpa24028_am.pdf
dc.identifier.doi10.1002/ajpa.24028
dc.identifier.sourceAmerican Journal of Physical Anthropology
dc.identifier.citedreferenceNewsome, S. D., Martínez del Rio, C., Bearhop, S., & Phillips, D. L. ( 2007 ). A niche for isotopic ecology. Frontiers in Ecology and Environment, 5, 429 - 436.
dc.identifier.citedreferenceKitchen, D. M., Cortés- Ortiz, L., Ho, L., Dias, P. A. D., Canales- Espinosa, D., & Bergman, T. J. ( 2017 ). Temporal but not acoustic plasticity in hybrid howler monkey ( Alouatta palliata x A. pigra ) loud calls. International Journal of Primatology, 40, 132 - 152.
dc.identifier.citedreferenceKuhnen, V. V., Romero, G. Q., Linhares, A. X., Vizentin- Bugoni, J., Porto, E. A. C., & Setz, E. Z. F. ( 2017 ). Diet overlap and spatial segregation between two neotropical marsupials revealed by multiple analytical approaches. PLoS One, 12, e0181188.
dc.identifier.citedreferenceLayman, C. A., Arrington, D. A., Montaña, C. G., & Post, D. M. ( 2007 ). Can stable isotope ratios provide for community- wide measures of trophic structure? Ecology, 88, 42 - 48.
dc.identifier.citedreferenceLópez- Bao, J. V., Mattisson, J., Persson, J., Aronsson, M., & Andrén, H. ( 2016 ). Tracking neighbours promotes the coexistence of large carnivores. Scientific Reports, 6, 23198.
dc.identifier.citedreferenceLush, L., Ward, A. I., & Wheeler, P. ( 2017 ). Dietary niche partitioning between sympatric brown hares and rabbits. Journal of Zoology, 303, 36 - 45.
dc.identifier.citedreferenceMatsushita, Y., Oota, H., Welker, B. J., Pavelka, M. S., & Kawamura, S. ( 2014 ). Color vision variation as evidenced by hybrid L/M opsin genes in wild populations of trichromatic Alouatta New World monkeys. International Journal of Primatology, 35, 71 - 87.
dc.identifier.citedreferenceMerkle, J. A., Polfus, J. L., Derbridge, J. J., & Heinemeyer, K. S. ( 2017 ). Dietary niche partitioning among black bears, grizzly bears and wolves in a multi- prey ecosystem. Canadian Journal of Zoology, 95, 663 - 671.
dc.identifier.citedreferenceOelze, V. M. ( 2016 ). Reconstructing temporal variation in great ape and other primate diets: A methodological framework for isotope analyses in hair. American Journal of Primatology, 78, 1004 - 1016.
dc.identifier.citedreferenceOelze, V. M., Fuller, B. T., Richards, M. P., Fruthd, B., Surbeckd, M., Hublina, J.- J., & Hohmann, G. ( 2011 ). Exploring the contribution and significance of animal protein in the diet of bonobos by stable isotope ratio analysis of hair. Proceedings of the National Academy of Sciences of the United States of America, 108, 9792 - 9797.
dc.identifier.citedreferenceOelze, V. M., Head, J. S., Robbins, M. M., Richards, M., & Boesch, C. ( 2014 ). Niche differentiation and dietary seasonality among sympatric gorillas and chimpanzees in Loango National Park (Gabon) revealed by stable isotope analysis. Journal of Human Evolution, 66, 95 - 106.
dc.identifier.citedreferencePeres, C. A., & Janson, C. H. ( 1999 ). Species coexistence, distribution and environmental determinants of neotropical primate richness: A community- level zoogeographic analysis. In J. G. Fleagle, C. H. Janson, & K. E. Reed (Eds.), Primate communities (pp. 55 - 74 ). Cambridge: Cambridge University Press.
dc.identifier.citedreferencePianka, E. R. ( 1974 ). Niche overlap and diffuse competition. Proceedings of the National Academy of Sciences of the United States of America, 71, 2141 - 2145.
dc.identifier.citedreferencePianka, E. R. ( 1981 ). Competition and niche theory. In R. M. May (Ed.), Theoretical ecology (pp. 167 - 196 ). Oxford: Blackwell.
dc.identifier.citedreferencePost, D. M. ( 2002 ). Using stable isotopes to estimate trophic position: Models, methods, and assumptions. Ecology, 83, 703 - 718.
dc.identifier.citedreferenceSánchez Colón, S., Flores Martínez, A., Cruz- Leyva, I. A., & Velázquez, A. ( 2009 ). Estado y transformación de los ecosistemas terrestres por causas humanas. In: CONABIO (Ed.), Capital natural de México: Estado de conservación y tendencias de cambio (Vol. II, pp. 75- 129). México: CONABIO.
dc.identifier.citedreferenceSchoener, T. W. ( 1974 ). Resource partitioning in ecological communities. Science, 185, 27 - 39.
dc.identifier.citedreferenceSchoeninger, M. J., Iwaniec, U. T., & Glander, K. E. ( 1997 ). Stable isotope ratios indicate diet and habitat use in New World monkeys. American Journal of Physical Anthropology, 103, 69 - 83.
dc.identifier.citedreferenceSchoeninger, M. J., Most, C. A., Moore, J. J., & Somerville, A. D. ( 2016 ). Environmental variables across Pan troglodytes study sites correspond with the carbon, but not the nitrogen, stable isotope ratios of chimpanzee hair. American Journal of Primatology, 78, 1055 - 1069.
dc.identifier.citedreferenceSimon, K. S., & Townsend, C. R. ( 2003 ). Impacts of freshwater invaders at different levels of ecological organisation, with emphasis on salmonids and ecosystem consequences. Freshwater Biology, 48, 982 - 994.
dc.identifier.citedreferenceSteinmetz, R., Garshelis, D. L., Chutipong, W., & Seuaturien, N. ( 2011 ). The shared preference niche of sympatric Asiatic black bears and sun bears in a tropical forest mosaic. PLoS One, 6, e14509.
dc.identifier.citedreferenceTilman, D. ( 1982 ). Resource competition and community structure. Princeton, NJ: Princeton University Press.
dc.identifier.citedreferenceTurner, T. F., Collyer, M. L., & Krabbenhoft, T. J. ( 2010 ). A general hypothesis- testing framework for stable isotope ratios in ecological studies. Ecology, 91, 2227 - 2233.
dc.identifier.citedreferencevan der Merwe, N. J., & Medina, E. ( 1991 ). The canopy effect, carbon isotope ratios and foodwebs in Amazonia. Journal of Archaeological Science, 18, 249 - 259.
dc.identifier.citedreferenceVanak, A. T., Fortin, D., Thaker, M., Ogden, M., Owen, C., Greatwood, S., & Slotow, R. ( 2013 ). Moving to stay in place: Behavioral mechanisms for coexistence of African large carnivores. Ecology, 94, 2619 - 2631.
dc.identifier.citedreferenceVernes, K. ( 2003 ). Fine- scale habitat preferences and habitat partitioning by three mycophagous mammals in tropical wet sclerophyll forest, North- Eastern Australia. Austral Ecology, 28, 471 - 479.
dc.identifier.citedreferenceWisheu, I. R. ( 1998 ). How organisms partition habitats: Different types of community organization can produce identical patterns. Oikos, 83, 246 - 258.
dc.identifier.citedreferenceAgostini, I., Holzmann, I., & Di Bitetti, M. S. ( 2010 ). Are howler monkey species ecologically equivalent? Trophic niche overlap in syntopic Alouatta guariba clamitans and Alouatta caraya. American Journal of Primatology, 72, 173 - 186.
dc.identifier.citedreferenceAraújo, M. S., Bolnick, D. I., & Layman, C. A. ( 2011 ). The ecological causes of individual specialisation. Ecology Letters, 14, 948 - 958.
dc.identifier.citedreferenceAyliffe, L., Cerling, T., Robinson, T., West, A., Sponheimer, M., Passey, B. H., - ¦ Ehleringer, J. R. ( 2004 ). Turnover of carbon isotopes in tail hair and breath CO 2 of horses fed an isotopically varied diet. Oecologia, 139, 11 - 22.
dc.identifier.citedreferenceBaumgarten, A., & Williamson, G. B. ( 2007 ). The distributions of howling monkeys ( Alouatta pigra and A. palliata ) in southeastern Mexico and Central America. Primates, 48, 310 - 315.
dc.identifier.citedreferenceBearhop, S., Adams, C. E., Waldron, S., Fuller, R. A., & Macleod, H. ( 2004 ). Determining trophic niche width: A novel approach using stable isotope analysis. Journal of Animal Ecology, 73, 1007 - 1012.
dc.identifier.citedreferenceBeaudrot, L., Struebig, M. J., Meijaard, E., van Balen, S., Husson, S., & Marshall, A. J. ( 2013 ). Cooccurrence patterns of Bornean vertebrates suggest competitive exclusion is strongest among distantly related species. Oecologia, 173, 1053 - 1062.
dc.identifier.citedreferenceBeck, H. E., Zimmermann, N. E., McVicar, T. R., Vergoplan, N., Berg, A., & Wood, E. F. ( 2018 ). Present and future Köppen- Geiger climate classification maps at 1- km resolution. Scientific Data, 5, 180214.
dc.identifier.citedreferenceBen- David, M., & Flaherty, E. A. ( 2012 ). Stable isotopes in mammalian research: A beginner’s guide. Journal of Mammalogy, 93, 312 - 328.
dc.identifier.citedreferenceBicca- Marques, J. C., Muhle, C. B., Prates, H. M., de Oliveira, S. G., & Calegaro- Marques, C. ( 2009 ). Habitat impoverishment and egg predation by Alouatta caraya. International Journal of Primatology, 30, 743 - 748.
dc.identifier.citedreferenceBlumenthal, S. A., Rothman, J. M., Chritz, K. L., & Cerling, T. E. ( 2016 ). Stable isotopic variation in tropical forest plants for applications in primatology. American Journal of Primatology, 78, 1041 - 1054.
dc.identifier.citedreferenceCanales- Espinosa, D., Dias, P. A. D., Rangel- Negrín, A., Aguilar- Cucurachi, S., García- Orduña, F., & Hermida- Lagunes, J. ( 2011 ). Translocación de primates mexicanos. In P. A. D. Dias, A. Rangel- Negrín, & D. Canales- Espinosa (Eds.), La conservación de los primates en México (pp. 81 - 107 ). Xalapa, Mexico: Consejo Veracruzano de Ciencia y Tecnología.
dc.identifier.citedreferenceCarothers, J. H., & Jaksic, F. M. ( 1984 ). Time as a niche difference: The role of interference competition. Oikos, 42, 403 - 406.
dc.identifier.citedreferenceChase, J. M., & Leibold, M. A. ( 2003 ). Ecological niches. Chicago, IL: University of Chicago Press.
dc.identifier.citedreferenceChesson, P. ( 2000 ). Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics, 31, 343 - 366.
dc.identifier.citedreferenceCodron, J., Kirkman, K., Duffy, K. J., Sponheimer, M., Lee- Thorp, J. A., Ganswindt, A., - ¦ Codron, D. ( 2013 ). Stable isotope turnover and variability in tail hairs of captive and free- ranging African elephants ( Loxodonta africana ) reveal dietary niche differences within populations. Canadian Journal of Zoology, 91, 124 - 134.
dc.identifier.citedreferenceCortés- Ortiz, L., Agostini, I., Aguiar, L. M., Kelaita, M., Silva, F. E., & Bicca- Marques, J. C. ( 2015 ). Hybridization in howler monkeys: Current understanding and future directions. In M. M. Kowalewski, P. A. Garber, L. Cortés- Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Adaptive radiation, systematics, and morphology (pp. 107 - 131 ). New York, NY: Springer.
dc.identifier.citedreferenceCortés- Ortiz, L., Bermingham, E., Rico, C., Rodríguez- Luna, E., Sampaio, I., & Ruiz- García, M. ( 2003 ). Molecular systematics and biogeography of the Neotropical monkey genus, Alouatta. Molecular Phylogenetics and Evolution, 26, 64 - 81.
dc.identifier.citedreferenceCortés- Ortiz, L., Duda, T. F., Canales- Espinosa, D., García- Orduña, F., Rodríguez- Luna, E., & Bermingham, E. ( 2007 ). Hybridization of large- bodied New World primates. Genetics, 176, 2421 - 2425.
dc.identifier.citedreferenceCortés- Ortiz, L., Nidiffer, M. D., Hermida- Lagunes, J., García- Orduña, F., Rangel- Negrín, A., Kitchen, D. M., - ¦ Canales- Espinosa, D. ( 2019 ). Reduced introgression of sex chromosome markers in the Mexican howler monkey ( Alouatta palliata x A. pigra ) hybrid zone. International Journal of Primatology, 40, 114 - 131.
dc.identifier.citedreferenceCortés- Ortiz, L., Rylands, A. B., & Mittermeier, R. A. ( 2015 ). The taxonomy of howler monkeys: Integrating old and new knowledge from morphological and genetic studies. In M. M. Kowalewski, P. A. Garber, L. Cortés- Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Adaptive radiation, systematics, and morphology (pp. 55 - 84 ). New York, NY: Springer.
dc.identifier.citedreferenceCrawford, K., McDonald, R. A., & Bearhop, S. ( 2008 ). Applications of stable isotope techniques to the ecology of mammals. Mammal Review, 38, 87 - 107.
dc.identifier.citedreferenceCrockett, C. M., & Eisenberg, J. F. ( 1987 ). Howlers: Variations in group size and demography. In B. B. Smuts, D. L. Cheney, R. M. Seyfarth, R. W. Wrangham, & T. M. Struhsaker (Eds.), Primate societies (pp. 54 - 68 ). Chicago, IL: The University of Chicago Press.
dc.identifier.citedreferenceCrowley, B. E. ( 2012 ). Stable isotope techniques and applications for primatologists. International Journal of Primatology, 33, 673 - 701.
dc.identifier.citedreferenceCrowley, B. E., Blanco, M. B., Arrigo- Nelson, S. J., & Irwin, M. T. ( 2013 ). Stable isotopes document resource partitioning and effects of forest disturbance on sympatric cheirogaleid lemurs. Naturwissenschaften, 100, 943 - 956.
dc.identifier.citedreferenceDammhahn, M., & Kappeler, P. M. ( 2014 ). Stable isotope analyses reveal dense trophic species packing and clear niche differentiation in a Malagasy primate community. American Journal of Physical Anthropology, 153, 249 - 259.
dc.identifier.citedreferenceDavies, T. J., Meiri, S., Barraclough, T. G., & Gittleman, J. L. ( 2007 ). Species co- existence and character divergence across carnivores. Ecology Letters, 10, 146 - 152.
dc.identifier.citedreferenceDayan, T., & Simberloff, D. ( 2005 ). Ecological and community- wide character displacement: The next generation. Ecology Letters, 8, 875 - 894.
dc.identifier.citedreferencede Roos, A. M., Schellekens, T., van Kooten, T., & Persson, L. ( 2008 ). Stage- specific predator species help each other to persist while competing for a single prey. Proceedings of the National Academy of Sciences of the United States of America, 105, 13930 - 13935.
dc.identifier.citedreferenceDeane, A. S., Nargolwalla, M. C., Kordos, L., & Begun, D. R. ( 2013 ). New evidence for diet and niche partitioning in Rudapithecus and Anapithecus from Rudabánya, Hungary. Journal of Human Evolution, 65, 704 - 714.
dc.identifier.citedreferenceDeNiro, M. J., & Epstein, S. ( 1981 ). Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta, 45, 341 - 351.
dc.identifier.citedreferenceDias, P. A. D., Alvarado, D., Rangel- Negrín, A., Canales- Espinosa, D., & Cortés- Ortiz, L. ( 2013 ). Landscape attributes affecting the natural hybridization of Mexican howler monkeys. In L. Marsh & C. A. Chapman (Eds.), Primates in fragments (Vol. 2, pp. 423 - 435 ). New York, NY: Springer.
dc.identifier.citedreferenceDias, P. A. D., & Rangel- Negrín, A. ( 2015 ). Diets of howler monkeys. In M. M. Kowalewski, P. A. Garber, L. Cortés- Ortiz, B. Urbani, & D. Youlatos (Eds.), Howler monkeys: Behavior, ecology and conservation (pp. 21 - 56 ). New York, NY: Springer.
dc.identifier.citedreferenceFahy, G. E., Richards, M. P., Riedel, J., Hublin, J. J., & Boesch, C. ( 2013 ). Stable isotope evidence of meat eating and hunting specialization in adult male chimpanzees. Proceedings of the National Academy of Sciences of the United States of America, 110, 5829 - 5833.
dc.identifier.citedreferenceFalk, J. J., ter Hofstede, H. M., Jones, P. L., Dixon, M. M., Faure, P. A., Kalko, E. K. V., & Page, R. A. ( 2015 ). Sensory- based niche partitioning in a multiple predator- multiple prey community. Proceedings of the Royal Society B, 282, 20150520.
dc.identifier.citedreferenceFick, S. E., & Hijmans, R. J. ( 2017 ). WorldClim 2: New 1- km spatial resolution climate surfaces for global land areas. International Journal of Climatology, 37, 4302 - 4315.
dc.identifier.citedreferenceFord, S. M. ( 2006 ). The biogeographic history of Mesoamerican primates. In A. Estrada, P. A. Garber, M. S. M. Pavelka, & L. A. Luecke (Eds.), New perspectives in the study of Mesoamerican primates: Distribution, ecology, behavior and conservation (pp. 81 - 114 ). New York, NY: Springer.
dc.identifier.citedreferenceGanzhorn, J. U., Wright, P. C., & Ratsimbazafy, J. ( 1999 ). Primate communities: Madagascar. In J. G. Fleagle, C. H. Janson, & K. E. Reed (Eds.), Primate communities (pp. 75 - 89 ). Cambridge: Cambridge University Press.
dc.identifier.citedreferenceGrant, P. R., & Grant, B. R. ( 2002 ). Unpredictable evolution in a 30- year study of Darwin’s finches. Science, 296, 707 - 711.
dc.identifier.citedreferenceHarcourt, A. H. ( 2006 ). Rarity in the tropics: Biogeography and macroecology of the primates. Journal of Biogeography, 33, 2077 - 2087.
dc.identifier.citedreferenceHo, L., Cortés- Ortiz, L., Dias, P. A. D., Canales- Espinosa, D., Kitchen, D. M., & Bergman, T. J. ( 2014 ). Effect of ancestry on behavioral variation in two species of howler monkeys ( Alouatta pigra and A. palliata ) and their hybrids. American Journal of Primatology, 76, 855 - 867.
dc.identifier.citedreferenceHobson, K. A. ( 1999 ). Tracing origins and migration of wildlife using stable isotopes: A review. Oecologia, 120, 314 - 326.
dc.identifier.citedreferenceHobson, K. A., & Clark, R. G. ( 1992 ). Assessing avian diets using stable isotopes II: Factors influencing diet- tissue fractionation. Condor, 94, 189 - 197.
dc.identifier.citedreferenceHutchinson, G. E. ( 1957 ). Concluding remarks. Cold Spring Harbor Symposia on Quantitative Biology, 22, 415 - 427.
dc.identifier.citedreferenceJackson, A., Inger, R., Parnell, A. C., & Bearhop, S. ( 2011 ). Comparing isotopic niche widths among and within communities: SIBER - Stable isotope Bayesian ellipses in R. Journal of Animal Ecology, 80, 595 - 602.
dc.identifier.citedreferenceJackson, A., & Parnell, A. C. ( 2019 ). Package SIBER. R package version 2.1.4.
dc.identifier.citedreferenceKelaita, M., Dias, P. A. D., Aguilar- Cucurachi, M. S., Canales- Espinosa, D., & Cortés- Ortiz, L. ( 2011 ). Impact of intrasexual selection on sexual dimorphism and testes size in the Mexican howler monkeys Alouatta palliata and A. pigra. American Journal of Physical Anthropology, 146, 179 - 187.
dc.owningcollnameInterdisciplinary and Peer-Reviewed


Files in this item

Name:
ajpa24028.pdf
Size:
1.840MB
Format:
PDF
View/Open
Name:
ajpa24028_am.pdf
Size:
817.6KB
Format:
PDF
View/Open

Show simple item record

Remediation of Harmful Language

The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.

Accessibility

If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.