Stable isotope analyses reveal dense trophic species packing and clear niche differentiation in a malagasy primate community

American Journal of Physical Anthropology

Volumn 153, Issue 2, 2014, Pages 249-259

  Dammhahn, Melanie ^a   Kappeler, Peter M ^a,b  

^a GERMAN PRIMATE CENTER   (Germany)

^b UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

coexistence; community ecology; ecological niche; lemurs, Madagascar

Indexed keywords

CARBON; NITROGEN; STABLE ISOTOPE;

ARTICLE; COMMUNITY ECOLOGY; DWARF LEMUR; ECOLOGICAL NICHE; FEEDING BEHAVIOR; FOREST; FOREST STRUCTURE; HAIR ANALYSIS; LEMURIDAE; MADAGASCAR; MALAGASY PRIMATE COMMUNITY; MAMMAL; MOUSE LEMUR; NONHUMAN; PRIMATE; SPECIES; SPECIES DIFFERENCE; SPECIES RICHNESS; TAXON; TROPHIC LEVEL;

COEXISTENCE; COMMUNITY ECOLOGY; ECOLOGICAL NICHE; LEMURS, MADAGASCAR;

ANIMALS; ANTHROPOLOGY, PHYSICAL; CARBON ISOTOPES; ECOSYSTEM; HAIR; MADAGASCAR; MULTIVARIATE ANALYSIS; NITROGEN ISOTOPES; STREPSIRHINI;

EID: 84892600763     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.22426     Document Type: Article

References (110)

1. Ackerly DD, Schwilk DW, Webb CO,. 2006. Niche evolution and adaptive radiation: testing the order of trait divergence. Ecology 87: S50-S61. (Pubitemid 44564725)
2. Andriafidison D, Andrianaivoarivelo R, Ramilijaona O, Razanahoera MR, MacKinnon J, Jenkins RKB, Racey PA,. 2006. Nectarivory by endemic Malagasy fruit bats during the dry season. Biotropica 38: 85-90.
3. Beaudrot L, Struebig MJ, Meijaard E, Van Balen S, Husson S, Young CF, Marshall AJ,. 2013. Interspecific interactions between primates, birds, bats, and squirrels may affect community composition on Borneo. Am J Primatol 75: 170-185.
4. Beaudrot LH, Marshall AJ,. 2011. Primate communities are structured more by dispersal limitation than by niches. J Anim Ecol 80: 332-341.
5. Boecklen WJ, Yarnes CT, Cook BA, James AC,. 2011. On the use of stable isotopes in trophic ecology. Ann Rev Ecol Syst 42: 411-440.
6. Cerling CE, Wittemyer G, Ehleringer JR, Remien CH, Douglas-Hamilton I,. 2009. History of animals using isotope records (HAIR): a 6-year dietary history of one family of African elephants. Proc Natl Acad Sci USA 106: 8093-8100.
7. Cerling TE, Hart JA, Hart TB,. 2004. Stable isotope ecology in the Ituri Forest. Oecologia 138: 5-12. (Pubitemid 38161930)
8. Chase JM, Leibold MA,. 2003. Ecological niches. Linking classical and contemporary approaches. Chicago: University of Chicago Press.
9. Chesson P,. 2000a. General theory of competitive coexistence in spatially varying environments. Theor Pop Biol 58: 211-237. (Pubitemid 33037539)
10. Chesson P,. 2000b. Mechanisms of maintenance of species diversity. Ann Rev Ecol Syst 31: 343-366. (Pubitemid 32122406)
11. Clark PJ, Evans FC,. 1954. Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35: 445-453.
12. Connell JH,. 1980. Diversity and the coevolution of competitors, or the ghost of competition past. Oikos 35: 131-138.
13. Crowley B,. 2012. Stable isotope techniques and applications for primatologists. Int J Primatol 33: 673-701.
14. Crowley BE, Godfrey LR, Irwin MT,. 2010. A glance to the past: subfossils, stable isotopes, seed dispersal, and lemur species loss in southern Madagascar. Am J Primatol 71: 1-13.
15. Crowley BE, Thorén S, Rasoazanabary E, Vogel ER, Barrett MA, Zohdy S, Blanco MB, McGoogan KC, Arrigo-Nelson SJ, Irwin MT, Wright PC, Radespiel U, Godfrey LR, Koch PL, Dominy NJ,. 2011. Explaining geographical variation in the isotope composition of mouse lemurs (Microcebus). J Biogeogr 38: 2106-2121.
16. Crowley BE, Godfrey LR, Guilderson TP, Zermeno P, Koch PL, Dominy NJ,. 2012. Extinction and ecological retreat in a community of primates. Proc R Soc B 279: 3597-3605.
17. Dammhahn M, Kappeler PM,. 2005. Social system of Microcebus berthae, the world's smallest primate. Int J Primatol 26: 407-435. (Pubitemid 40534135)
18. Dammhahn M, Kappeler PM,. 2008. Comparative feeding ecology of sympatric Microcebus berthae and M. murinus. Int J Primatol 29: 1567-1589.
19. Dammhahn M, Kappeler PM,. 2010. Scramble or contest competition over food in solitarily foraging mouse lemurs (Microcebus spp.): new insights from stable isotopes. Am J Phys Anthropol 141: 181-189.
20. Dammhahn M, Soarimalala V, Goodman SM,. 2013. Trophic niche differentiation and microhabitat utilization in a species-rich montane forest small mammal community of eastern Madagascar. Biotropica 45: 111-118.
21. Dammhahn M, Goodman SM,. Under review. Trophic niche differentiation and microhabitat utilization revealed by stable isotope analyses in a dry-forest bat assamblage at Ankarana, northern Madagascar. J Trop Ecol.
22. Darimont CT, Reimchen TE,. 2002. Intra-hair stable isotope analysis implies seasonal shift to salmon in gray wolf diet. Can J Zool 80: 1638-1642. (Pubitemid 36048872)
23. DeNiro MJ, Epstein S,. 1978. Influence of diet on the distribution of carbon isotopes in animals. Geochimica et Cosmochimica Acta 42: 495-506.
24. DeNiro MJ, Epstein S,. 1981. Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45: 341-351.
25. Dew JL, Wright PC,. 1998. Frugivory and seed dispersal by four species of primates in Madagascar's eastern rain forest. Biotropica 30: 425-437.
26. Dittmann M, Dammhahn M, Kappeler PM,. In press. The impact of selective logging on behavior and ecology of Aphaenogaster swammerdami (Formicidae): 20 years later-a happy ant? Malagasy Nat.
27. Donati G, Lunardini A, Kappeler PM,. 1999. Cathemeral activity of red-fronted brown lemurs (Eulemur fulvus rufus) in the Kirindy Forest/CFPF. In:, Rakotosamimanana B, Rasamimanana H, Ganzhorn JU, Goodman SM, editors. New directions in lemur studies. New York: Plenum Press. p 119-137.
28. Eggers T, Jones TH,. 2000. You are what you eat.or are you? Trends Ecol Evol 15: 265-266.
29. Erkert HG, Kappeler PM,. 2004. Arrived in the light: diet and seasonal activity patterns in wild Verreaux's sifakas (Propithecus v. verreauxi; Primates: Indriidae). Behav Ecol Sociobiol 57: 174-186. (Pubitemid 40047532)
30. Fichtel C,. 2012. Predation. In:, Mitani JC, Call J, Kappeler PM, Palombit RA, Silk J, editors. The evolution of primate societies. Chicago: University of Chicago Press. p 169-194.
31. Fietz J, Ganzhorn JU,. 1999. Feeding ecology of the hibernating primate Cheirogaleus medius: how does it get so fat? Oecologia 121: 157-164.
32. Fleagle JG, Reed KE,. 1996. Comparing primate communities: a multivariate approach. J Hum Evol 30: 489-510.
33. Ganzhorn JU,. 1988. Food partitioning among Malagasy primates. Oecologia 75: 436-450. (Pubitemid 20419953)
34. Ganzhorn JU,. 1989a. Niche separation of seven lemur species in the eastern rainforest of Madagascar. Oecologia 79: 279-286.
35. Ganzhorn JU,. 1989b. Primate species separation in relation to secondary plant chemicals. Hum Evol 4: 125-132. (Pubitemid 20067423)
36. Ganzhorn JU,. 1992. Leaf chemistry and the biomass of folivorous primates in tropical forests. Oecologia 91: 540-547.
37. Ganzhorn JU,. 1995. Low-level forest disturbance effects on primary production, leaf chemistry, and lemur populations. Ecology 76: 2084-2096. (Pubitemid 26448988)
38. Ganzhorn JU,. 1997. Test of Fox's assembly rule for functional groups in lemur communities in Madagascar. J Zool Lond 241: 533-542.
39. Ganzhorn JU,. 1998. Nested patterns of species composition and their implications for lemur biogeography in Madagascar. Folia Primatol 69: 332-341.
40. Ganzhorn JU,. 2002. Distribution of a folivorous lemur in relation to seasonally varying food resources: integrating quantitative and qualitative aspects of food characteristics. Oecologia 131: 427-435. (Pubitemid 36064431)
41. Ganzhorn JU, Arrigo-Nelson S, Boinski S, Bollen A, Carrai V, Derby A, Donati G, Koenig A, Kowalewski M, Lahann P, et al. 2009. Possible fruit protein effects on primate communities in Madagascar and the Neotropics. PLoS One 4: 1-8.
42. Ganzhorn JU, Kappeler PM,. 1996. Lemurs of the Kirindy Forest. In:, Sorg, JP, Ganzhorn JU, editors. Ecology and economy of a tropical dry forest in Madagascar. Göttingen: Goltze. p 257-274.
43. Ganzhorn JU, Malcomber S, Andrianantoanina O, Goodman SM,. 1997. Habitat characteristics and lemur species richness in Madagascar. Biotropica 29: 331-343.
44. Ganzhorn JU, Wright PC, Ratsimbazafy J,. 1999. Primate communities: Madagascar. In:, Fleagle JG, Janson CH, Reed KE, editors. Primate communities. Cambridge: Cambridge University Press. p 75-89.
45. Godfrey LR, Winchester JM, King SJ, Boyer DM, Jernvall J,. 2012. Dental topography indicates ecological contraction of lemur communities. Am J Physical Anthropol 148: 215-227.
46. Goodman SM, O'Connor S, Langrand O,. 1993. A review of predation on lemurs: implications for the evolution of social behaviour in small mammals. In:, Kappeler PM, Ganzhorn JU, editors. Lemur social systems and their ecological basis. New York: Plenum Press. p 51-66.
47. Hilgartner R, Zinner D, Kappeler PM,. 2008. Life history traits and parental care in Lepilemur ruficaudatus. Am J Primatol 70: 2-11. (Pubitemid 351160114)
48. Hladik A, Charles-Dominique P, Cooper HM, Hladik A, Hladik CM,. 1980a. The dry forest of the west coast of Madagascar climate, phenology, and food availability for prosimians. In:, Pages E, Pariente GF, Petter-Rousseaux A, Schilling A, editors. Nocturnal Malagasy primates: ecology, physiology, and behavior. New York: Academic Press. p 3-40.
49. Hladik CM, Charles-Dominique P, Petter JJ, Charles-Dominique P, Cooper HM, Hladik A, Hladik CM,. 1980b. Feeding strategies of five nocturnal prosimians in the dry forest of the west coast of Madagascar. In:, Pages E, Pariente GF, Petter-Rousseaux A, Schilling A, editors. Nocturnal Malagasy primates: ecology, physiology, and behavior. New York: Academic Press. p 41-73.
50. Holt RD,. 1977. Apparent competition and the structure of prey communities. Theor Pop Biol 12: 197-229.
51. Holt RD,. 1984. Spatial heterogeneity, indirect interactions, and the coexistence of prey species. Am Nat 124: 377-406. (Pubitemid 16273065)
52. Holt RD, Grover J, Tilman D,. 1994. Simple rules for interspecific dominance in systems with exploitative and apparent competition. Am Nat 144: 741-771.
53. Hubbell SP,. 2001. The unified neutral theory of species abundance and diversity. Princeton, NJ: Princeton University Press.
54. Hutchinson GE,. 1957. Concluding remarks. Cold Spring Harb Symp Quant Biol 22: 415-427.
55. Jernvall J, Wright PC,. 1998. Diversity components of impending primate extinctions. Proc Natl Acad Sci USA 95: 11279-11283. (Pubitemid 28450119)
56. Kamilar JM,. 2009. Environmental and geographic correlates of the taxonomic structure of primate communities. Am J Phys Anthropol 139: 382-393.
57. Kamilar JM, Guidi LM,. 2010. The phylogenetic structure of primate communities: variation within and across continents. J Biogeogr 37: 801-813.
58. Kamilar JM, Ledogar JA,. 2011. Species co-occurrence patterns and dietary resource competition in primates. Am J Phys Anthropol 144: 131-139.
59. Kappeler PM,. 1997. Intrasexual selection in Mirza coquereli: evidence for scramble competition polygyny in a solitary primate. Behav Ecol Sociobiol 45: 115-127. (Pubitemid 27383391)
60. Kappeler PM, Fichtel C,. 2012. A 15-year perspective on the social organization and life history of sifaka in Kirindy Forest. In:, Kappeler PM, Watts DP, editors. Long-term field studies of primates. Berlin: Springer. p 101-121.
61. Karpanty SM,. 2006. Direct and indirect impacts of raptor predation on lemurs in southeastern Madagascar. Int J Primatol 27: 239-261.
62. Krebs CJ,. 1998. Ecological methodology. Menlo Park, CA: Addison-Wesley Educational Publishers.
63. Lack D,. 1947. Darwin's finches. Cambridge: Cambridge University Press.
64. Lahann P,. 2008. Habitat utilization of three sympatric cheirogaleid lemur species in a littoral rain forest of southeastern Madagascar. Int J Primatol 29: 117-134.
65. Layman CA, Araujo MS, Boucek R, Hammerschlag-Peyer CM, Harrison E, Jud ZR, Matich P, Rosenblatt AE, Vaudo JJ, Yeager LA, Post DM, Bearhop S,. 2012. Applying stable isotopes to examine food-web structure: an overview of analytical tools. Biol Rev 87: 545-562.
66. Layman CA, Arrington DA, Montana CG, Post DM,. 2007. Can stable isotope ratios provide for community-wide measures of trophic structure? Ecology 88: 42-48. (Pubitemid 46596820)
67. Lührs M-L, Dammhahn M,. 2010. An unusual case of cooperative hunting in a solitary carnivore. J Ethol 28: 379-383.
68. Lührs M-L, Dammhahn M, Kappeler P,. 2013. Strength in numbers: males in a carnivore grow bigger when they associate and hunt cooperatively. Behav Ecol 24: 21-28.
69. Marshall JD, Brooks R, Lajtha K,. 2007. Sources of variation in the stable isotopic composition of plants. In:, Michener R, Lajtha K, editors. Stable isotopes in ecology and environmental science. Malden, MA: Blackwell Publishing. p 22-60.
70. MacArthur RH, Levins R,. 1967. The limiting similarity, convergence, and divergence of coexisting species. Am Nat 101: 377-385.
71. McCutchan JH Jr, Lewis WM Jr, Kendall C, McGrath CC,. 2003. Variation in trophic shift for stable isotope ratios of carbon, nitrogen, and sulfur. Oikos 102: 378-390. (Pubitemid 36914279)
72. 13C values of leaves in Amazonian rain forests. Oecologia 45: 377-378.
73. Muldoon KM, Goodman SM,. 2010. Ecological biogeography of Malagasy non-volant mammals: community structure is correlated with habitat. J Biogeography 37: 1144-1159.
74. Norsica I, Carrai V, Borgognini-Tarli SM,. 2006. 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. (Pubitemid 44610608)
75. Ostner J,. 2002. Sex-specific reproductive strategies of redfronted lemurs (Eulemur fulvus rufus, Primates, Lemuridae). PhD Thesis University of Würzburg.
76. Pagés E, Charles-Dominique P, Cooper HM, Hladik A, Hladik CM,. 1980. Ethoecology of Microcebus coquereli during the dry season. In:, Pages E, Pariente GF, Petter-Rousseaux A, Petter JJ, Schilling A, editors. Nocturnal Malagasy primates: ecology, physiology and behavior. New York: Academic Press. p 97-116.
77. Petter JJ, Schilling A, Pariente GF,. 1971. Observation écoéthologiques sur deux lémurien malagaches nocturnes: Phaner furcifer et Microcebus coquereli. Terre et La Vie 25: 287-327.
78. Petter JJ, Albignac R, Rumpler Y,. 1977. Faune de Madagascar. Paris: Orstrom CNRS.
79. Petter JJ, Chivers DJ, Herbert J,. 1978. Ecological and physiological adaptations of five sympatric nocturnal lemurs to seasonal variation in food production. In: Recent advances in primatology. Volume 1, Behaviour. London: Academic Press. p 211-223.
80. Post DM, Pace ML, Hairstone NG Jr,. 2000. Ecosystem size determines food-chain length in lakes. Nature 405: 1047-1049. (Pubitemid 30447786)
81. Power ML,. 2010. Nutritional and digestive challenges to being a gum-feeding primate. In:, Burrows AM, Nash LT, editors. The evolution of exudativory in primates. New York: Springer.
82. 13C in sympatric mouse lemurs. Naturwissenschaften 98: 909-917.
83. Rakotonirina G,. 1996. Composition and structure of the dry forest on sandy soils near Morondava. In:, Sorg, JP, Ganzhorn JU, editors. Ecology and economy of a tropical dry forest in Madagascar. Göttingen: Goltze. p 81-87.
84. Razafindratsima OH, Mehtani S, Dunham AE,. 2013. Extinctions, traits and phylogenetic community structure: insights from primate assemblages in Madagascar. Ecography 36: 47-56.
85. Reed KE,. 1999. Population density of primates in communities: differences in community structure. In:, Fleagle JG, Janson CH, Reed KE, editors. Primate communities. Cambridge: Cambridge University Press. p 116-140.
86. Reed KE, Bidner LR,. 2004. Primate communities: past, present, and possible future. Yearb Phys Anthropol 47: 2-39.
87. Rex K, Czaczkes BI, Michener R, Kunz TH, Voigt CC,. 2010. Specialization and omnivory in diverse mammalian assemblages. Ecoscience 17: 37-46.
88. Sandberg PA, Loudon JE, Sponheimer M,. 2012. Stable isotope analysis in primatology: a critical review. Am J Primatol 74: 969-989.
89. Schäffler L,. 2011. Determinants of population structure in the world's smallest primate, Microcebus berthae, across its global range in Menabe Central, western Madagascar. PhD Thesis University of Göttingen.
90. Schliehe-Diecks S, Markolf M, Huchard E,. 2010. When big lemurs swallow up small ones: Coquerel's dwarf lemur as a predator of grey mouse lemurs and endemic rodents. Lemur News 15: 13-14.
91. Schoeninger MJ, DeNiro MJ,. 1984. Nitrogen and carbon isotopic composition of bone collagen from marine and terrestrial animals. Geochimica et Cosmochimica Acta 48: 625-639.
92. Schoeninger MJ, Iwaniec UT, Glander KE,. 1997. Stable isotope ratios indicate diet and habitat use in New World monkeys. Am J Physical Anthropol 103: 69-83. (Pubitemid 27240901)
93. Schoeninger MJ, Iwaniec UT, Nash LT,. 1998. Ecological attributes recorded in stable isotope ratios of arboreal prosimian hair. Oecologia 113: 222-230. (Pubitemid 28111424)
94. Schoeninger MJ, Moore J, Sept JM,. 1999. Subsistence strategies of two "Savanna" chimpanzee populations: the stable isotope evidence. Am J Primatol 49: 297-314. (Pubitemid 29523894)
95. Schreier BM, Harcourt AH, Coppeto SA, Somi MF,. 2009. Interspecific competition and niche separation in primates: a global analysis. Biotropica 41: 283-291.
96. Schülke O,. 2003. To breed or not to breed: food competition and other factors involved in female breeding decisions in the pair-living nocturnal fork-marked lemur (Phaner furcifer). Behav Ecol Sociobiol 55: 11-21. (Pubitemid 37399698)
97. Sorg JP, Ganzhorn JU, Kappeler PM,. 2003. Forestry and research in the Kirindy Forest / Centre de Formation Professionnelle Forestiére. In:, Goodman SM, Benstead JP, editors. The natural history of Madagascar. Chicago: University of Chicago Press. p 1512-1519.
98. Sorg JP, Rohner U,. 1996. Climate and tree phenology of the dry deciduous forest of the Kirindy Forest. In:, Sorg, JP, Ganzhorn JU, editors. Ecology and economy of a tropical dry forest in Madagascar. Göttingen: Goltze. p 57-80.
99. 15N in preserved ecological material. Rapid Commun Mass Spectrom 18: 2587-2592. (Pubitemid 39481714)
100. Thalmann U,. 2007. Biodiversity, phylogeography, biogeography and conservation: lemurs as an example. Folia Primatol 78: 420-443. (Pubitemid 47413401)
101. Tilman D,. 1982. Resource competition and community structure. Princeton, NJ: Princeton University Press.
102. Turner TF, Collyer ML, Krabbenhoft TJ,. 2010. A general hypothesis-testing framework for stable isotope ratios in ecological studies. Ecology 91: 2227-2233.
103. van Schaik CP, Kappeler PM,. 1996. The social systems of gregarious lemurs: lack of convergence with anthropoids due to evolutionary disequilibrium? Ethology 102: 915-941.
104. 15N enrichment: a meta-analysis. Oecologia 136: 169-182. (Pubitemid 36933250)
105. Vences M, Wollenberg KC, Vieites DR, Lees DC,. 2009. Madagascar as a model region of species diversification. Trends Ecol Evol 24: 456-465.
106. Waser PM,. 1987. Interactions among primate species. In:, Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate societies. Chicago: Chicago University Press.
107. West AG, Ayliffe LK, Cerling CE, Robinson TF, Karren B, Dearing MD, Ehleringer JR,. 2004. Short-term diet changes revealed using stable carbon isotopes in horse tail-hair. Funct Ecol 18: 616-624. (Pubitemid 39059422)
108. Wilmé L, Goodman SM, Ganzhorn JU,. 2006. Biogeographic evolution of Madagascar's microendemic biota. Science 312: 1063-1065.
109. Wright PC,. 1999. Lemur traits and Madagascar ecology: coping with an island environment. Yearb Phys Anthropol 42: 31-32.
110. Yoder AD, Cartmill M, Ruvolo M, Smith K, Vilgalys R,. 1996. Ancient single origin for Malagasy primates. Proc Natl Acad Sci 93: 5122-5126. (Pubitemid 26162881)