Articles | Volume 8, issue 1
https://doi.org/10.5194/pb-8-1-2021
© Author(s) 2021. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
https://doi.org/10.5194/pb-8-1-2021
© Author(s) 2021. This work is distributed under
the Creative Commons Attribution 4.0 License.
the Creative Commons Attribution 4.0 License.
Life on the edge: behavioural and physiological responses of Verreaux's sifakas (Propithecus verreauxi) to forest edges
Klara Dinter
Behavioral Ecology and Sociobiology Unit, German Primate Center,
Kellnerweg 4, 37077 Göttingen, Germany
Michael Heistermann
Endocrinology Laboratory, German Primate Center, Kellnerweg 4, 37077
Göttingen, Germany
Peter M. Kappeler
Behavioral Ecology and Sociobiology Unit, German Primate Center,
Kellnerweg 4, 37077 Göttingen, Germany
Department of Sociobiology and Anthropology,
Johann-Friedrich-Blumenbach Institute for Zoology and Anthropology,
Georg-August University, Kellnerweg 6, 37077 Göttingen, Germany
Claudia Fichtel
CORRESPONDING AUTHOR
Behavioral Ecology and Sociobiology Unit, German Primate Center,
Kellnerweg 4, 37077 Göttingen, Germany
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Cited articles
Altmann, J.: Observational study of behavior: sampling methods, Behaviour,
49, 227–67, 1974.
Andriatsitohaina, B., Ramsay, M. S., Kiene, F., Lehman, S. M.,
Rasoloharijaona, S., Rakotondravony, R., and Radespiel, U.: Ecological
fragmentation effects in mouse lemurs and small mammals in northwestern
Madagascar, Am. J. Primatol., e23059, https://doi.org/10.1002/ajp.23059, 2019.
Baayen, R. H.: Analyzing linguistic data: A practical introduction to
statistics using R, Cambridge University Press, Cambridge, UK, 2008.
Baden, A. L., Mancini, A. N., Federman, S., Holmes, S. M., Johnson, S. E., Kamilar, J., Louis Jr., E. E., and Bradley, B. J.: Anthropogenic pressures drive
population genetic structuring across a critically endangered lemur species
range, Sci. Rep.-UK, 9, 16276, https://doi.org/10.1038/s41598-019-52689-2, 2019.
Balestri, M., Barresi, M., Campera, M., Serra, V., Ramanamanjato, J. B.,
Heistermann, M., and Donati, G.: Habitat degradation and seasonality affect
physiological stress levels of Eulemur collaris in littoral forest fragments, PloS One,
9, e107698, https://doi.org/10.1371/journal.pone.0107698, 2014.
Bates, D., Maechler, M., Bolker, B., and Walker, S.: Fitting linear
mixed-effects models using lme4, J. Stat. Softw., 67, 1–48,
2015.
Benadi, G., Fichtel, C., and Kappeler, P. M.: Intergroup relations and home
range use in Verreaux's Sifaka (Propithecus verreauxi), Am. J. Primatol., 70,
956–965, 2008.
Brearley, G., McAlpine, C., Bell, S., and Bradley, A.: Influence of urban
edges on stress in an arboreal mammal: a case study of squirrel gliders in
southeast Queensland, Australia, Landscape Ecol., 27, 1407–1419,
2012.
Buck, C. L., O'Reilly, K. M., and Kildaw, S. D.: Interannual variability of
Black-legged Kittiwake productivity is reflected in baseline plasma
corticosterone, Gen. Comp. Endocr., 150, 430–436, 2007.
Burgman, M. A. and Fox, J. C.: Bias in species range estimates from minimum
convex polygons: implications for conservation and options for improved
planning, Anim. Conserv., 6, 19–28, 2003.
Cameron, J. L.: Stress and behaviourally induced reproductive dysfunction in
primates, Semin. Reprod. Endocr., 15, 37–45, 1997.
Carrai, V. and Lunardini, A.: Activity patterns and home range use of two
groups of Propithecus v. verreauxi in the Kirindy Forest, Primate Report, 46, 275–284, 1996.
Creel, S., Fox, J. E., Hardy, A., Sands, J., Garrott, B., and Peterson, R.
O.: Snowmobile activity and glucocorticoid stress responses in wolves and
elk, Conserv. Biol., 16, 809–814, 2002.
Dantzer, B., Fletcher, Q. E., Boonstra, R., and Sheriff, M. J.: Measures of
physiological stress: a transparent or opaque window into the status,
management and conservation of species?, Conserv. Physiol., 2, cou023, https://doi.org/10.1093/conphys/cou023,
2014.
Delattre, P., Morellet, N., Codreanu, P., Miot, S., Quéré, J.-P.,
Sennedot, F., and Baudry, J.: Influence of edge effects on common vole
population abundance in an agricultural landscape of eastern France, Acta
Theriol., 54, 51–60, 2009.
Dunn, J. C., Cristóbal-Azkarate, J., Schulte-Herbrüggen, B.,
Chavira, R., and Veà, J. J.: Travel time predicts fecal glucocorticoid
levels in free-ranging howlers (Alouatta palliata), Int. J. Primatol.,
34, 246–259, 2013.
Ellenberg, U., Setiawan, A. N., Cree, A., Houston, D. M., and Seddon, P. J.:
Elevated hormonal stress response and reduced reproductive output in
Yellow-eyed penguins exposed to unregulated tourism, Gen. Comp.
Endocr., 152, 54–63, 2007.
Eppley, T. M., Santini, L., Tinsman, J. C., and Donati, G.: Do functional
traits offset the effects of fragmentation? The case of large-bodied diurnal
lemur species, Am. J. Primatol., 82, e23104, https://doi.org/10.1002/ajp.23104, 2020.
Fichtel, C., Kraus, C., Ganswindt, A., and Heistermann, M.: Influence of
reproductive season and rank on faecal glucocorticoid levels in free-ranging
male Verreaux's sifakas (Propithecus verreauxi), Horm. Behav., 51, 640–648, 2007.
Gabriel, D. N.: Habitat use and activity patterns as an indication of
fragment quality in a strepsirrhine primate, Int. J.
Primatol., 34, 388–406, 2013.
Ganzhorn, J. U.: Leaf chemistry and the biomass of folivorous primates in
tropical forests, Oecologia, 91, 540–547, 1992.
Gómez-Espinosa, E., Rangel-Negrín, A., Chavira, R.,
Canales-Espinosa, D., and Dias, P. A. D.: The effect of energetic and
psychosocial stressors on glucocorticoids in mantled howler monkeys
(Alouatta palliata), Am. J. Primatol., 76, 362–373, 2014.
Gould, L. and Cowen, L. L.: Lemur catta in small forest fragments: Which variables
best predict population viability?, Am. J. Primatol., 82, e23095, https://doi.org/10.1002/ajp.23095,
2020.
Hardy, M. P., Gao, H., Dong, Q., Ge, R., Wang, Q., Chai, W. R., Feng, X.,
and Sottas, C.: Stress hormone and male reproductive function, Cell
Tissue Res., 322, 147–153, 2005.
Harper, G. J., Steininger, M. K., Tucker, C. J., Juhn, D., and Hawkins, F.:
Fifty years of deforestation and forest fragmentation in Madagascar,
Environ. Conserv., 34, 1–9, 2007.
Heistermann, M., Ademmer, C. H. R., and Kaumanns, W.: Ovarian cycle and
effect of social changes on adrenal and ovarian function in Pygatherix nemaeus, Int.
J. Primatol., 25, 689–708, 2004.
Heistermann, M., Palme, R., and Ganswindt, A.: Comparison of different
enzyme-immunoassays for assessment of adrenocortical activity in primates
based on faecal analysis, Am. J. Primatol., 68, 257–273,
2006.
Hinam, H. L. and St. Clair, C. C. S.: High levels of habitat loss and
fragmentation limit reproductive success by reducing home range size and
provisioning rates of Northern saw-whet owls, Biol.
Conserv., 141, 524–535, 2008.
Homan, R. N., Regosin, J. V., Rodrigues, D. M., Reed, J. M., Windmiller, B.
S., and Romero, L. M.: Impacts of varying habitat quality on the
physiological stress of spotted salamanders (Ambystoma maculatum), Anim. Conserv., 6,
11–18, 2003.
Irwin, M. T.: Diademed sifaka (Propithecus diadema) ranging and habitat use in continuous and
fragmented forest: higher density by lower viability in fragments?,
Biotropica, 40, 231–240, 2008.
Irwin, M. T., Junge, R. E., Raharison, J.-L., and Samonds, K. E.: Variation
in physiological health of diademed sifakas across intact and fragmented
forest at Tsinjoarivo, Eastern Madagascar, Am. J. Primatol.,
72, 1013–1025, 2010.
Irwin, M. T., Samonds, K. E., Raharison, J. L., Junge, R. E., Mahefarisoa, K. L., Rasambainarivo, F., Godfrey, L. R., and Glander, K. E.: Morphometric signals of
population decline in diademed sifakas occupying degraded rainforest habitat
in Madagascar, Sci. Rep., 9, 1–14, 2019.
IUCN: The IUCN Red List of Threatened Species, Version 2020-2, available at:
https://www.iucnredlist.org, last access: 9 July 2020.
Jaimez, N. A., Bribiescas, R. G., Aronsen, G. P., Anestis, S. A., and Watts,
D. P.: Urinary cortisol levels of gray-cheeked mangabeys are higher in
disturbed compared to undisturbed forest areas in Kibale National Park,
Uganda, Anim. Conserv., 15, 242–247, 2012.
Kalbitzer, U. and Heistermann, M.: Long-term storage effects in steroid
metabolite extracts from baboon (Papio sp.) faeces – a comparison of three commonly
applied storage methods, Methods Ecol. Evol., 4, 493–500,
2013.
Kappeler, P. M. and Fichtel, C.: A 15-year perspective on the social
organization and life history of Sifaka in Kirindy Forest, in: Long-Term
Field Studies of Primates, edited by: Kappeler, P. M. and Watts, D. P.,
Springer, Berlin and Heidelberg, Germany, 101–121, 2012.
Koch, F., Signer, J., Kappeler, P. M., and Fichtel, C.: Intergroup
encounters in Verreaux's sifakas (Propithecus verreauxi): who fights and why?, Behav. Ecol. Sociobiol., 70, 797–808, 2016.
Koch, F., Ganzhorn, J. U., Rothman, J. M., Chapman, C. A., and Fichtel, C.:
Sex and seasonal differences in diet and nutrient intake in Verreaux's
sifakas (Propithecus verreauxi), Am. J. Primatol., 79, e22595, https://doi.org/10.1002/ajp.22595, 2017.
Laurance, W. F.: Reflections on the tropical deforestation crisis,
Biol. Conserv., 91, 109–117, 1999.
Laurance, W. F., Delamônica, P., Laurance, S., Delamônica, P.,
Laurance, S. G., Vasconcelos, H. L., and Thomas, E.: Rainforest fragmentation
kills big trees, Nature, 404, 836, https://doi.org/10.1038/35009032, 2000.
Laurance, W. F., Camargo, J. L., Luizão, R. C., Laurance, S. G., Pimm,
S. L., Bruna, E. M., and Van Houtan, K. S.: The fate of
Amazonian forest fragments: a 32-year investigation, Biol.
Conserv., 144, 56–67, 2011.
Lehman, S., Rajaonson, A., and Day, S.: Lemur responses to edge effects in
the Vohibola III classified forest, Madagascar, Am. J.
Primatol., 68, 293–299, 2006a.
Lehman, S., Rajaonson, A., and Day, S.: Edge effects and their influence on
lemur density and distribution in Southeast Madagascar, Am. J.
Phys. Anthropol., 129, 232–241, 2006b.
Lehman, S., Rajaonson, A., and Day, S.: Edge effects on the density of
Cheirogaleus major, Int. J. Primatol., 27, 1569–1588, 2006c.
Lehtinen, R. M., Ramanamanjato, J.-B., and Raveloarison, J. G.: Edge effects
and extinction proneness in a herpetofauna from Madagascar, Biodivers.
Conserv., 12, 1357–1370, 2003.
Lidicker, W. Z.: Responses of mammals to habitat edges: an overview,
Landscape Ecol., 14, 333–343, 1999.
Martínez-Mota, R., Valdespino, C., Sánchez-Ramos, M. A., and
Serio-Silva, J. C.: Effects of forest fragmentation on the physiological
stress response of black howler monkeys, Anim. Conserv., 10, 374–379,
2007.
Mastromonaco, G. F., Gunn, K., McCurdy-Adams, H., Edwards, D. B., and
Schulte-Hostedde, A. I.: Validation and use of hair cortisol as a measure of
chronic stress in eastern chipmunks (Tamias striatus), Conserv. Physiol., 2, cou055, https://doi.org/10.1093/conphys/cou055, 2014.
McGoogan, K. C., Steffens, T., and Lehman, S.: Edge effects on home range
size of Propithecus coquereli in northwest Madagascar, Am. J. Primatol., 71, Suppl: 1–27, abstract 127, https://doi.org/10.1002/ajp.20733, 2009.
Muller, M. N. and Wrangham, R. W.: Dominance, cortisol and stress in wild
chimpanzees (Pan troglodytes schweinfurthii), Behav. Ecol. Sociobiol., 55, 332–340, 2004.
Murcia, C.: Edge effects in fragmented forests: implications for
conservation, TREE, 10, 58–62, 1995.
Norscia, I., Carrai, V., and Borgognini-Tarli, S. M.: Influence of dry
season and food quality and quantity on behavior and feeding strategy of
Propithecus verreauxi in Kirindy, Madagascar, Int. J. Primatol., 27,
1001–1022, 2006.
Pride, E.: High faecal glucocorticoid levels predict mortality in
ring-tailed lemurs (Lemur catta), Biol. Letters, 1, 60–63, 2005.
Radespiel, U., Schulte, J., Burke, R. J., and Lehman, S. M.: Molecular edge
effects in the Endangered golden-brown mouse lemur, Microcebus ravelobensis, Oryx, 53, 716–726,
2019.
Rakotoniaina, J. H., Kappeler, P. M., Ravoniarimbinina, P., Pechouskova, E.,
Hämäläinen, A. M., Grass, J., Kirschbaum, C., and Kraus, C.:
Does habitat disturbance affect stress, body condition and parasitism in two
sympatric lemurs?, Conserv. Physiol., 4, cow034, https://doi.org/10.1093/conphys/cow034, 2016.
Rangel-Negrín, A., Alfaro, J. L., Valdez, R. A., Romano M. C., and
Serio-Silva, J. C.: Stress in Yucatan spider monkeys: effects of
environmental conditions on faecal cortisol levels in wild and captive
populations, Anim. Conserv., 12, 496–502, 2009.
Rangel-Negrín, A., Coyohua-Fuentes, A., Chavira, R., Canales-Espinosa,
D., and Dias, P. A.: Primates living outside protected habitats are more
stressed: the case of black howler monkeys in the Yucatán
Peninsula, PloS one, 9, e112329, https://doi.org/10.1371/journal.pone.0112329, 2014.
Richard, A. F.: Behavioral variation: Case study of a Malagasy lemur,
Bucknell University Press, Lewisburg, PA, USA, 1978.
Rimbach, R., Link, A., Heistermann, M., Gomez-Posada, C., and Heymann, E.
W.: Effects of logging, hunting, and forest fragment size on physiological
stress levels of two sympatric ateline primates in Colombia, Conserv.
Physiol., 1, cot031, https://doi.org/10.1093/conphys/cot031, 2013a.
Rimbach, R. Heymann, E. W., Link, A., and Heistermann, M.: Validation of an
enzymeimmunoassay for assessing adrenocortical activity and evaluation of
factors that affect levels of fecal glucocorticoid metabolites in two New
World primates, Gen. Comp. Endocr., 191, 13–23, 2013b.
Rudolph, K., Fichtel, C., Schneider, D., Heistermann, M., Koch, F., Daniel,
R., and Kappeler, P. M.: One size fits all? Relationships among group size,
health, and ecology indicate a lack of an optimal group size in a wild lemur
population, Behav. Ecol. Sociobiol., 73, 132, https://doi.org/10.1007/s00265-019-2746-0, 2019.
Rudolph, K., Fichtel, C., Heistermann, M., and Kappeler, P. M.:
Dynamics and determinants of glucocorticoid metabolite concentrations in
wild Verreaux's sifakas, Horm. Behav., 124, 104760, https://doi.org/10.1016/j.yhbeh.2020.104760, 2020.
Schwitzer, C., Mittermeier, R. A., Johnson, S. E., Donati, G., Irwin, M.,
Peacock, H., Ratsimbazafy, J., Razafindramanana, J., Louis, E. E., Chikhi,
L., Colquhoun, I. C., Tinsman, J., Dolch, R., LaFleur, M., Nash, S., Patel,
E., Randrianambinina, B., Rasolofoharivelo, T., and Wright, P. C.: Averting
lemur extinctions amid Madagascar's political crisis, Science, 343,
842–843, 2014.
Shutt, C., Setchell, J., and Heistermann, M.: Non-invasive monitoring of
physiological stress in the western lowland gorilla (Gorilla gorilla gorilla): Validation of a
faecal glucocorticoid assay and methods for practical application in the
field, Gen. Comp. Endocr., 179, 167–177, 2012.
Tarlow, E. M. and Blumstein, D. T.: Evaluating methods to quantify anthropogenic
stressors on wild animals, Appl. Anim. Behav. Sci., 102, 429–451,
2007.
Tecot, R. S., Irwin, M. T., and Raharison, J.-L.: Faecal glucocorticoid
metabolite profiles in diademed sifakas increase during seasonal fruit
scarcity with interactive effects of age/sex class and habitat
degradation, Conserv. Physiol., 7, coz001, https://doi.org/10.1093/conphys/coz001, 2019.
Trillmich, J., Fichtel, C., and Kappeler, P. M.: Coordination of group
movements in wild Verraux's sifakas (Propithecus verreauxi), Behaviour, 141, 1103–1120, 2004.
Vieilledent, G., Grinand, C., Rakotomalala, F. A., Ranaivosoa, R.,
Rakotoarijaona, J. R., Allnutt, T. F., and Achard, F.: Combining global
tree cover loss data with historical national forest cover maps to look at
six decades of deforestation and forest fragmentation in
Madagascar, Biol. Conserv., 222, 189–197, 2018.
Vitousek, M. N., Taff, C. C., Hallinger, K. K., Zimmer, C., and Winkler, D.
W.: Hormones and fitness: evidence for trade-offs in glucocorticoid
regulation across contexts, Front. Ecol. Evol., 6, 42 pp., https://doi.org/10.3389/fevo.2018.00042, 2018.
Watson, J. E. M., Whittaker, R. J., and Dawson, T. P.: Habitat structure and
proximity to forest edge affect the abundance and distribution of
forest-dependent birds in tropical coastal forests of southeastern
Madagascar, Biol. Conserv., 120, 311–327, 2004.
Zinner, D., Wygoda, C., Razafimanantsoa, L., Rasoloarison, R.,
Andrianandrasana, H. T., Ganzhorn, J. U., and Torkler, F.: Analysis of
deforestation patterns in the central Menabe, Madagascar, between 1973 and
2010, Reg. Environ. Change, 14, 157–166, 2014.
Zuur, A. F., Ieno, E. N., Walker, N. J., Saveliev, A. A., and Smith, G. M.:
Mixed effects models and extensions in ecology with R, Springer, New York, USA, 2009.
Short summary
We examined the influence of forest edge effects on activity budgets, feeding ecology, and stress hormone output in five groups of Verreaux’s sifakas (Propithecus verreauxi) in western Madagascar. Sifakas in the edge habitat travelled more, tended to have smaller home ranges, had lower fruit consumption, higher stress hormone levels, and lower birth rates than sifakas in the forest interior. Hence, Verreaux’s sifakas appear to be sensitive to microhabitat characteristics linked to forest edges.
We examined the influence of forest edge effects on activity budgets, feeding ecology, and...