Hostname: page-component-76fb5796d-skm99 Total loading time: 0 Render date: 2024-04-26T00:33:21.864Z Has data issue: false hasContentIssue false

Cross-habitat predation in Nepenthes gracilis: the red crab spider Misumenops nepenthicola influences abundance of pitcher dipteran larvae

Published online by Cambridge University Press:  08 December 2011

Trina Jie Ling Chua
Affiliation:
Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543
Matthew Lek Min Lim*
Affiliation:
Department of Biological Sciences, National University of Singapore, 14 Science Drive 4, Singapore 117543 Department of Organismic and Evolutionary Biology, Harvard University, 26 Oxford Street, Cambridge, Massachusetts 02138, USA
*
1Corresponding author. Email: matthewlim@oeb.harvard.edu

Abstract:

Phytotelmata (plant-held waters) are useful ecological models for studying predator–prey interactions. However, the ability of terrestrial predators to influence organism abundance within phytotelmata remains poorly studied. We investigated the predation of two pitcher-dwelling spiders, the red crab spider Misumenops nepenthicola and the yellow crab spider Thomisus nepenthiphilus (Araneae: Thomisidae) on dipteran larval abundance by manipulating their presence in the pitcher Nepenthes gracilis. Lower abundance in the larvae of the mosquito Tripteriodes spp. and increased spider mass were recorded after M. nepenthicola was introduced into laboratory-maintained pitchers (n = 10); T. nepenthiphilus did not affect larval abundance and a decrease in spider mass was recorded. Further investigations on two other dipteran larval species, the scuttle fly Endonepenthia schuitemakeri and gall midges Lestodiplosis spp., reported reduced numbers with the introduction of M. nepenthicola. We further tested this predation on dipteran larval abundance by its introduction, removal, and re-introduction to pitchers in the field (n = 42) over 1 mo. The spider's absence and presence significantly influenced larval numbers: all four dipteran species reported a significant decrease in numbers after M. nepenthicola was introduced. These results are one of the first to demonstrate the influence of a terrestrial phytotelm forager on the abundance of pitcher organisms via direct predation, reiterating the ecological importance of terrestrial phytotelm predators on phytotelm community structure and dynamics.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2011

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

ARMBRUSTER, P., HUTCHINSON, R. A. & COTGREAVE, P. 2002. Factors influencing community structure in a South American tank bromeliad fauna. Oikos 96:225234.CrossRefGoogle Scholar
BARTHLOTT, W., POREMBSKI, S., SEINE, R. & THEISEN, I. 2007. The curious world of carnivorous plants: a comprehensive guide to their biology and cultivation. Timber Press, Portland. 224 pp.Google Scholar
BENNETT, K. F. & ELLISON, A. M. 2009. Nectar, not colour, may lure insects to their death. Biology Letters 5:469472.CrossRefGoogle Scholar
CLARKE, C. M. 1997. Nepenthes of Borneo. Natural History Publications, Kota Kinabalu. 207 pp.Google Scholar
CLARKE, C. M. 1998. A re-examination of geographical variation in Nepenthes food webs. Ecography 21:430436.CrossRefGoogle Scholar
CLARKE, C. M. 2001. Nepenthes of Sumatra and Peninsula Malaysia. Natural History Publications, Kota Kinabalu. 336 pp.Google Scholar
CLARKE, C. M. & KITCHING, R. L. 1993. The metazoan food webs from six Bornean Nepenthes species. Ecological Entomology 18:716.CrossRefGoogle Scholar
CLARKE, C. M. & KITCHING, R. L. 1995. Swimming ants and pitcher plants - A unique ant-plant interaction from Borneo. Journal of Tropical Ecology 11:589602.CrossRefGoogle Scholar
CLARKE, C. M., BAUER, U., LEE, C. C., TUEN, A. A., REMBOLD, K. & MORAN, J. A. 2009. Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biology Letters 5:632635.CrossRefGoogle Scholar
DI GIUSTO, B., GROSBOIS, V., FARGEAS, E., MARSHALL, D. J. & GAUME, L. 2008. Contribution of pitcher fragrance and fluid viscosity to high prey diversity in a Nepenthes carnivorous plant from Borneo. Journal of Biosciences 33:121136.CrossRefGoogle Scholar
GORB, E., KASTNER, V., PERESSADKO, A., ARZT, E., GAUME, L., ROWE, N. & GORB, S. 2004. Structure and properties of the glandular surface in the digestive surface in the digestive zone of the pitcher in the carnivorous plant Nepenthes ventrata and its role in insect trapping and retention. Journal of Experimental Biology 207:29472963.CrossRefGoogle ScholarPubMed
GREENEY, H. F. 2001. The insects of plant-held waters: a review and bibliography. Journal of Tropical Ecology 17:241260.CrossRefGoogle Scholar
HOEKMAN, D. 2010. Turning up the heat: temperature influences the relative importance of top-down and bottom-up effects. Ecology 91:28192825.CrossRefGoogle ScholarPubMed
JURGENS, A., EL-SAYED, A. M. & SUCKLING, D. M. 2009. Do carnivorous plants use volatiles for attracting prey insects? Functional Ecology 23:875887.CrossRefGoogle Scholar
KITCHING, R. L. 2000. Food webs and container habitats: the natural history and ecology of phytotelmata. Cambridge University Press, Cambridge. 431 pp.CrossRefGoogle Scholar
KITCHING, R. L. 2001. Food webs in phytotelmata: “Bottom-up” and “top-down” explanations for community structure. Annual Review of Entomology 46:729760.CrossRefGoogle ScholarPubMed
KNEITEL, J. M. & MILLER, T. E. 2002. Resource and top-predator regulation in the pitcher plant (Sarracenia purpurea) inquiline community. Ecology 83:680688.CrossRefGoogle Scholar
LAND, M. F. 1985. The morphology and optics of spider eyes. Pp. 5378 in Barth, F. G. (ed.). Neurobiology of arachnids. Springer, Berlin.CrossRefGoogle Scholar
MAGUIRE, B., BELK, D. & WELLS, G. 1968. Control of community structure by mosquito larvae. Ecology 49:207210.CrossRefGoogle Scholar
MOGI, M. & CHAN, K. L. 1997. Variation in communities of dipterans in Nepenthes pitchers in Singapore: predators increase prey community diversity. Annals of the Entomological Society of America 90:177183.CrossRefGoogle Scholar
MOGI, M. & YONG, H. S. 1992. Aquatic arthropod communities in Nepenthes pitchers - the role of niche differentiation, aggregation, predation and competition in community organization. Oecologia 90:172184.CrossRefGoogle ScholarPubMed
MOON, D. C., ROSSI, A. M., DEPAZ, J., MCKELVEY, L., ELIAS, S., WHEELER, E. & MOON, J. 2010. Ants provide nutritional and defensive benefits to the carnivorous plant Sarracenia minor. Oecologia 164:185192.CrossRefGoogle Scholar
MORAN, J. A. 1993. Misumenops nepenthicola: the top aquatic predator of the Nepenthes food web? Brunei Museum Journal 8:8384.Google Scholar
MOUQUET, N., DAUFRESNE, T., GRAY, S. M. & MILLER, T. E. 2008. Modelling the relationship between a pitcher plant (Sarracenia purpurea) and its phytotelma community: mutualism or parasitism? Functional Ecology 22:728737.CrossRefGoogle Scholar
NAEEM, S. 1988. Predator-prey interactions and community structure - chironomids, mosquitos and copepods in Heliconia imbricata (Musaceae). Oecologia 77:202209.CrossRefGoogle ScholarPubMed
PETERSON, C. N., DAY, S., WOLFE, B. E., ELLISON, A. M., KOLTER, R. & PRINGLE, A. 2008. A keystone predator controls bacterial diversity in the pitcher-plant (Sarracenia purpurea) microecosystem. Environmental Microbiology 10:22572266.CrossRefGoogle ScholarPubMed
PHILLIPPS, A., LAMB, A. & LEE, C. C. 2008. Pitcher plants of Borneo. (Second edition). Natural History Publications, Kota Kinabalu. 305 pp.Google Scholar
POLLARD, S. D. 2005. Bugs in jugs. Nature Australia 28:6869.Google Scholar
ROMERO, G. Q. & SRIVASTAVA, D. S. 2010. Food-web composition affects cross-ecosystem interactions and subsidies. Journal of Animal Ecology 79:11221131.CrossRefGoogle ScholarPubMed
ROMERO, G. Q., MAZZAFERA, P., VASCONCELLOS-NETO, J., & TRIVELIN, P. C. O. 2006. Bromeliad-living spiders improve host plant nutrition and growth. Ecology 87:803808.CrossRefGoogle ScholarPubMed
SCHAEFER, H. M. & RUXTON, G. D. 2008. Fatal attraction: carnivorous plants roll out the red carpet to lure insects. Biology Letters 4:153155.CrossRefGoogle ScholarPubMed
SCHOLZ, I., BÜCKINS, M., DOLGE, L., ERLINGHAGEN, T., WETH, A., HISCHEN, F., MAYER, J., HOFFMANN, S., RIEDERER, M., RIEDEL, M. & BAUMGARTNER, W. 2010. Slippery surfaces of pitcher plants: Nepenthes wax crystals minimize insect attachment via microscopic surface roughness. Journal of Experimental Biology 213:11151125.CrossRefGoogle ScholarPubMed
SEIFERT, R. P. & SEIFERT, F. H. 1976. Natural history of insects living in inflorescences of two species of Heliconia. Journal of the New York Entomological Society 84:233242.Google Scholar
SIEGEL, S. & CASTELLAN, J. N. J. 1988. Nonparametric statistics for the behavioural sciences. (Second edition). McGraw Hill, Singapore. 399 pp.Google Scholar
SRIVASTAVA, D. S., KOLASA, J., BENGTSSON, J., GONZALEZ, A., LAWLER, S. P., MILLER, T. E., MUNGUIA, P., ROMANUK, T., SCHNEIDER, D. C. & TRZCINSKI, M. K. 2004. Are natural microcosms useful model systems for ecology? Trends in Ecology & Evolution 19:379384.CrossRefGoogle ScholarPubMed
TAN, H. T. W. 1997. A guide to the carnivorous plants of Singapore. Singapore Science Centre, Singapore. 177 pp.Google Scholar
TRAILL, L. W., LIM, M. L. M., SODHI, N. S. & BRADSHAW, C. J. A. 2010. Mechanisms driving change: altered species interactions and ecosystem function through global warming. Journal of Animal Ecology 79:937947.CrossRefGoogle ScholarPubMed