In ring-tailed lemurs, Lemur catta, the factors modulating hypothalamic-pituitary-adrenal (HPA) activity differ between wild and semi-free-ranging populations. Here we assess factors modulating HPA activity in ring-tailed lemurs housed in a third environment: the zoo. First we validate an enzyme immunoassay to quantify levels of glucocorticoid (GC) metabolites in the faeces of L. catta. We determine the nature of the female-female dominance hierarchies within each group by computing David's scores and examining these in relation to faecal GC (fGC). Relationships between female age and fGC are assessed to evaluate potential age-related confounds. The associations between fGC, numbers of males in a group and reproductive status are explored. Finally, we investigate the value of 7 behaviours in predicting levels of fGC. The study revealed stable linear dominance hierarchies in females within each group. The number of males in a social group together with reproductive status, but not age, influenced fGC. The 7 behavioural variables accounted for 68% of the variance in fGC. The amounts of time an animal spent locomoting and in the inside enclosure were both negative predictors of fGC. The study highlights the flexibility and adaptability of the HPA system in ring-tailed lemurs.

Keywords:
Lemur catta, Non-invasive methods, Zoo, Dominance, Social rank, Glucocorticoids
1.
Abbott DH, Keverne EB, Bercovitch FB, Shively CA, Mendoza SP, Saltzman W, Snowdon CT, Ziegler TE, Banjevic M, Garland T, Sapolsky RM (2003). Are subordinates always stressed? A comparative analysis of rank differences in cortisol levels among primates. Hormones and Behavior 43: 67-82.
2.
Altmann J, Muruthi P (1988). Differences in daily life between semiprovisioned and wild-feeding baboons. American Journal of Primatology 15: 213-221.
3.
Amrein M, Heistermann M, Weingrill T (2014). The effect of fission-fusion zoo housing on hormonal and behavioural indicators of stress in Bornean orangutans (Pongo pygmaeus). International Journal of Primatology 35: 509-528.
4.
Appleby MC (1983). The probability of linearity in hierarchies. Animal Behaviour 31: 600-608.
5.
Arlet ME, Grote MN, Molleman F, Isbell, LA, Carey JR (2009). Reproductive tactics influence cortisol levels in individual male gray-cheeked mangabeys (Lophocebus albigen a). Hormones and Behavior 55: 210-216.
6.
Bales KL, French JA, Hostetler CM, Dietz JM (2005). Social and reproductive factors affecting cortisol levels in wild female golden lion tamarins (Leontopithecus rosalia). American Journal of Primatology 67: 25-35.
7.
Beehner JC, McCann C (2008). Seasonal and altitudinal effects on glucocorticoid metabolites in a wild primate (Theropithecus gelada). Physiology and Behavior 95: 508-514.
8.
Bergman TJ, Beehner JC, Cheney DL, Seyfarth RM, Whitten PL (2005). Correlates of stress in free-ranging male chacma baboons, Papio hamadryas ursinus. Animal Behaviour 70: 703-713.
9.
Calisi RM, Bentley GE (2009). Lab and field experiments: are they the same animal? Hormones and Behavior 56: 1-10.
10.
Carnegie SD, Fedigan LM, Ziegler TE (2011). Social and environmental factors affecting fecal glucocorticoids in wild, female white-faced capuchins (Cebus capucinus). American Journal of Primatology 73: 861-869.
11.
Cavigelli SA (1999). Behavioral patterns associated with faecal cortisol levels in free-ranging female ring-tailed lemurs, Lemur catta. Animal Behaviour 57: 935-944.
12.
Cavigelli SA, Caruso MJ (2015). Sex, social status and physiological stress in primates: the importance of social and glucocorticoid dynamics. Philosophical Transactions of the Royal Society B Biological Sciences 370: 20140103.
13.
Cavigelli SA, Dubovick T, Levash W, Jolly A, Pitts A (2003). Female dominance status and fecal corticoids in a cooperative breeder with low reproductive skew: ring-tailed lemurs (Lemur catta). Hormones and Behavior 43: 166-179.
14.
Coe CL, Levine S (1995). Diurnal and annual variation of adrenocortical activity in the squirrel-monkey. American Journal of Primatology 35: 283-292.
15.
Creel S (2001). Social dominance and stress hormones. Trends in Ecology and Evolution 16: 491-497.
16.
David HA (1987). Ranking from unbalanced paired-comparison data. Biometrika 74: 432-436.
17.
De Vries H (1995). An improved test of linearity in dominance hierarchies containing unknown or tied relationships. Animal Behaviour 50: 1375-1389.
18.
De Vries H (1998). Finding a dominance order most consistent with a linear hierarchy: a new procedure and review. Animal Behaviour 55: 827-843.
19.
De Vries H, Netto WJ, Hanegraaf PLH (1993). MATMAN: a program for the analysis of sociometric matrices and behavioral transmission matrices. Behaviour 125: 157-175.
20.
De Vries H, Stevens J, Vervaecke H (2006). Measuring and testing steepness of dominance hierarchies. Animal Behaviour 71: 585-592.
21.
Diamandus ED, Christopoulos TK (1996). Immunoassay. London, Academic Press.
22.
Ebner NC, Kamin H, Diaz V, Cohen RA, MacDonald K (2015). Hormones as ‘difference makers' in cognitive and socioemotional aging processes. Frontiers in Psychology 5: 1595.
23.
Edwards KL, Walker SL, Bodenham RF, Ritchie H, Shultz S (2013). Associations between social behaviour and adrenal activity in female Barbary macaques: consequences of study design. General and Comparative Endocrinology 186: 72-79.
24.
Emery Thompson M, Muller MN, Kahlenberg SM, Wrangham RW (2010). Dynamics of social and energetic stress in wild female chimpanzees. Hormones and Behavior 58: 440-449.
25.
Feng X, Wang L, Yang S, Qin D, Wang J, Li C, Lv L, Ma Y, Hu X (2011). Maternal separation produces lasting changes in cortisol and behavior in rhesus monkeys. Proceedings of the National Academy of Sciences of the United States of America 108: 14312-14317.
26.
Fichtel C, Kraus C, Ganswindt A, Heistermann M (2007). Influence of reproductive season and rank on fecal glucocorticoid levels in free-ranging male Verreaux's sifakas (Propithecus verreauxi). Hormones and Behavior 51: 640-648.
27.
Foerster S, Monfort SL (2010). Fecal glucocorticoids as indicators of metabolic stress in female Sykes' monkeys ( Cercopithecus mitis albogularis). Hormones and Behavior 58: 685-697.
28.
Foerster S, Cords M, Monfort SL (2011). Social behavior, foraging strategies, and fecal glucocorticoids in female blue monkeys (Cercopithecus mitis): potential fitness benefits of high rank in a forest guenon. American Journal of Primatology 73: 870-882.
29.
Follenius M, Brandenberger G, Oyono S, Candas V (1982). Cortisol as a sensitive index of heat-intolerance. Physiology and Behaviour 29: 509-513.
30.
Fontani S, Vaglio S, Beghelli V, Mattioli M, Bacci S, Accorsi PA (2014). Fecal concentrations of cortisol, testosterone, and progesterone in cotton-top tamarins housed in different zoological parks: relationships among physiological data, environmental conditions, and behavioral patterns. Journal of Applied Animal Welfare Science 17: 228-252.
31.
Galvao-Coelho NL, Silva HPA, Cordeiro De Sousa MB (2012). The influence of sex and relatedness on stress response in common marmosets (Callithrix jacchus). American Journal of Primatology 74: 819-827.
32.
Gammell MP, De Vries H, Jennings DJ, Carlin CM, Hayden TJ (2003). David's score: a more appropriate dominance ranking method than Clutton-Brock et al.'s index. Animal Behaviour 66: 601-605.
33.
Gesquiere LR, Learn NH, Simao MCM, Onyango PO, Alberts SC, Altmann J (2011). Life at the top: rank and stress in wild male baboons. Science 333: 357-360.
34.
Gould L, Kelley EA, LaFleur M (2015). Reproductive female feeding strategies in spiny forest-dwelling Lemur catta in southern and southwestern Madagascar: how do females meet the challenges of reproduction in this harsh habitat? Folia Primatologica 86: 16-24.
35.
Gould L, Power ML, Ellwanger N, Rambeloarivony H (2011). Feeding behavior and nutrient intake in spiny forest-dwelling ring-tailed lemurs (Lemur catta) during early gestation and early to mid-lactation periods: compensating in a harsh environment. American Journal of Physical Anthropology 145: 469-479.
36.
Gould L, Ziegler TE, Wittwer DJ (2005). Effects of reproductive and social variables on fecal glucocorticoid levels in a sample of adult male ring-tailed lemurs (Lemur catta) at the Beza Mahafaly Reserve, Madagascar. American Journal of Primatology 67: 5-23.
37.
Goymann W, Wingfield JC (2004). Allostatic load, social status and stress hormones: the costs of social status matter. Animal Behaviour 67: 591-602.
38.
Hosey GR (2005). How does the zoo environment affect the behaviour of captive primates? Applied Animal Behaviour Science 90: 107-129.
39.
Ichino S, Soma T, Miyamoto N, Chatani K, Sato H, Koyama N, Takahata Y (2015). Lifespan and reproductive senescence in a free-ranging ring-tailed lemur (Lemur catta) population at Berenty, Madagascar. Folia Primatologica 86: 134-139.
40.
Jolly A (1966). Lemur Behaviour. Chicago, University of Chicago Press.
41.
Jolly A, Dobson A, Rasamimanana HM, Walker J, O'Connor S, Solberg M, Perel V (2002). Demography of Lemur catta at Berenty Reserve, Madagascar: effects of troop size, habitat and rainfall. International Journal of Primatology 23: 327-354.
42.
Kappeler PM (1990). Female dominance in Lemur catta: more than just female feeding priority. Folia Primatologica 55: 92-95.
43.
Kappeler PM (1993). Female dominance in primates and other mammals. In Perspectives in Ethology (Bateson P, Klopfer PH, Emery Thompson NS, eds.), vol 10: Behavior and Evolution, pp 143-158. New York, Plenum Press.
44.
Mahar I, Bambico FR, Mechawar N, Nobrega JN (2014). Stress, serotonin, and hippocampal neurogenesis in relation to depression and antidepressant effects. Neuroscience and Biobehavioral Reviews 38: 173-192.
45.
McCusker C (2006). Factors Influencing Cortisol Release in the Captive Ring-Tailed Lemur, Lemur catta. Unpublished PhD thesis, Queen's University, Belfast.
46.
Munro C, Stabenfeldt G (1985). Development of a cortisol enzyme immunoassay in plasma. Clinical Chemistry 31: 956.
47.
Nater UM, Hoppmann CA, Scott SB (2013). Diurnal profiles of salivary cortisol and alpha-amylase change across the adult lifespan: evidence from repeated daily life assessments. Psychoneuroendocrinology 38: 3167-3171.
48.
Ostner J, Heistermann M, Schülke O (2008). Dominance, aggression and physiological stress in wild male Assamese macaques (Macaca assamensis). Hormones and Behavior 54: 613-619.
49.
Parga JA, Lessnau RG (2005). Female age-specific reproductive rates, birth seasonality, and infant mortality of ring-tailed lemurs on St. Catherines Island: 17-year reproductive history of a free-ranging colony. Zoo Biology 24: 295-309.
50.
Pearson BL, Reeder DM, Judge PG (2015). Crowding increases salivary cortisol but not self-directed behavior in captive baboons. American Journal of Primatology 77: 462-467.
51.
Pereira ME, Kappeler PM (1997). Divergent systems of agonistic behavior in lemurid primates. Behaviour 134: 225-274.
52.
Pirovino M, Heistermann M, Zimmermann N, Zingg R, Clauss M, Codron D, Kaup FJ, Steinmetz HW (2011). Fecal glucocorticoid measurements and their relation to rearing, behavior, and environmental factors in the population of pileated gibbons (Hylobates pileatus) held in European Zoos. International Journal of Primatology 32: 1161-1178.
53.
Pride RE (2005). Foraging success, agonism, and predator alarms: behavioural predictors of cortisol in Lemur catta. International Journal of Primatology 26: 295-319.
54.
Qin D, Rizak JD, Feng XI, Chu X, Yang SC, Li CL, Lv LB, Ma YY, Hu XT (2013). Social rank and cortisol among female rhesus macaques (Macaca mulatta). Zoological Research 34: E42-E49.
55.
Ray JC, Sapolsky RM (1992). Styles of male social-behavior and their endocrine correlates among high-ranking wild baboons. American Journal of Primatology 28: 231-250.
56.
Rivier C, Rivest S (1991). Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis - peripheral and central mechanisms. Biology of Reproduction 45: 523-532.
57.
Sapolsky RM (1983). Individual-differences in cortisol secretory patterns in the wild baboon - role of negative feedback sensitivity. Endocrinology 113: 2263-2267.
58.
Sapolsky RM (2002). Endocrinology of the stress-response. In Behavioral Endocrinology (Becker J, Breedlove S, Crews D, McCarthy M, eds.), pp 409-450. Cambridge, MIT Press.
59.
Sapolsky RM (2005). The influence of social hierarchy on primate health. Science 308: 648-652.
60.
Sauther ML, Sussman RW, Gould L (1999). The socioecology of the ringtailed lemur: thirty-five years of research. Evolutionary Anthropology 8: 120-132.
61.
Setchell JM, Smith TE, Wickings J, Knapp LA (2010). Stress, social behavior, and secondary sexual traits in a male primate. Hormones and Behavior 58: 720-728.
62.
Shutt K, MacLarnon A, Heistermann M, Semple S (2007). Grooming in Barbary macaques: better to give than receive? Biology Letters 3: 231-233.
63.
Smith TE, French JA (1997). Social and reproductive conditions modulate urinary cortisol excretion in black tufted-ear marmosets (Callithrix kuhli). American Journal of Primatology 42: 253-267.
64.
Smith TE, McGreer-Whitworth B, French JA (1998). Close proximity of the heterosexual partner reduces the physiological and behavioral consequences of novel-cage housing in black tufted-ear marmosets (Callithrix kuhli). Hormones and Behavior 34: 211-222.
65.
Sokal RR, Rohlf FJ (1995). Biometry: The Principles and Practices of Statistics in Biological Research, 3rd ed. New York, Freeman and Company.
66.
Sonnweber RS, Ravignani A, Stobbe N, Schiestl G, Wallner B, Fitch WT (2015). Rank-dependent grooming patterns and cortisol alleviation in Barbary macaques. American Journal of Primatology 77: 715-821.
67.
Starling AP, Charpentier MJE, Fitzpatrick C, Scordato ES, Drea CM (2010). Seasonality, sociality, and reproduction: long-term stressors of ring-tailed lemurs (Lemurcatta). Hormones and Behavior 57: 76-85.
68.
Strier KB, Lynch JW, Ziegler TE (2003). Hormonal changes during the mating and conception seasons of wild northern muriquis (Brachyteles arachnoides hypoxanthus). American Journal of Primatology 61: 85-99.
69.
Surbeck M, Deschner T, Weltring A, Hohmann G (2012). Social correlates of variation in urinary cortisol in wild male bonobos (Pan paniscus). Hormones and Behavior 62: 27-35.
70.
Tabachnick BG, Fidell LS (2001). Using Multivariate Statistics, 4th ed. Boston, Allyn & Bacon.
71.
Takeshita RSC, Bercovitch FB, Huffman MA, Mouri K, Garcia C, Rigaill L, Shimizu K (2014). Environmental, biological, and social factors influencing fecal adrenal steroid concentrations in female Japanese macaques (Macaca fuscata). American Journal of Primatology 76: 1084-1093.
72.
Tung J, Barreiro LB, Johnson ZP, Hansen KD, Michopoulos V, Toufexis D, Michelini K, Wilson ME, Gilad Y (2012). Social environment is associated with gene regulatory variation in the rhesus macaque immune system. Proceedings of the National Academy of Sciences of the United States of America 109: 6490-6495.
73.
Van Hooff JARAM, Wensing JAB (1987). Dominance and its behavioral measures in a captive wolf pack. In Man and Wolf (Frank HW, ed.), pp 219-252. Dordrecht, Junk.
74.
Van Schaik CP (1989). The ecology of social relationships among female primates. In Comparative Socio-Ecology of Mammals and Humans (Standen V, Foley R, eds.), pp 195-218. Blackwell, Oxford University Press.
75.
Virgin CE, Sapolsky RM (1997). Styles of male social behavior and their endocrine correlates among low-ranking baboons. American Journal of Primatology 42: 25-39.
76.
Wasser SK, Thomas R, Nair PP, Guidry C, Southers J, Lucas J, Wildt DE, Monfort SL (1993). Effects of dietary fibre on faecal steroid measurements in baboons (Papio cynocephalus cynocephalus). Journal of Reproduction and Fertility 97: 569-574.
77.
Weingrill T, Gray DA, Barrett L, Henzi SP (2004). Fecal cortisol levels in free-ranging female chacma baboons: relationship to dominance, reproductive state and environmental factors. Hormones and Behavior 45: 259-269.
78.
Wolfram M, Bellingrath S, Kudielka BM (2011). The cortisol awakening response (CAR) across the female menstrual cycle. Psychoneuroendocrinology 36: 905-912.
79.
Zaragoza F, Ibanez M, Mas B, Laiglesia S, Anzola B (2011). Influence of environmental enrichment in captive chimpanzees (Pan troglodytes spp.) and gorillas (Gorilla gorilla gorilla): behavior and faecal cortisol levels. Revista Cientifica de la Facultad de Ciencias Veterinarias de la Universidad del Zulia 21: 447-456.
© 2016 S. Karger AG, Basel
2016
Copyright / Drug Dosage / Disclaimer
Copyright: All rights reserved. No part of this publication may be translated into other languages, reproduced or utilized in any form or by any means, electronic or mechanical, including photocopying, recording, microcopying, or by any information storage and retrieval system, without permission in writing from the publisher.
Drug Dosage: The authors and the publisher have exerted every effort to ensure that drug selection and dosage set forth in this text are in accord with current recommendations and practice at the time of publication. However, in view of ongoing research, changes in government regulations, and the constant flow of information relating to drug therapy and drug reactions, the reader is urged to check the package insert for each drug for any changes in indications and dosage and for added warnings and precautions. This is particularly important when the recommended agent is a new and/or infrequently employed drug.
Disclaimer: The statements, opinions and data contained in this publication are solely those of the individual authors and contributors and not of the publishers and the editor(s). The appearance of advertisements or/and product references in the publication is not a warranty, endorsement, or approval of the products or services advertised or of their effectiveness, quality or safety. The publisher and the editor(s) disclaim responsibility for any injury to persons or property resulting from any ideas, methods, instructions or products referred to in the content or advertisements.
You do not currently have access to this content.