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
Related authors
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Lilith Sidler, Johanna Rode-White, and Peter M. Kappeler
Primate Biol., 11, 13–17, https://doi.org/10.5194/pb-11-13-2024, https://doi.org/10.5194/pb-11-13-2024, 2024
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Reports of male dominance in greater bamboo lemurs were not supported by data. We studied agonistic behavior in one captive group and could confirm this assertion, which sets this species apart from all other group-living lemurs.
Maria Daskalaki, Charis Drummer, Rüdiger Behr, and Michael Heistermann
Primate Biol., 9, 23–28, https://doi.org/10.5194/pb-9-23-2022, https://doi.org/10.5194/pb-9-23-2022, 2022
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Alfaxalone is a general anesthetic used widely in veterinary medicine and has a chemical structure similar to progesterone. Here we report an unexpectedly high serum progesterone value in a female common marmoset following the treatment with alfaxalone. Cross-reactivity of the antibody used in the progesterone assay with alfaxalone most likely explains this finding, and therefore evaluation of serum progesterone results in animals treated with alfaxalone should be done with caution.
Andrea Springer and Peter M. Kappeler
Primate Biol., 3, 51–63, https://doi.org/10.5194/pb-3-51-2016, https://doi.org/10.5194/pb-3-51-2016, 2016
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Parasites play important roles in ecosystems, ultimately by affecting host health and survival. Several host traits generate differences in parasite diversity among host species living in the same habitat. We examine these traits in relation to intestinal parasitism of six sympatric lemur species. We highlight the opportunities of exploring the parasitic fauna of wildlife from a community ecology and evolutionary perspective, and identify avenues for future research on lemur parasitism.
Related subject area
Behaviour
Male-biased dominance in greater bamboo lemurs (Prolemur simus)
Report of an attack on a howler monkey Alouatta sara by a group of collared peccaries Dicotyles tajacu at a mammal clay lick in Madre de Dios, Peru
Fur rubbing in Plecturocebus cupreus – an incidence of self-medication?
Masturbation in a male Phayre's langur, Trachypithecus phayrei
Potential self-medication by brown titi monkeys, Plecturocebus brunneus, in an urban fragment forest in the Brazilian Amazon
Postural behavior of howler monkeys (Alouatta palliata, A. macconnelli, and A. caraya) during sleep: an assessment across the genus range
Active anti-predator behaviour of red titi monkeys (Plecturocebus cupreus)
Self-anointing behaviour in captive titi monkeys (Callicebus spp.)
Estimation of baboon daily travel distances by means of point sampling – the magnitude of underestimation
Fur-rubbing with Piper leaves in the San Martín titi monkey, Callicebus oenanthe
Olive baboons' (Papio anubis) response towards crowned eagles (Stephanoaetus coronatus) at Lake Manyara National Park
Age-dependent change of coalitionary strategy in male Barbary macaques
Female infanticide and female-directed lethal targeted aggression in a group of ring-tailed lemurs (Lemur catta)
Meat sharing between male and female Guinea baboons (Papio papio)
Tree shrews at the German Primate Center
History of primate behavioural and ecological field research at the German Primate Center
Dry season drinking from terrestrial man-made watering holes in arboreal wild Temminck's red colobus, The Gambia
Do wild titi monkeys show empathy?
Lilith Sidler, Johanna Rode-White, and Peter M. Kappeler
Primate Biol., 11, 13–17, https://doi.org/10.5194/pb-11-13-2024, https://doi.org/10.5194/pb-11-13-2024, 2024
Short summary
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Reports of male dominance in greater bamboo lemurs were not supported by data. We studied agonistic behavior in one captive group and could confirm this assertion, which sets this species apart from all other group-living lemurs.
Raul Bello, Eckhard Heymann, and Sam Pottie
Primate Biol., 9, 29–31, https://doi.org/10.5194/pb-9-29-2022, https://doi.org/10.5194/pb-9-29-2022, 2022
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A camera trap captured the moment in which a group of collared peccaries attacked and killed a howler monkey at a clay lick in the Taricaya Ecological Reserve, Madre de Dios, Peru. This novel behaviour helps us understand the myriad risks howler monkeys face when descending to the forest floor while also indirectly emphasizing the importance of geophagy for these animals.
Gurjit K. Theara, Juan Ruíz Macedo, Ricardo Zárate Gómez, Eckhard W. Heymann, and Sofya Dolotovskaya
Primate Biol., 9, 7–10, https://doi.org/10.5194/pb-9-7-2022, https://doi.org/10.5194/pb-9-7-2022, 2022
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As part of our study on coppery titi monkeys in the Peruvian Amazon, we observed an individual rubbing his belly with leaves from a potentially medicinal plant. He climbed down from high above and grabbed a handful of leaves from an understory tree, which made it look like a deliberate action. Sitting on a liana he then chewed on the leaves before rubbing them slowly on his belly for a couple of minutes. The plant genus is known in traditional medicine and is used for various effects.
Md Shalauddin, Md Jayedul Islam, and Tanvir Ahmed
Primate Biol., 8, 43–45, https://doi.org/10.5194/pb-8-43-2021, https://doi.org/10.5194/pb-8-43-2021, 2021
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We report the first masturbatory behaviour in a male Phayre's langur, in a semi-evergreen forest in Bangladesh. We discuss possible reasons for masturbation and suggest an adequate characterization of the socio-sexual behaviour and reproductive strategies of this globally endangered primate to demonstrate the causes, cost and consequences of masturbation. We also urge further scientific exploration into masturbation among primates due to its evolutionary and conservation significance.
Brenda Letícia Pereira Oliveira, João Pedro Souza-Alves, and Marcela Alvares Oliveira
Primate Biol., 7, 35–39, https://doi.org/10.5194/pb-7-35-2020, https://doi.org/10.5194/pb-7-35-2020, 2020
Bernardo Urbani, Dionisios Youlatos, and Martín M. Kowalewski
Primate Biol., 7, 25–33, https://doi.org/10.5194/pb-7-25-2020, https://doi.org/10.5194/pb-7-25-2020, 2020
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Sleep is the longest and most continuous behavioral phase in the 24 h cycle of mammals. However, selection of postures, substrates, and tree parts during sleep has not been adequately explored, as well as their evolutionary consequences. The present study investigates postural behavior, substrate, and tree part use during sleep in three howler species (A. palliata, A. macconnelli, and A. caraya) in Nicaragua, French Guiana, and Argentina. All three species were consistent in the use of a crouch.
Sofya Dolotovskaya, Camilo Flores Amasifuen, Caroline Elisabeth Haas, Fabian Nummert, and Eckhard W. Heymann
Primate Biol., 6, 59–64, https://doi.org/10.5194/pb-6-59-2019, https://doi.org/10.5194/pb-6-59-2019, 2019
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Reactions to predators vary a lot in primates and can be passive (hiding, fleeing) or active (mobbing, alarm calls). Due to their secretive lifestyle, Neotropical titi monkeys are thought to use mainly passive crypsis and hiding as anti-predator responses. Predator mobbing has been reported only for one titi species, Callicebus nigrifrons. We report mobbing of an ocelot and Boa constrictor in red titi monkeys and Plecturocebus cupreus, and alarm calling as a reaction to tayras and raptors.
João Pedro Souza-Alves, Natasha M. Albuquerque, Luana Vinhas, Thayane S. Cardoso, Raone Beltrão-Mendes, and Leandro Jerusalinsky
Primate Biol., 5, 1–5, https://doi.org/10.5194/pb-5-1-2018, https://doi.org/10.5194/pb-5-1-2018, 2018
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These data come from the major study on gut passage with two primate species (Callicebus coimbrai and Callicebus barbarabrownae) enclosed in the Zoobotanical Park localized in the north-eastern Brazil. During the sampling period, we have decided to obtain self-anointing and laterality data. Due to the presence of large glands in C. coimbrai and C. barbarabrownae chests, we cautiously suggest that the use of Bauhinia may be linked to olfactory communication.
Holger Sennhenn-Reulen, Langhalima Diedhiou, Matthias Klapproth, and Dietmar Zinner
Primate Biol., 4, 143–151, https://doi.org/10.5194/pb-4-143-2017, https://doi.org/10.5194/pb-4-143-2017, 2017
Rosario Huashuayo-Llamocca and Eckhard W. Heymann
Primate Biol., 4, 127–130, https://doi.org/10.5194/pb-4-127-2017, https://doi.org/10.5194/pb-4-127-2017, 2017
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We report observations fur-rubbing with leaves from the spiked pepper plant, Piper aduncum, in the San Martín titi monkey, Callicebus oenanthe. As leaf extracts from this plant include insecticidal compounds, we interpret this behaviour as a defense against ectoparasites. Our observations expand the number of primate species for which this kind of self-medication is reported.
Filipa M. D. Paciência, Deusdedith Baluya, Pay Mbaryo, Sascha Knauf, and Dietmar Zinner
Primate Biol., 4, 101–106, https://doi.org/10.5194/pb-4-101-2017, https://doi.org/10.5194/pb-4-101-2017, 2017
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Here we report two encounters between olive baboons (Papio anubis) and crowned eagles (Stephanoaetus coronatus), a potential predator, at Lake Manyara National Park, Tanzania. On both events, baboons gave alarm calls while infants got close to adults and juveniles ran to cover. Adult males approached the eagles and chased them away. The baboons’ reactions indeed support the assumption that crowned eagles pose a threat, at least for juvenile baboons.
Eva-Maria Rathke, Andreas Berghänel, Annie Bissonnette, Julia Ostner, and Oliver Schülke
Primate Biol., 4, 1–7, https://doi.org/10.5194/pb-4-1-2017, https://doi.org/10.5194/pb-4-1-2017, 2017
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Coalitions are a specific case of cooperative competition and have been explained by various factors like partner availability, distribution of fighting ability, or cost of coordination. We investigated if age is an important factor influencing coalition formation and, specifically, if males switch from a solo strategy to a cooperative one after reaching post-prime age. We found that older males formed more coalitions than younger ones, stressing the importance of age in cooperative competition.
Klara Kittler and Silvio Dietzel
Primate Biol., 3, 41–46, https://doi.org/10.5194/pb-3-41-2016, https://doi.org/10.5194/pb-3-41-2016, 2016
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We report on extremely rare events of group eviction and eventually lethal aggression in a group of ring-tailed lemurs (Lemur catta) that were targeted against the two highest-ranking females. These events erupted after an infanticide by the highest-ranking female directed at the offspring of a subordinate. We suggest that this aggressive changeover of power between two matrilines was based on the growing group size and was an act of female reproductive competition during birth season.
A. S. Goffe and J. Fischer
Primate Biol., 3, 1–8, https://doi.org/10.5194/pb-3-1-2016, https://doi.org/10.5194/pb-3-1-2016, 2016
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We describe the acquisition, sharing and consumption of meat by wild Guinea baboons. Males were the hunters and shared meat passively only with females in their social and reproductive units. Females were able to acquire meat from sharing episodes and by scavenging from their male social partners. The presence of existing social bonds, rather than short-term exchanges of meat for sex, is likely a driving factor in the occurrence of meat sharing between males and females in this species.
E. Fuchs
Primate Biol., 2, 111–118, https://doi.org/10.5194/pb-2-111-2015, https://doi.org/10.5194/pb-2-111-2015, 2015
E. W. Heymann and J. U. Ganzhorn
Primate Biol., 2, 73–80, https://doi.org/10.5194/pb-2-73-2015, https://doi.org/10.5194/pb-2-73-2015, 2015
A. P. Hillyer, R. Armstrong, and A. H. Korstjens
Primate Biol., 2, 21–24, https://doi.org/10.5194/pb-2-21-2015, https://doi.org/10.5194/pb-2-21-2015, 2015
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Terrestrial drinking is not normally reported for arboreal primates. Here we report observations of terrestrial drinking from man-made watering holes by Temminck’s red colobus (Piliocolobus badius temminckii) at two sites in The Gambia. Our observations show that shallow man-made watering holes, not harbouring predators, were used by different age classes. The implications of this behaviour for this endangered subspecies and the trend of increasing temperatures in The Gambia are discussed.
A. Clyvia, M. C. Kaizer, R. V. Santos, R. J. Young, and C. Cäsar
Primate Biol., 1, 23–28, https://doi.org/10.5194/pb-1-23-2014, https://doi.org/10.5194/pb-1-23-2014, 2014
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We report the first case of putative empathic response in titi monkeys (Callibebus). Pair bonds between males and females are typically strong, with substantial time spent grooming and tail twining. In an intriguing and unexpected observation we recorded an injured adult out-group male travelling with a neighbouring group. The group appeared to adapt travel patterns to allow him to accompany them, provided pro-social behaviour such as grooming and tolerated his presence at their sleeping site
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...