Hostname: page-component-586b7cd67f-r5fsc Total loading time: 0 Render date: 2024-11-25T23:16:58.909Z Has data issue: false hasContentIssue false

Predation on exposed and leaf-rolling artificial caterpillars in tropical forests of Papua New Guinea

Published online by Cambridge University Press:  01 June 2012

Katerina Tvardikova*
Affiliation:
Faculty of Science, University of South Bohemia and Biology Center, Czech Academy of Sciences, Branisovska 31/1160, 370 05 Ceske Budejovice, Czech Republic
Vojtech Novotny
Affiliation:
Faculty of Science, University of South Bohemia and Biology Center, Czech Academy of Sciences, Branisovska 31/1160, 370 05 Ceske Budejovice, Czech Republic
*
1Corresponding author. Email: [email protected]

Abstract:

Although predation is generally seen as one of the key factors determining the abundance and composition of insect herbivore communities in tropical rain forests, quantitative estimates of predation pressure in rain-forest habitats remain rare. We compared incidence of attacks of different natural enemies on semi-concealed and exposed caterpillars (Lepidoptera) in lowland and montane tropical rain forests, using plasticine models of caterpillars. We recorded attacks on caterpillars in four habitats: primary forest, secondary forest and forest fragment in lowlands (200 m asl), and montane primary forest (1700 m asl). We used 300 exposed and 300 semi-concealed caterpillars daily, and conducted the experiment for 6 d in every habitat. Daily incidence of attacks was higher on exposed caterpillars (4.95%) than on semi-concealed (leaf-rolling) caterpillars (2.99%). Attack pressure of natural enemies differed also among habitats. In the lowlands, continuous primary and secondary forests had similar daily incidence of attacks (2.39% and 2.36%) which was however lower than that found in a primary forest fragment (4.62%). This difference was caused by higher incidence of attacks by birds, ants and wasps in the forest fragment. The most important predators were birds in montane rain forests (61.9% of identified attacks), but insect predators, mostly ants, in the lowlands (58.3% of identified attacks). These results suggest that rapid decrease in the abundance of ants with altitude may be compensated by increased importance of birds as predators in montane forests. Further, it suggests that small rain-forest fragments may suffer from disproportionately high pressure from natural enemies, with potentially serious consequences for survival of their herbivorous communities.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

LITERATURE CITED

ATLEGRIM, O. 1992. Mechanisms regulating bird predation on a herbivorous larva guild in boreal coniferous forests. Ecography 15:1924.CrossRefGoogle Scholar
BANKO, P. C., OBOYSKI, P. T., SLOTTERBACK, J. W., DOUGILL, S. J., GOLTZ, D. M., JOHNSON, L., LAUT, M. E. & MURRAY, T. C. 2002. Availability of food resources, distribution of invasive species, and conservation of a Hawaiian bird along a gradient of elevation. Journal of Biogeography 29:789808.CrossRefGoogle Scholar
BARLOW, J., PERES, C. A., HENRIQUES, L. M. P., STOUFFER, P. C. & WUNDERLE, J. M. 2006. The responses of understorey birds to forest fragmentation, logging and wildfires: an Amazonian synthesis. Biological Conservation 128:182192.CrossRefGoogle Scholar
BASSET, Y. & NOVOTNY, V. 1999. Species richness of insect herbivore communities on Ficus in Papua New Guinea. Biological Journal of the Linnean Society 67:477499.CrossRefGoogle Scholar
BRODIE, E. D. 1993. Differential avoidance of coral snake banded patterns by free-ranging avian predators in Costa Rica. Evolution 47:227235.CrossRefGoogle ScholarPubMed
CAPPUCCINO, N. 1993. Mutual use of leaf-shelters by lepidopteran larvae on paper birch. Ecological Entomology 18:287292.Google Scholar
DEMPSTER, J. P. 1983. The natural control of populations of butterflies and moths. Biological Reviews 58:461481.CrossRefGoogle Scholar
DIDHAM, R. K., GHAZOUL, J., STORK, N. E. & DAVIS, A. J. 1996. Insects in fragmented forests: a functional approach. Trends in Ecology and Evolution 11:255260.CrossRefGoogle ScholarPubMed
DOAK, P. 2000. The effects of plant dispersion and prey density on parasitism rates in a naturally patchy habitat. Oecologia 122:556567.CrossRefGoogle Scholar
DYER, L. A. 1997. Effectiveness of caterpillar defenses against three species of invertebrate predators. Journal of Research on the Lepidoptera 34:4868.CrossRefGoogle Scholar
DYER, L. A. 2002. A quantification of predation rates, indirect positive effects on plants, and foraging variation of the giant tropical ant, Paraponera clavata. Journal of Insect Science 2:1825.Google ScholarPubMed
FAVERI, S. B., VASCONCELOS, H. L. & DIRZO, R. 2008. Effects of Amazonian forest fragmentation on the interaction between plants, insect herbivores, and their natural enemies. Journal of Tropical Ecology 24:5764.CrossRefGoogle Scholar
FAYNOR, C., MEHMOOD, S. A. & POTDAR, D. 1996. The effects of light and temperature on the surface activity of ants. Biological Station, University of Michigan, Michigan. 113 pp.Google Scholar
FEENY, P., BLAU, W. S. & KAREIVA, P. M. 1985. Larval growth and survivorship of the black swallowtail butterfly in central New York. Ecological Monographs 55:167187.CrossRefGoogle Scholar
FOWLER, S. V. & MACGARVIN, M. 1985. The impact of hairy wood ants, Formica lugubris, on the guild structure of herbivorous insects on birch, Betula pubescens. Journal of Animal Ecology 54:847855.CrossRefGoogle Scholar
GENTRY, G. L. & DYER, L. A. 2002. On the conditional nature of neotropical caterpillar defenses against their natural enemies. Ecology 83:31083119.CrossRefGoogle Scholar
GONZÁLEZ-GÓMEZ, P., ESTADES, C. & SIMONETTI, J. 2006. Strengthened insectivory in a temperate fragmented forest. Oecologia 148:137143.CrossRefGoogle Scholar
HAIRSTON, N. G., SMITH, F. E. & SLOBODKIN, L. B. 1960. Community structure, population control, and competition. American Naturalist 94:421425.CrossRefGoogle Scholar
HAWKINS, B. A., CORNELL, H. V. & HOCHBERG, M. E. 1997. Predators, parasitoids, and pathogens as mortality agents in phytophagous insect populations. Ecology 78:21452152.CrossRefGoogle Scholar
HODKINSON, I. D. 1999. Species response to global environmental change or why ecophysiological models are important: a reply to Davis et al. Journal of Animal Ecology 68:12591262.CrossRefGoogle Scholar
HÖLLDOBLER, B. & WILSON, E. 1990. The ants. Belknap Press of Harvard University Press, Cambridge. 732 pp.CrossRefGoogle Scholar
HOWE, A., LÖVEI, G. L. & NACHMAN, G. 2009. Dummy caterpillars as a simple method to assess predation rates on invertebrates in a tropical agroecosystem. Entomologia Experimentalis et Applicata 131:325329.CrossRefGoogle Scholar
HUMAN, K. G. & GORDON, D. M. 1999. Behavioral interactions of the invasive Argentine ant with native ant species. Insectes Sociaux 46:159163.CrossRefGoogle Scholar
ITO, F. & HIGASHI, S. 1991. Variance of ant effects on the different life forms of moth caterpillars. Journal of Animal Ecology 60:327334.CrossRefGoogle Scholar
JEANNE, R. L. 1979. A latitudinal gradient in rates of ant predation. Ecology 60:12111224.CrossRefGoogle Scholar
KAREIVA, P. 1987. Habitat fragmentation and the stability of predator–prey interactions. Nature 326:388390.Google Scholar
KESSLER, M., HERZOG, S. K., FJELDSÅ, J. & BACH, K. 2001. Species richness and endemism of plant and bird communities along two gradients of elevation, humidity and land use in the Bolivian Andes. Diversity and Distributions 7:6177.CrossRefGoogle Scholar
KLEIN, A., DEWENTER, I., BUCHORI, D. & TSCHARNTKE, T. 2002. Effects of land-use intensity in tropical agroforestry systems on coffee flower-visiting and trap-nesting bees and wasps. Conservation Biology 16:10031014.Google Scholar
KLIMES, P., JANDA, M., IBALIM, S., KUA, J. & NOVOTNY, V. 2011. Experimental suppression of ants foraging on rainforest vegetation in New Guinea: testing methods for a whole-forest manipulation of insect communities. Ecological Entomology 36:94103.CrossRefGoogle Scholar
KOH, L. P. & MENGE, D. N. L. 2006. Rapid assessment of Lepidoptera predation rates in neotropical forest fragments. Biotropica 38:132134.CrossRefGoogle Scholar
KROMBEIN, K. V. 1967. Trap-nesting wasps and bees: life histories, nests, and associates. Smithsonian Press, Washington DC. 570 pp.CrossRefGoogle Scholar
KRUESS, A. 2003. Effects of landscape structure and habitat type on a plant–herbivore–parasitoid community. Ecography 26:283290.CrossRefGoogle Scholar
LEWINSOHN, T. M., NOVOTNY, V. & BASSET, Y. 2005. Insects on plants: diversity of herbivore assemblages revisited. Annual Reviews of Ecology, Evolution and Systematics 36:597620.CrossRefGoogle Scholar
LIMA, S. L. 1992. Strong preferences for apparently dangerous habitats? A consequence of differential escape from predators. Oikos 64:597600.CrossRefGoogle Scholar
LIMA, S. L. & DILL, L. M. 1990. Behavioral decisions made under the risk of predation: a review and prospectus. Canadian Journal of Zoology 68:619640.CrossRefGoogle Scholar
LOEFFLER, C. C. 1996. Caterpillar leaf folding as a defense against predation and dislodgement: staged encounters using Dichomeris (Gelechiidae) larvae on goldenrods. Journal of the Lepidopterists’ Society 50:245260.Google Scholar
LOISELLE, B. A. & FARJI-BRENER, A. G. 2002. What's up? An experimental comparison of predation levels between canopy and understory in a tropical wet forest. Biotropica 34:327330.CrossRefGoogle Scholar
LOUDA, S. M. & RODMAN, J. E. 1996. Insect herbivory as a major factor in the shade distribution of a native crucifer (Cardamine cordifolia A. Gray, Bittercress). Journal of Ecology 84:229237.CrossRefGoogle Scholar
MÄNTYLÄ, E., ALESSIO, G. A., BLANDE, J. D., HEIJARI, J., HOLOPAINEN, J. K., LAAKSONEN, T., PIIRTOLA, P. & KLEMOLA, T. 2008. From plants to birds: higher avian predation rates in trees responding to insect herbivory. PLoS ONE 3:2832.CrossRefGoogle ScholarPubMed
MARTIN, T. E. & KARR, J. R. 1986. Patch utilization by migrating birds: resource oriented? Ornis Scandinavica 17:165174.CrossRefGoogle Scholar
MCALPINE, J. R., KEIG, R. & FALLS, R. 1983. Climate of Papua New Guinea. CSIRO and Australian National University Press, Canberra. 200 pp.Google Scholar
MCCOY, E. D. 1990. The distribution of insects along elevational gradients. Oikos 58:313322.CrossRefGoogle Scholar
MURAKAMI, M. 1999. Effect of avian predation on survival of leaf-rolling lepidopterous larvae. Researches on Population Ecology 41:135138.CrossRefGoogle Scholar
NAKAMURA, M. & OHGUSHI, T. 2003. Positive and negative effects of leaf shelters on herbivorous insects: linking multiple herbivore species on a willow. Oecologia 136:445449.CrossRefGoogle ScholarPubMed
NOVOTNY, V. & BASSET, Y. 1999. Body size and host plant specialisation: a relationship from a community of herbivorous insects from New Guinea. Journal of Tropical Ecology 15:315328.CrossRefGoogle Scholar
NOVOTNY, V. & BASSET, Y. 2005. Host specificity of insect herbivores in tropical forests. Proceedings of the Royal Society, London, Biological Sciences 272:10831090.CrossRefGoogle ScholarPubMed
NOVOTNY, V., MILLER, S. E., BASSET, Y., CIZEK, L., DARROW, K., KAUPA, B., KUA, J. & WEIBLEN, G. D. 2005. An altitudinal comparison of caterpillar (Lepidoptera) assemblages on Ficus trees in Papua New Guinea. Journal of Biogeography 32:13031314.CrossRefGoogle Scholar
NOVOTNY, V., MILLER, S. E., HRCEK, J., BAJE, L., BASSET, Y., LEWIS, O. T., STEWART, A. J. A. & WEIBLEN, G. D. 2012. Insects on plants: explaining the paradox of low diversity within specialist herbivore guilds. American Naturalist 179:351362.CrossRefGoogle ScholarPubMed
NYFFELER, M. 1999. Prey selection of spiders in the field. Journal of Arachnology 27:317324.Google Scholar
PEKIN, B. & MACFARLANE, C. 2009. Measurement of crown cover and leaf area index using digital cover photography and its application to remote sensing. Remote Sensing 1:12981320.CrossRefGoogle Scholar
PERFECTO, I. & VANDERMEER, J. 1996. Microclimatic changes and the indirect loss of ant diversity in a tropical agroecosystem. Oecologia 108:577582.CrossRefGoogle Scholar
PETERS, M. K., FISCHER, G., SCHAAB, G. & KRAEMER, M. 2009. Species compensation maintains abundance and raid rates of African swarm-raiding army ants in rainforest fragments. Biological Conservation 142:668675.CrossRefGoogle Scholar
PHILPOTT, S., PERFECTO, I. & VANDERMEER, J. 2006. Effects of management intensity and season on arboreal ant diversity and abundance in coffee agroecosystems. Biodiversity and Conservation 15:139155.CrossRefGoogle Scholar
POSA, M. R. C., SODHI, N. S. & KOH, L. P. 2007. Predation on artificial nests and caterpillar models across a disturbance gradient in Subic Bay, Philippines. Journal of Tropical Ecology 23:2733.CrossRefGoogle Scholar
REMMEL, T., DAVISON, J. & TAMMARU, T. 2011. Quantifying predation on folivorous insect larvae: the perspective of life-history evolution. Biological Journal of the Linnean Society 104:118.CrossRefGoogle Scholar
RICHARDS, L. A. & COLEY, P. D. 2007. Seasonal and habitat differences affect the impact of food and predation on herbivores: a comparison between gaps and understory of a tropical forest. Oikos 116:3140.CrossRefGoogle Scholar
ROBINSON, S. K. & HOLMES, R. T. 1982. Foraging behavior of forest birds: the relationships among search tactics, diet, and habitat structure. Ecology 63:19181931.Google Scholar
RODEWALD, A. D., YAHNER, R. H. & BRAWN, J. 2001. Avian nesting success in forested landscapes: influence of landscape composition, stand and nest-patch microhabitat, and biotic interactions. The Auk 118:10181028.CrossRefGoogle Scholar
RODRÍGUEZ-CASTAÑEDA, G., DYER, L. A., BREHM, G., CONNAHS, H., FORKNER, R. E. & WALLA, T. R. 2010. Tropical forests are not flat: how mountains affect herbivore diversity. Ecology Letters 13:13481357.CrossRefGoogle Scholar
RODRÍGUEZ-CASTAÑEDA, G., FORKNER, R. A., DYER, L. A., TEPE, E. & GENTRY, G. L. 2011. Weighing defensive and nutritive roles of ant mutualists across a tropical altitudinal gradient. Biotropica 43:343350.CrossRefGoogle Scholar
ROUX, L., CHAPUIS, J. L., FRENOT, Y. & VERNON, P. 2002. Diet of the house mouse (Mus musculus) on Guillou Island, Kerguelen archipelago, Subantarctic. Polar Biology 25:4957.CrossRefGoogle Scholar
SAAB, V. 1999. Importance of spatial scale to habitat use by breeding birds in riparian forest: a hierarchical analysis I. Ecological Applications 9:135151.CrossRefGoogle Scholar
SALVO, A. & VALLADARES, G. R. 2004. Looks are important: parasitic assemblages of agromyzid leafminers (Diptera) in relation to mine shape and contrast. Journal of Animal Ecology 73:494505.CrossRefGoogle Scholar
SAMSON, D. A., RICKART, E. A. & GONZALES, P. C. 1997. Ant diversity and abundance along an elevational gradient in the Philippines. Biotropica 29:349363.Google Scholar
SANDERS, N. J. 2002. Elevational gradients in ant species richness: area, geometry, and Rapoport's rule. Ecography 25:2532.CrossRefGoogle Scholar
SCHWENK, W. S., STRONG, A. M. & SILLETT, T. S. 2010. Effects of bird predation on arthropod abundance and tree growth across an elevational gradient. Journal of Avian Biology 41:367377.CrossRefGoogle Scholar
SHELLY, T. E. 1986. Rates of prey consumption by neotropical Robber flies (Diptera: Asilidae). Biotropica 18:166170.CrossRefGoogle Scholar
SIEVING, K. E. & WILLSON, M. F. 1998. Nest predation and avian species diversity in northwestern forest understory. Ecology 79:23912402.Google Scholar
SIVINSKI, J., PIÑERO, J. & ALUJA, M. 2000. The distributions of parasitoids (Hymenoptera) of anastrepha fruit flies (Diptera: Tephritidae) along an altitudinal gradient in Veracruz, Mexico. Biological Control 18:258269.CrossRefGoogle Scholar
STAMP, N. E. & BOWERS, M. D. 1988. Direct and indirect effects of predatory wasps (Polistes sp.: Vespidae) on gregarious caterpillars (Hemileuca lucina: Saturniidae). Oecologia 75:619624.CrossRefGoogle ScholarPubMed
STAMP, N. E. & BOWERS, M. D. 1991. Indirect effect on survivorship of caterpillars due to presence of invertebrate predators. Oecologia 88:325330.CrossRefGoogle ScholarPubMed
STIREMAN, J. O., O'HARA, J. O. & WOOD, D. M. 2006. Tachinidae: evolution, behavior, and ecology. Annual Review of Entomology 51:525555.CrossRefGoogle ScholarPubMed
TROLLOPE, S. T., WHITE, J. G. & COOKE, R. 2009. The response of ground and bark foraging insectivorous birds across an urban-forest gradient. Landscape and Urban Planning 93:142150.CrossRefGoogle Scholar
VALLADARES, G., SALVO, A. & CAGNOLO, L. 2006. Habitat fragmentation effects on trophic processes of insect–plant food webs. Conservation Biology 20:212217.CrossRefGoogle ScholarPubMed
VET, L. E. M. & DICKE, M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annual Reviews of Entomology 37:141172.CrossRefGoogle Scholar
VINSON, S. 1984. How parasitoids locate their hosts: a case of insect espionage. Symposia of the Royal Entomological Society of London 12:325348.Google Scholar
WALKER, M. & JONES, T. H. 2001. Relative roles of top-down and bottom-up forces in terrestrial tritrophic plant–insect herbivore–natural enemy systems. Oikos 93:177187.CrossRefGoogle Scholar
WEISS, M. R., WILSON, E. E. & CASTELLANOS, I. 2004. Predatory wasps learn to overcome the shelter defences of their larval prey. Animal Behaviour 68:4554.CrossRefGoogle Scholar
WITZ, B. W. 1990. Antipredator mechanisms in arthropods: a twenty year literature survey. The Florida Entomologist 73:7199.CrossRefGoogle Scholar
WÖLFLING, M. & ROSTÁS, M. 2009. Parasitoids use chemical footprints to track down caterpillars. Communicative and Integrative Biology 2:353355.CrossRefGoogle ScholarPubMed
ZANETTE, L., DOYLE, P. & TREMONT, S. M. 2000. Food shortage in small fragments: evidence from an area-sensitive passerine. Ecology 81:16541666.CrossRefGoogle Scholar