Skip to main content

The Evolutionary Morphology of Tree Gouging in Marmosets

  • Chapter
  • First Online:
The Smallest Anthropoids

Abstract

The marmosets, Callithrix spp. and Cebuella pygmaea, are unique among anthropoids in their habitual biting of trees with their anterior teeth to elicit exudate flow. This tree-gouging behavior is thought to offer certain ecological benefits to marmosets, such as routine access to an under-exploited resource, as well as have specific influences on their behavioral ecology.

In order to better understand morphological adaptations for tree gouging in the marmoset masticatory apparatus, we characterized the mechanics of this behavior in a laboratory setting and compared these data to field observations of common marmosets (Callithrix jacchus) in northeast Brazil. Common marmosets generate biting forces up to eight times their body mass when biting simulated tree substrates in the laboratory. When gouging, however, marmosets are not biting as forcefully as they can. Comparisons of the mechanical properties of laboratory substrates with trees gouged in the wild suggest that gouging forces observed in the laboratory are comparable to those that marmosets use during gouging in the wild. Moreover, marmosets use relatively wide jaw gapes during gouging both in the laboratory and in the wild. These wide jaw gapes during gouging approach the maximum structural capacity for jaw opening in common marmosets.

Morphological comparisons of masticatory apparatus form between gouging marmosets and nongouging tamarins corroborate these laboratory and field data. Marmosets do not exhibit morphologies that offer increased force generation or load resistance abilities. Furthermore, marmosets exhibit several morphologies of their masticatory apparatus that facilitate increased jaw opening. Previous suggestions that marmoset gouging involves relatively large bite forces likely misre­present the nature of this behavior. Instead, marmosets need only to score the tree bark to elicit the tree’s defense response of exudate flow.

Resumen

Los marmosets Callithrix spp. y Cebuella pygmea, son únicos entre los antropóides en su habitual mordisco en árboles con sus dientes anteriores para sacar corrientes exudadas. Este comportamiento de excavación de árboles se cree ofrece a ellos ciertos beneficios ecológicos, tal como el acceso rutinario a recursos poco utilizados, asi como tener influencias específicas en su comportamiento ecológico.

Con el propósito de entender adaptaciones morfológicas para excavar árboles en el aparato masticatorio de los marmoset, caracterizamos los mecanismos de dicho comportamiento en un laboratorio y comparamos nuestros datos de laboratorio con las observaciones de campo de Callithrix jacchus en el noreste de Brazil. Los Callithrix jacchus generan al morder hasta ocho veces su masa corporal al ser estimulados por substancias de árboles en el laboratorio. Sin embargo, al cavar, los C. jacchus no mordieron tan fuerte como ellos pueden. Comparaciones de las propiedades mecánicas de los substratos de laboratorio con árboles excavados en estado salvaje sugiere que las fuerzas de excavación observadas en el laboratorio son comparables con aquellos que los marmosets usarian durante la excavación en la selva. Alternativamente, los marmosets usan aperturas de mandíbulas relativamente amplias, medidas como la distancia entre las puntas incisivas superiores e inferiores, durante la excavación tanto en el laboratorio como en lo salvaje. Dichas aperturas de mandíbulas durante la excavación se acercan la capacidad máxima estructural de apertura de mandíbula en los marmosets comunes.

Comparaciones morfológicas de la forma de los aparatos masticatorios entre los marmosets excavadores y los tamarins no excavadores corroboran los datos de laboratorio y de campo. Los marmosets no muestran morfologías que ofrecen incremento en la generación de fuerza o habilidades de resistencia de carga. Alternativamente, los marmosets exhiben variadas morfologías en su aparato masticatorio que facilitan las habilidades de apertura de mandibula. Sugerencias anteriores de que la excavación marmoset muestra fuerzas de mordiscos relativamente grandes es probable que no representa la naturaleza de este comportamiento; los marmosets simplemente proponen marcar árboles para sacarle a los árboles su reacción de defensa.

Resumo

Os sagüis, Callithrix spp. and Cebuella pygmaea, são únicos entre os antropóides no hábito de morder as árvores com seus dentes anteriores para induzir o fluxo de exsudados. Este comportamento de perfurar o tronco das árvores é concebido como algo que ofereceria benefícios ecológicos aos sagüis, tais como o acesso rotineiro a recursos sub-explorados, assim como traria influências específicas na sua ecologia comportamental.

Para entender melhor estas adaptações morfológicas para perfuração de árvores no aparato mastigação dos sagüis, nós caracterizamos a mecânica deste comportamento em laboratório e comparamos estes dados à s observações de campo de sagüis (Callithrix jacchus) no nordeste do Brasil. Sagüis geram forças de mordida de até oito vezes as suas massas corporais quando mordem substratos de árvores simulados no laboratório. Quando perfuram o tronco, entretanto, os sagüis não mordem tão forte quanto poderiam. Comparações das propriedades mecânicas dos substratos de laboratório com as árvores perfuradas no campo sugerem que as forças de mordida observadas em laboratório são comparáveis aquelas que os sagüis devem empregar na perfuração dos troncos no campo. Ademais, os sagüis fazem aberturas da boca relativamente amplas durante a perfuração tanto no laboratório como no campo. Estas aberturas amplas durante a perfuração dos troncos se aproximam da capacidade de abertura máxima estrutural da mandíbula nos sagüis.

Comparações morfológicas do aparato de mastigação entre micos e sagüis que perfuram e que não perfuram troncos corroboram com estes dados de laboratório e do campo. Sagüis não apresentam morfologias que permitam um aumento na geração de força ou na capacidade de resistência à carga. Além disso, sagüis exibem várias morfologias do aparato de mastigação que facilitam um aumento da abertura da boca. Sugestões prévias de que a perfuração dos troncos nos sagüis envolvem forças de mordidas relativamente grandes foram provavelmente fruto de uma má interpretação da natureza deste comportamento. Ao invés disso, os sagüis precisam somente raspar a casca das árvores para estimular su a resposta de defesa sob a forma de um fluxo de exsudado.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Notes

  1. 1.

    The terms gummivory and exudativory have both been used to describe feeding on tree exudates. Nash (1986) discusses differences in these terms. We use them synonymously to include references applying either term as our interest is primarily related to the associated feeding behavior.

References

  • Ashby MF, Jones DRH (1980) Engineering materials 1: An introduction to their properties and applications. Pergamon Press, New York

    Google Scholar 

  • Chivers DJ, Hladik CM (1980) Morphology of the gastrointestinal tract in primates: comparisons with other mammals in relation to diet. J Morphol 166:337–386.

    Article  CAS  PubMed  Google Scholar 

  • Coimbra-Filho AF, Mittermeier RA (1977) Tree-gouging, exudate-eating and the “short-tusked” condition in Callithrix and Cebuella. In: Kleiman DG (ed) The biology and conservation of the Callitrichidae. Smithsonian Institution Press, Washington, DC, pp 105–115

    Google Scholar 

  • Coimbra-Filho AF, Da Cruz Rocha N, Pissinatti A (1980) Morfofisiologia do ceco e sua correlacao com o tipo odontologico em callitrichidae (Platyrrhini, Primates). Rev Brasil Biol 40:177–185

    CAS  PubMed  Google Scholar 

  • Coimbra-Filho AF, Mittermeier RA, Constable ID (1981) Callithrix flaviceps (Thomas, 1903) recorded from Minas Geraos. Brazil; (Callitrichidae, Primates). Rev Brasil Biol 40:177–185

    Google Scholar 

  • Daegling DJ (1993) The relationship of in vivo bone strain to mandibular corpus morphology in (Macaca fascicularis). J Hum Evol 25:247–269

    Article  Google Scholar 

  • de Faria DS (1983) Uso de arvores gomiferas do cerrado por Callithrix jacchus penicillata. In: Mello MT (ed) A primatologica no Brasil. Sociedade Brasileira de Primatologica, Belo Horizonte, pp 83–96

    Google Scholar 

  • Dumont ER (1997) Cranial shape in fruit, nectar, and exudate feeders: implications for interpreting the fossil record. Am J Phys Anthropol 102:187–202

    Article  CAS  PubMed  Google Scholar 

  • Ferrari SF (1993) Ecological differentiation in the Callitrichidae. In: Rylands AB (ed) Marmosets and tamarins: systematics, behaviour, and ecology. Oxford Univ Press, Oxford, pp 314–328

    Google Scholar 

  • Ferrari SF, Ferrari MA (1989) A re-evaluation of the social organisation of the Callitrichidae, with reference to the ecological differences between genera. Folia Primatol 52:132–147

    Article  CAS  PubMed  Google Scholar 

  • Fonseca GAB, Lacher TE (1984) Exudate-feeding by Callithrix jacchus penicillata in the semideciduous woodland (Cerradao) in Central Brazil. Primates 25:441–450

    Article  Google Scholar 

  • Garber PA (1980) Locomotor behavior and feeding ecology of the Panamanian tamarin (Saguinus oedipus geoffroyi, Callitrichidae). Int J Primatol 1:185–201

    Article  Google Scholar 

  • Garber PA (1984) Proposed nutritional importance of plant exudates in the diet of the Panamanian tamarin, Saguinus oedipus geoffroyi. Int J Primatol 5:1–15

    Article  CAS  Google Scholar 

  • Garber PA (1992) Vertical clinging, small body size, and the evolution of feeding adaptations in the Callitrichinae. Am J Phys Anthropol 88:469–482

    Article  CAS  PubMed  Google Scholar 

  • Garber PA, Rosenberger AL, Norconk MA (1996) Marmoset misconceptions. In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiation of neotropical primates. Plenum Press, New York, pp 87–95

    Google Scholar 

  • Hamrick MW (1998) Functional and adaptive significance of primate pads and claws: Evidence from New World anthropoids. Am J Phys Anthropol 106:113–127

    Article  CAS  PubMed  Google Scholar 

  • Harrison ML, Tardif SD (1994) Social implications of gummivory in marmosets. Am J Phys Anthropol 95:399–408

    Article  CAS  PubMed  Google Scholar 

  • Hershkovitz P (1977) Living New World primates (Platyrrhini), with an introduction to primates, vol 1. University Chicago Press, Chicago

    Google Scholar 

  • Izawa K (1975) Foods and feeding behavior of monkeys in the upper Amazon basin. Primates 16:295–316

    Article  Google Scholar 

  • Kinzey WG (1997) Callithrix. In: Kinzey WG (ed) New World primates: Ecology, evolution, and behavior. Aldine de Gruyter, New York, pp 230–239

    Google Scholar 

  • Kinzey WG, Rosenberger AL, Ramirez M (1975) Vertical clinging and leaping in a neotropical anthropoid. Nature 255:327–328

    Article  CAS  PubMed  Google Scholar 

  • Lacher TE, Fonseca GAB, Alves C, Magalhaes-Castro B (1981) Exudate-eating, scent-marking, and territoriality in wild populations of marmosets. Anim Behav 29:306–307

    Article  Google Scholar 

  • Lacher TE, Fonseca GAB, Alves C, Magalhaes-Castro B (1984) Parasitism of trees by marmosets in a central Brazilian gallery forest. Biotropica 16:202–209

    Article  Google Scholar 

  • Maier W, Alonso C, Langguth A (1982) Field observations of Callithrix jacchus jacchus. Zeits fur Saugetier 47:334–346

    Google Scholar 

  • Martin RD (1990) Primate origins and evolution: A phylogenetic reconstruction. Princeton University Press, Princeton

    Google Scholar 

  • Melo LCO (2001) Seleção de recursos alimentares por Callithrix jacchus – Sagui-do-Nordeste: Um foco sobre a teoria de Otimização. Masters Thesis, Univ Federal de Pernambuco

    Google Scholar 

  • Nash LT (1986) Dietary, behavioral, and morphological aspects of gumnivory in primates. Yrbk Phys Anthropol 29:113–137

    Article  Google Scholar 

  • Power ML (1996) The other side of Callitrichine gummivory. In: Norconk MA, Rosenberger AL, Garber PA (eds) Adaptive radiation of neotropical primates. Plenum, New York, pp 97–110

    Google Scholar 

  • Ramirez MF, Freese CH, Revilla J (1977) Feeding ecology of the pygmy marmoset, Cebuella pygmaea, in Northeastern Peru. In: Kleiman DG (ed) The biology and conservation of the Callitrichidae. Smithsonian Institution Press, Washington, DC, pp 91–104

    Google Scholar 

  • Rosenberger AL (1978) Loss of incisor enamel in marmosets. J Mamm 59:207–208

    Article  Google Scholar 

  • Rosenberger AL (1992) Evolution of feeding niches in New World monkeys. Am J Phys Anthropol 88:525–562

    Article  CAS  PubMed  Google Scholar 

  • Rylands AB (1981) Preliminary field observations on the marmoset, Callithrix humeralifer intermedius (Hershkovitz, 1977) at Dardanelos, Rio Aripuana, Mato Grosso. Primates 22:46–59

    Article  Google Scholar 

  • Rylands AB (1984) Exudate-eating and tree-gouging by marmosets (Callitrichidae, Primates). In: Chadwick AC, Sutton SL (eds) Tropical rain forest: The leeds symposium. Leeds Philosophical and Literary Society, Leeds, pp 155–168

    Google Scholar 

  • Rylands AB, de Faria DS (1993) Habitats, feeding ecology, and home range size in the genus Callithrix. In: Rylands AB (ed) Marmosets and tamarins: Systematics, behaviour, and ecology. Oxford University Press, Oxford, pp 262–272

    Google Scholar 

  • Soini P (1982) Ecology and population dynamics of the pygmy marmoset, Cebuella pygmaea. Folia Primatol 39:1–21

    Article  CAS  PubMed  Google Scholar 

  • Soini P (1987) Ecology of the saddle-back tamarin Saguinus fuscicollis illigeri on the Rio Pacaya, northeastern Peru. Folia Primatol 49:11–32

    Article  Google Scholar 

  • Spencer MA (1999) Constraints on masticatory system evolution in anthropoid primates. Am J Phys Anthropol 108:483–506

    Article  CAS  PubMed  Google Scholar 

  • Stevenson MF, Rylands AB (1988) The marmosets, Genus Callithrix. In: Mittermeier RA, Rylands AB, Coimbra-Filho AF, Fonseca GAB (eds) Ecology and behavior of neotropical primates. World Wildlife Fund, Washington, DC, pp 131–222

    Google Scholar 

  • Sussman RW, Kinzey WG (1984) The ecological role of the Callitrichidae: A review. Am J Phys Anthropol 64:419–449

    Article  CAS  PubMed  Google Scholar 

  • Szalay FS, Seligsohn D (1977) Why did the strepsirhine tooth comb evolve? Folia Primatol 27:75–82

    Article  CAS  PubMed  Google Scholar 

  • Taylor AB, Vinyard CJ (2004) Comparative analysis of masseter fiber architecture in tree-gouging (Callithrix jacchus) and nongouging (Saguinus oedipus) callitrichids. J Morphol 261:276–285

    Article  PubMed  Google Scholar 

  • Taylor AB, Vinyard CJ (2008) The relationship between jaw-muscle fiber architecture and feeding behavior in primates. Tree-gouging and nongouging gummivorous callitrichids as a natural experiment. In: Vinyard CJ, Ravosa MJ. Wall CE (eds) Primate Craniofacial Function and Biology, p. 241–264. New York: Springer

    Google Scholar 

  • Taylor AB, Eng EM, Anapol FC, Vinyard CJ (this volume) The functional significance of jaw-muscle fiber architecture in tree-gouging marmosets. In: Ford SM, Porter LM, Davis LC (eds) The smallest anthropoids: The marmoset/callimico radiation. Springer Press, New York, (this volume)

    Google Scholar 

  • Vinyard CJ, Ryan TM (2006) Cross-sectional bone distribution in the mandibles of gouging and non-gouging platyrrhines. Int J Primatol 27:1461–1490

    Article  Google Scholar 

  • Vinyard CJ, Schmitt D (2004) A new technique for studying reaction forces during primate behaviors on vertical substrates. Am J Phys Anthropol 125:343–351

    Article  PubMed  Google Scholar 

  • Vinyard CJ, Wall CE, Williams SH, Schmitt D, Hylander WL (2001) A preliminary report on the jaw mechanics during tree gouging in common marmosets (Callithrix jacchus). In: Brooks A (ed) Dental Morphology 2001: Proceedings of the 12th international symposium on dental morphology. Sheffield Academic Press, Ltd., Sheffield UK, pp 283–297

    Google Scholar 

  • Vinyard CJ, Wall CE, Williams SH, Hylander WL (2003) A comparative functional analysis of the skull morphology of tree gouging primates. Am J Phys Anthropol 120:153–170

    Article  PubMed  Google Scholar 

  • Vinyard CJ, Lucas PW, Valença-Montenegro MM, Melo LCO, Valle YM, Monteiro da Cruz MAO (2004) Where the wild things are: Linking lab and field work in studying tree gouging in common marmosets (Callithrix jacchus). Am J Phys Anthropol 38(Suppl):200–201

    Google Scholar 

  • Yepez P, de la Torre S, Snowdon CT (2005) Interpopulation differences in exudate feeding of pygmy marmosets in Ecuadorian Amazonia. Am J Primatol 66:145–158

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Susan Ford, Lesa Davis and Leila Porter for inviting us to contribute to this volume and participate in the symposium “Advances in Marmoset and Goeldi’s Monkey (Callimico) Research: Anatomy, Behavioral Ecology, Phylogeny, and Conservation” held at the American Association of Physical Anthropologists Meetings on April 8, 2005. We also thank B. Darvell, W. Horne, P. Lemelin and P. Vinyard for assistance and advice. This research was supported by grants from NSF (BCS-0094666), (BCS-0412153), (SBR-9701425), (SBR-940764), (BCS-99-04401), the L.S.B. Leakey Foundation, and the National Geographic Society.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Christopher J. Vinyard .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Vinyard, C.J. et al. (2009). The Evolutionary Morphology of Tree Gouging in Marmosets. In: Ford, S., Porter, L., Davis, L. (eds) The Smallest Anthropoids. Developments in Primatology: Progress and Prospects. Springer, Boston, MA. https://doi.org/10.1007/978-1-4419-0293-1_20

Download citation

Publish with us

Policies and ethics