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Apparent Competition Structures Ecological Assemblages

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Apparent Competition Structures Ecological Assemblages letters to nature 20. Leakey, R. E. & Leakey, M. G. A new Miocene hominoid from Kenya. Nature 342, 143–146 (1986). 21. Leakey, M. G., Leakey, R. E., Richtsmeier, J. T., Simons, E. L. & Walker, A. C. Similarities in Aegyptopithecus and Afropithecus facial morphology. Folia Primatol. 56, 65–85 (1991). 22. Delson, E. & Andrews, P.in Phylogeny of the Primates: A Multidisciplinary Approach (eds Luckett, W. P. & Szalay, F. S.) 405–446 (Plenum, New York, 1975). 23. Strasser, E. & Delson, E. Cladistic analysis of cercopithecid relationships. J. Hum. Evol. 16, 81–99 (1987). Acknowledgements. Excavations at Maboko were conducted with permission of the Office of the President, Republic of Kenya and in collaboration with the National Museums of Kenya. We thank the field crew (especially B. Onyango, V. Oluoch and S. Gitau) and M. G. Leakey for assistance, and E. Delson, M. Kohler, S. Moya-Sola and D. Pilbeam for comments and advice. This work was supported by NSF, L. S. B. Leakey Foundation, National Geographic Society, Wenner Gren Foundation for Anthropological Research, Fulbright, and Boise Fund. Correspondence and requests for materials should be addressed to B.R.B. (e-mail: bbenefi[email protected]). Apparent competition structures ecological assemblages M. B. Bonsall & M. P. Hassell Department of Biology and the NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, UK ......................................................................................................................... Competition is a major force in structuring ecological com- munities1. It acts directly2 or indirectly, in which case it may be mediated by shared natural enemies and is known as ‘apparent 3–6 Figure 3 Bivariate plot of log10-transformed mean brain and body weight data for competition’ . The effects of apparent competition on species extant hominoids (H), cercopithecoids (C), platyrrhines (P), tarsiers (T), lemuroids coexistence are well known theoretically7,8 but have not previously and lorisoids (L)14, Victoriapithecus and Aegyptopithecus. Superimposed best fit been demonstrated empirically in controlled multigenerational lines for extant anthropoids (higher) and strepsirhines (lower) are based on least- experiments. Here we report on the population dynamic conse- squares linear regression equations. quences of apparent competition in a laboratory insect system with two host species and a common parasitoid attacking them. We find that whereas the two separate, single host–single para- catarrhine features, rather than derived indicators of affinity with sitoid interactions are persistent, the three-species system with the great ape and human clade. In this way, the Victoriapithecus skull the parasitoid attacking both hosts species (which are not allowed shows that the anatomy of fossil cercopithecoids is as important as to compete directly) is unstable, and that one of the host species is that of hominoids for deciphering the evolutionary history of Old eliminated from the interaction owing to the effects of apparent World higher primates. M competition. Received 21 November 1996; accepted 30 May 1997 Classical ecological theory predicts that simple interactions in 1. Pilbeam, D. R. New hominoid skull material from the Miocene of Pakistan. Nature 295, 232–234 which species share common natural enemies are unstable, leading 9 (1982). to one species being eliminated from the interaction . This effect 2. Brown, B. & Ward, S. in Orang-utan Biology (ed. Schwartz, J. H.) 247–260 (Oxford Univ. Press, New arises through competitive interactions mediated by the natural York, 1988). 7,8 3. Moya-Sola, S. & Kohler, M. Recent discoveries of Dryopithecus shed new light on evolution of great enemy in ‘apparent competition’ . As the two host species are not apes. Nature 365, 543–545 (1993). directly competing for resources, the loss of one of the species results 4. Moya-Sola, S. & Kohler, M. New partial cranium of Dryopithecus Lartet, 1863 (Hominoidea, Primates) from the upper Miocene of Can Llobateres, Barcelona, Spain. J. Hum. Evol. 29, 101–139 solely from the dynamic consequences of the natural enemy (1995). becoming more abundant as a consequence of having an alternative 5. Von Koenigswald, G. H. R. Miocene Cercopithecoidea and Oreopithecoidea from the Miocene of East host species. The species that persists in the interaction is the one Africa. Foss. Vert. Afr. 1, 39–51 (1969). 6 6. Benefit, B. R. & McCrossin, M. L. Ancestral facial morphology of Old World higher primates. Proc. that can support the higher parasitoid density . Natl Acad. Sci. USA 88, 5267–5271 (1991). These indirect competitive interactions have received little atten- 7. Benefit, B. R. The permanent dentition and phylogenetic position of Victoriapithecus from Maboko Island, Kenya. J. Hum. Evol. 25, 83–172 (1993). tion from natural or laboratory systems, although they are likely to 8. Benefit, B. R. Phylogenetic, paleodemographic and taphonomic implications of Victoriapithecus be as important, if not more so, than direct competitive interac- deciduous teeth from Maboko, Kenya. Am. J. Phys. Antropol. 95, 277–331 (1994). tions. Empirical work so far has focused mainly on short-term, 9. Feibel, C. S. & Brown, F. H. Age of the primate-bearing deposits on Maboko Island, Kenya. J. Hum. Evol. 21, 221–225 (1991). behaviourally orientated studies in which natural enemy responses 10. Andrews, P., Meyer, G., Pilbeam, D. R., Van Couvering, J. A. & Van Couvering, J. A. H. The Miocene are recorded within a single field season of the interaction10–15.No fossil beds of Maboko Island, Kenya: Geology, age, taphonomy and paleontology. J. Hum. Evol. 10, 35–48 (1981). empirical studies have addressed directly the long-term effects of 11. Stromer, E. Mitteilungen uber die Wirbeltierreste aus dem Mittelpliocan des Natrontales (Agypten). apparent competition on the population dynamics of the interact- 1. Affen. Z. Deutsch. Geol. Gesell. Abh. 65, 349–361 (1913). ing organisms. We now report on the temporal consequences of 12. Harrison, T. New postcranial remains of Victoriapithecus from the middle Miocene of Kenya. J. Hum. Evol. 18, 3–54 (1989). such apparent competition (Figs 1, 2). A series of long-term 13. Radinsky, L. The fossil evidence of anthropoid brain evolution. Am.J.Phys.Anthropol.41, 15–28 (1974). laboratory experiments were used to explore the interaction 14. Martin, R. D. Primate Origins and Evolution (Princeton Univ. Press, Princeton, NJ, 1990). 15. Benefit, B. R. & McCrossin, M. L. The facial anatomy of Victoriapithecus and its relevance to the between the ichneumonid parasitic wasp Venturia canescens ancestral cranial morphology of Old World monkeys and apes. Am.J.Phys.Anthropol.92, 329–370 (1993). (Gravenhorst) and two of its moth hosts, Plodia interpunctella 16. Vogel, C. Morphologische studien am gesichtschadel Catarrhiner primaten. Biblio Primatol. 4, 1–226 (Hubner) and Ephestia kuehniella Zeller, over a period of several (1966). 17. Harrison, T. The phylogenetic relationships of the early catarrhine primates: A review of the current generations. The direct competitive effects between the host evidence. J. Hum. Evol. 16, 41–80 (1987). species were fully excluded by a vertical barrier of nylon mesh 18. Simons, E. L. The earliest apes. Sci. Am. 217, 28–35 (1967). 19. Simons, E. L. New faces of Aegyptopithecus from the Oligocene of Egypt. J. Hum. Evol. 16, 273–289 dividing each cage in half. The mesh size was large enough to (1987). allow free access for the searching parasitoids between the two NATURE | VOL 388 | 24 JULY 1997 Nature © Macmillan Publishers Ltd 1997 371 letters to nature Figure 1 Representative examples of the population dynamics of the single host-single parasitoid interac- tions: a, b, P.interpunctella (dotted line)–V. canescens (dashed line); c, d, E. kuehniella (unbroken line)–V. canescens (dashed line). Experiments were carried in cages (30 3 30 3 30 cm) under standard environmen- tal conditions (25 6 2 8C; 70 6 5% R.H. 16 : 8 h light– dark cycle). Linear time series analysis indicates an underlying tendency for oscillations dampening towards a stable equilibrium. Figure 2 Representative examples of the population dynamics of the three species system of two hosts and a single parasitoid: P. interpunctella (dotted line)–E. kuehniella (unbroken line)–V. canescens (dashed line). In all these cases, E. kuehniella is eliminated from the interaction by the action of the shared natural enemy, V. canescens. Time series analysis now indicates damped oscillations for the interaction between P. interpunctella and V. canescens and diverging oscillations for E. kuehniella. halves, but was too small to let the hosts pass through. The between the two apparently competing host species (P. interpunc- interactions with a single host and single parasitoid, and the more tella and E. kuehniella) is amensal: the effect of P. interpunctella on E. complex three-species interactions of two hosts and a single kuehniella is strong whereas the reciprocal effects of E. kuehniella on parasitoid, were each replicated eight times and monitored over P. interpunctella is negligible (Fig. 3). P. interpunctella is dominant 15 generations by weekly census counts of dead adults16. because it has a larger intrinsic rate of increase and shorter In all the two-species systems, the two populations persisted in development time16. relatively stable interactions (Fig. 1). Time-series statistics show that Such asymmetric relationships in the interaction strengths have the dynamics in these cases
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