Information transfer through food from parents to offspring in wild Javan gibbons.

Yoonjung Yi, Yena Kim, Agus Hikmat, Jae C Choe
Author Information
  1. Yoonjung Yi: Laboratory of Behavioral Ecology, Interdisciplinary Program of EcoCreative, Ewha Womans University, Seoul, 03760, Republic of Korea. ORCID
  2. Yena Kim: Cognitive Psychology Unit, Institute of Psychology, Leiden University, 2333 AK, Leiden, the Netherlands.
  3. Agus Hikmat: Department of Forest Resources Conservation and Ecotourism, Faculty of Forestry, Bogor Agricultural University, Bogor, 16680, West Java, Indonesia.
  4. Jae C Choe: Laboratory of Behavioral Ecology, Department of Life Sciences and Division of EcoScience, Ewha Womans University, Seoul, 03760, Republic of Korea. jaechoe@ewha.ac.kr.

Abstract

The adaptive functions of food transfer from parents to their offspring have been explained mainly by two mutually non-exclusive hypotheses: the nutritional and informational hypotheses. In this study, we examined the functions of food transfer in wild Javan gibbons (Hylobates moloch) by testing these hypotheses from both infants' and mothers' perspectives. We observed 83 cases of food solicitations that resulted in 54 occasions of food transfers in three groups over a 19-month period in Gunung Halimun-Salak National Park, Indonesia. Infants initiated all solicitations directed at their mothers with one solicitation towards a father. Food solicitation rate decreased as infant age increased and ceased before weaning. As predicted by the informational hypothesis, infants solicited more food items difficult to obtain and preferred by their parents. On the contrary to the nutritional hypothesis, infants solicited low-quality items more often than high-quality items. Mothers did not change probability of food transfer according to the food characteristics or infant age. Hence, our results suggest that the primary function of food transfer from mother to infant Javan gibbons seems to be information transfer rather than nutritional aids, similarly to great apes.

References

  1. Jaeggi, A. V. & Gurven, M. Natural cooperators: food sharing in humans and other primates. Evolutionary anthropology 22, 186–195, https://doi.org/10.1002/evan.21364 (2013). [DOI: 10.1002/evan.21364]
  2. Jaeggi, A. V. & van Schaik, C. P. The evolution of food sharing in primates. Behavioral Ecology and Sociobiology 65, 2125 (2011). [DOI: 10.1007/s00265-011-1221-3]
  3. Feistner, A. T. & McGrew, W. C. Food-sharing in primates: a critical review. Perspectives in primate biology 3, 21–36 (1989).
  4. Silk, J. B. Patterns of food sharing among mother and infant chimpanzees at Gombe National Park, Tanzania. Folia primatologica 29, 129–141 (1978). [DOI: 10.1159/000155835]
  5. Lefebvre, L. Parent-offspring food sharing: a statistical test of the early weaning hypothesis. Journal of Human Evolution 14, 255–261 (1985). [DOI: 10.1016/S0047-2484(85)80066-X]
  6. Price, E. C. & Feistner, A. T. Food sharing in lion tamarins: tests of three hypotheses. American Journal of Primatology 31, 211–221 (1993). [DOI: 10.1002/ajp.1350310306]
  7. Brown, G. R., Almond, R. E. & van Bergen, Y. Begging, stealing, and offering: food transfer in nonhuman primates. Advances in the Study of Behavior 34, 265–295 (2004). [DOI: 10.1016/S0065-3454(04)34007-6]
  8. Jaeggi, A. V., van Noordwijk, M. A. & van Schaik, C. P. Begging for information: mother–offspring food sharing among wild Bornean orangutans. American Journal of Primatology 70, 533–541 (2008). [PMID: 18186082]
  9. Heymann, E. W. Social behavior of wild moustached tamarins, Saguinus mystax, at the Estación Biológica Quebrada Blanco, Peruvian Amazonia. American Journal of Primatology 38, 101–113 (1996). [PMID: 31914710]
  10. Izawa, K. A field study of the ecology and behavior of the black-mantle tamarin (Saguinus nigricollis). Primates 19, 241–274 (1978). [DOI: 10.1007/BF02382796]
  11. Ferrari, S. F. Food transfer in a wild marmoset group. Folia Primatologica (1987).
  12. Tardif, S. D. & Ross, C. N. Integration of proximate and evolutionary explanation of reproductive strategy: the case of callitrichid primates and implications for human biology. American Journal of Human Biology: The Official Journal of the Human Biology Association 21, 731–738 (2009). [DOI: 10.1002/ajhb.20932]
  13. Ziegler, T. E. et al. Detection of the chemical signals of ovulation in the cotton-top tamarin, Saguinus oedipus. Animal Behaviour 45, 313–322 (1993). [DOI: 10.1006/anbe.1993.1036]
  14. Dunbar, R. The mating system of callitrichid primates: I. Conditions for the coevolution of pair bonding and twinning. Animal Behaviour 50, 1057–1070 (1995). [DOI: 10.1016/0003-3472(95)80106-5]
  15. Garber, P. A. & Leigh, S. R. Ontogenetic variation in small-bodied New World primates: implications for patterns of reproduction and infant care. Folia Primatologica 68, 1–22 (1997). [DOI: 10.1159/000157226]
  16. Ross, C. & MacLarnon, A. The evolution of non-maternal care in anthropoid primates: a test of the hypotheses. Folia Primatologica 71, 93–113 (2000). [DOI: 10.1159/000021733]
  17. Hoage, R. J. Social and physical maturation in captive lion tamarins, Leontopithecus rosalia rosalia (Primates: Callitrichidae). Vol. 354 (Smithsonian Contributions to Zoology, 1982).
  18. Feistner, A. T. & Price, E. C. Food sharing in black lion tamarins (Leontopithecus chrysopygus). American Journal of Primatology 52, 47–54 (2000). [PMID: 10993137]
  19. Galdikas, B. M. & Wood, J. W. Birth spacing patterns in humans and apes. American Journal of Physical Anthropology 83, 185–191 (1990). [PMID: 2248378]
  20. Ruiz‐Miranda, C. R. et al. Food transfers in wild and reintroduced golden lion tamarins, Leontopithecus rosalia. American Journal of Primatology 48, 305–320 (1999). [PMID: 10402039]
  21. Corp, N. & Byrne, R. W. Leaf processing by wild chimpanzees: Physically defended leaves reveal complex manual skills. Ethology 108, 673–696 (2002). [DOI: 10.1046/j.1439-0310.2002.00801.x]
  22. Nowell, A. A. & Fletcher, A. W. Food transfers in immature wild western lowland gorillas (Gorilla gorilla gorilla). Primates 47, 294–299 (2006). [PMID: 16596463]
  23. Hiraiwa-Hasegawa, M. In The chimpanzees of Mahale mountains 267–275 (Tokyo University Press, 1990).
  24. Nishida, T. & Turner, L. A. Food transfer between mother and infant chimpanzees of the Mahale Mountains National Park, Tanzania. International journal of primatology 17, 947–968 (1996). [DOI: 10.1007/BF02735296]
  25. Laska, M., Salazar, L. T. H. & Luna, E. R. Food preferences and nutrient composition in captive spider monkeys, Ateles geoffroyi. International Journal of Primatology 21, 671–683 (2000). [DOI: 10.1023/A]
  26. Ganas, J., Ortmann, S. & Robbins, M. M. Food preferences of wild mountain gorillas. American Journal of Primatology 70, 927–938 (2008). [PMID: 18567010]
  27. van de Waal, E., Borgeaud, C. & Whiten, A. Potent social learning and conformity shape a wild primate’s foraging decisions. Science 340, 483–485 (2013). [PMID: 23620053]
  28. Bilkó, Á., Altbäcker, V. & Hudson, R. Transmission of food preference in the rabbit: the means of information transfer. Physiology & Behavior 56, 907–912 (1994). [DOI: 10.1016/0031-9384(94)90322-0]
  29. Galef, B. G. & Giraldeau, L.-A. Social influences on foraging in vertebrates: causal mechanisms and adaptive functions. Animal behaviour 61, 3–15 (2001). [PMID: 11170692]
  30. Melo, A. I. et al. Maternal and littermate deprivation disrupts maternal behavior and social‐learning of food preference in adulthood: Tactile stimulation, nest odor, and social rearing prevent these effects. Developmental psychobiology 48, 209–219 (2006). [PMID: 16568415]
  31. Hikami, K., Hasegawa, Y. & Matsuzawa, T. Social transmission of food preferences in Japanese monkeys (Macaca fuscata) after mere exposure or aversion training. Journal of Comparative Psychology 104, 233 (1990). [PMID: 2225760]
  32. Brosnan, S. F. & de Waal, F. Socially learned preferences for differentially rewarded tokens in the brown capuchin monkey (Cebus apella). Journal of Comparative Psychology 118, 133 (2004). [PMID: 15250800]
  33. Marshall, A. J. & Wrangham, R. W. Evolutionary consequences of fallback foods. International Journal of Primatology 28, 1219 (2007). [DOI: 10.1007/s10764-007-9218-5]
  34. Trivers, R. L. Parent-offspring conflict. Integrative and Comparative Biology 14, 249–264 (1974).
  35. Schessler, T. & Nash, L. T. Food sharing among captive gibbons (Hylobates lar). Primates 18, 677–689 (1977). [DOI: 10.1007/BF02383142]
  36. Nettelbeck, A. R. Observations on food sharing in wild lar gibbons (Hylobates lar). Folia Primatologica 69, 386–391 (1998). [DOI: 10.1159/000021658]
  37. Fan, P.-f. & Jiang, X.-l. Predation on giant flying squirrels (Petaurista philippensis) by black crested gibbons (Nomascus concolor jingdongensis) at Mt. Wuliang, Yunnan, China. Primates 50, 45–49 (2009). [PMID: 19015936]
  38. Berkson, G. & Schusterman, R. J. Reciprocal food sharing of gibbons. Primates 5, 1–10 (1964). [DOI: 10.1007/BF01758272]
  39. Treesucon, U. Social development of young gibbons (Hylobates lar) in Khao Yai National Park. Master thesis thesis, Mahidol University (1984).
  40. Reichard, U. H. & Barelli, C. Life history and reproductive strategies of Khao Yai Hylobates lar: implications for social evolution in apes. International Journal of Primatology 29, 823–844 (2008). [DOI: 10.1007/s10764-008-9285-2]
  41. Brockelman, W. Y., Reichard, U., Treesucon, U. & Raemaekers, J. J. Dispersal, pair formation and social structure in gibbons (Hylobates lar). Behavioral Ecology and Sociobiology 42, 329–339 (1998). [DOI: 10.1007/s002650050445]
  42. Geissmann, T. Reassessment of age of sexual maturity in gibbons (Hylobates spp.). American Journal of Primatology 23, 11–22 (1991). [DOI: 10.1002/ajp.1350230103]
  43. Dal Pra, G. & Geissmann, T. Behavioural development of twin siamangs (Hylobates syndactylus). Primates 35, 325–342 (1994). [DOI: 10.1007/BF02382729]
  44. Fischer, J. O. & Geissmann, T. Group harmony in gibbons: Comparison between white-handed gibbon (Hylobates lar) and siamang (H. syndactylus). Primates 31, 481–494 (1990). [DOI: 10.1007/BF02382532]
  45. Parker, S. T. & Gibson, K. R. Object manipulation, tool use and sensorimotor intelligence as feeding adaptations in Cebus monkeys and great apes. Journal of Human Evolution 6, 623–641 (1977). [DOI: 10.1016/S0047-2484(77)80135-8]
  46. Malone, N. & Fuentes, A. In The Gibbons 241–264 (Springer, 2009).
  47. Marshall, A. J., Cannon, C. H. & Leighton, M. In The Gibbons 161–188 (Springer, 2009).
  48. Kim, S., Lappan, S. & Choe, J. C. Responses of Javan Gibbon (Hylobates moloch) Groups in Submontane Forest to Monthly Variation in Food Availability: Evidence for Variation on a Fine Spatial Scale. American journal of primatology 74, 1154–1167 (2012). [PMID: 22972588]
  49. Berkson, G. Development of an infant in a captive gibbon group. The Journal of genetic psychology 108, 311–325 (1966). [PMID: 4960212]
  50. Roush, R. S. & Snowdon, C. T. Food transfer and development of feeding behavior and food‐associated vocalizations in cotton‐top tamarins. Ethology 107, 415–429 (2001). [DOI: 10.1046/j.1439-0310.2001.00670.x]
  51. Sacchi, R., Saino, N. & Galeotti, P. Features of begging calls reveal general condition and need of food of barn swallow (Hirundo rustica) nestlings. Behavioral Ecology 13, 268–273 (2002). [DOI: 10.1093/beheco/13.2.268]
  52. Joyce, S. M. & Snowdon, C. T. Developmental changes in food transfers in cotton‐top tamarins (Saguinus oedipus). American Journal of Primatology: Official Journal of the American Society of Primatologists 69, 955–965 (2007). [DOI: 10.1002/ajp.20393]
  53. Iacovides, S. & Evans, R. M. Begging as graded signals of need for food in young ring-billed gulls. Animal Behaviour 56, 79–85 (1998). [PMID: 9710464]
  54. Schuppli, C. et al. Development of foraging skills in two orangutan populations: needing to learn or needing to grow? Frontiers in zoology 13, 43 (2016). [PMID: 27708679]
  55. Janson, C. H. In Juvenile primates: life history, development, behavior (ed. Fairbanks Mepala) 57–74 (Oxford University Press, 1993).
  56. Boesch, C. & Boesch-Achermann, H. The chimpanzees of the Taï Forest: Behavioural ecology and evolution. (Oxford University Press, USA, 2000).
  57. Tarnaud, L. Ontogeny of feeding behavior of Eulemur fulvus in the dry forest of Mayotte. International Journal of Primatology 25, 803–824 (2004). [DOI: 10.1023/B]
  58. Schiel, N., Souto, A., Huber, L. & Bezerra, B. M. Hunting strategies in wild common marmosets are prey and age dependent. American journal of primatology 72, 1039–1046 (2010). [PMID: 20623501]
  59. Matsuzawa, T. In Chimpanzee cultures (eds. Richard W Wrangham, William C McGrew, Frans B. M de Waal, & Paul G Heltne) (Harvard University Press, 1994).
  60. Boesch, C. & Boesch, H. Tool use and tool making in wild chimpanzees. Folia primatologica 54, 86–99 (1990). [DOI: 10.1159/000156428]
  61. Inoue-Nakamura, N. & Matsuzawa, T. Development of stone tool use by wild chimpanzees (Pan troglodytes). Journal of comparative psychology 111, 159 (1997). [PMID: 9170281]
  62. van Schaik, C. P. et al. Orangutan cultures and the evolution of material culture. Science 299, 102–105 (2003). [PMID: 12511649]
  63. Fragaszy, D., Izar, P., Visalberghi, E., Ottoni, E. B. & de Oliveira, M. G. Wild capuchin monkeys (Cebus libidinosus) use anvils and stone pounding tools. American Journal of Primatology 64, 359–366 (2004). [PMID: 15580579]
  64. Cheyne, S. M. In Primate Locomotion. Developments in Primatology: Progress and Prospects. (eds. D’Août, K. & Vereecke, E.) 201–213 (Springer, 2011).
  65. Feistner, A. T. & Chamove, A. High motivation toward food increases food‐sharing in cotton‐top tamarins. Developmental psychobiology 19, 439–452 (1986). [PMID: 3093299]
  66. Kopp, K. S. & Liebal, K. Here you are!—Selective and active food sharing within and between groups in captive Sumatran orangutans (Pongo abelii). Behavioral ecology and sociobiology 70, 1219–1233 (2016). [DOI: 10.1007/s00265-016-2130-2]
  67. Pusey, A. E. Mother-offspring relationships in chimpanzees after weaning. Animal Behaviour 31, 363–377 (1983). [DOI: 10.1016/S0003-3472(83)80055-4]
  68. Assersohn, C. & Whiten, A. Food sharing between mother and infant chimpanzees in the wild: Beggars can be choosers. Folia Primatologica 70, 226 (1999).
  69. Russon, A. E. Developmental perspectives on great ape traditions. The biology of traditions: models and evidence. Cambridge University Press, Cambridge, 329–364 (2003). [DOI: 10.1017/CBO9780511584022.013]
  70. Caldwell, C. A. & Whiten, A. Scrounging facilitates social learning in common marmosets, Callithrix jacchus. Animal Behaviour 65, 1085–1092 (2003). [DOI: 10.1006/anbe.2003.2145]
  71. Kim, S., Lappan, S. & Choe, J. C. Diet and ranging behavior of the endangered Javan gibbon (Hylobates moloch) in a submontane tropical rainforest. American Journal of Primatology 73, 270–280 (2011). [PMID: 20938967]
  72. Altmann, J. Observational study of behavior: sampling methods. Behaviour 49, 227–266 (1974). [PMID: 4597405]
  73. Blurton Jones, N. G. Tolerated theft, suggestions about the ecology and evolution of sharing, hoarding and scrounging. Social Science Information 26, 31–54 (1987). [DOI: 10.1177/053901887026001002]
  74. Jaeggi, A. V., Burkart, J. M. & Van Schaik, C. P. On the psychology of cooperation in humans and other primates: combining the natural history and experimental evidence of prosociality. Philosophical Transactions of the Royal Society B: Biological Sciences 365, 2723–2735 (2010). [DOI: 10.1098/rstb.2010.0118]
  75. McConkey, K. R., Ario, A., Aldy, F. & Chivers, D. J. Influence of forest seasonality on gibbon food choice in the rain forests of Barito Ulu, Central Kalimantan. International Journal of Primatology 24, 19–32 (2003). [DOI: 10.1023/A]
  76. R Development Core Team. R: A language and environment for statistical computing. Vienna, Austria: R foundation for Statistical Computing. Retrieved from http://www.R-project.org (2018).
  77. Barr, D. J., Levy, R., Scheepers, C. & Tily, H. J. Random effects structure for confirmatory hypothesis testing: Keep it maximal. Journal of memory language 68, 255–278 (2013). [DOI: 10.1016/j.jml.2012.11.001]
  78. Fox, J. et al. Package ‘car’. Vienna: R Foundation for Statistical Computing (2012).
  79. Forstmeier, W. & Schielzeth, H. Cryptic multiple hypotheses testing in linear models: overestimated effect sizes and the winner’s curse. Behavioral Ecology & Sociobiology 65, 47–55 (2011). [DOI: 10.1007/s00265-010-1038-5]
  80. Magnusson, A. et al. Package ‘glmmTMB’ (2017).

MeSH Term

Animals
Animals, Wild
Behavior, Animal
Feeding Behavior
Female
Food
Hylobates
Indonesia
Male
Maternal Behavior

Word Cloud

Created with Highcharts 10.0.0foodtransferparentsnutritionalJavangibbonsinfantitemsfunctionsoffspringinformationalhypotheseswildsolicitationssolicitationagehypothesisinfantssolicitedadaptiveexplainedmainlytwomutuallynon-exclusivehypotheses:studyexaminedHylobatesmolochtestinginfants'mothers'perspectivesobserved83casesresulted54occasionstransfersthreegroups19-monthperiodGunungHalimun-SalakNationalParkIndonesiaInfantsinitiateddirectedmothersonetowardsfatherFoodratedecreasedincreasedceasedweaningpredicteddifficultobtainpreferredcontrarylow-qualityoftenhigh-qualityMotherschangeprobabilityaccordingcharacteristicsHenceresultssuggestprimaryfunctionmotherseemsinformationratheraidssimilarlygreatapesInformation

Similar Articles

Cited By