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Parasitism in a social wasp: effect of gregarines on foraging behavior, colony productivity, and adult mortality

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A Publisher’s Erratum to this article was published on 07 June 2006

Abstract

Behavior in eusocial insects likely reflects a long history of selection imposed by parasites and pathogens because the conditions of group living often favor the transmission of infection among nestmates. Yet, relatively few studies have quantified the effects of parasites on both the level of individual colony members and of colony success, making it difficult to assess the relative importance of different parasites to the behavioral ecology of their social insect hosts. Colonies of Polybia occidentalis, a Neotropical social wasp, are commonly infected by gregarines (Phylum Apicomplexa; Order Eugregarinida) during the wet season in Guanacaste, Costa Rica. To determine the effect of gregarine infection on individual workers in P. occidentalis, we measured foraging rates of marked wasps from colonies comprising both infected and uninfected individuals. To assess the effect of gregarines on colony success, we measured productivity and adult mortality rates in colonies with different levels of infection prevalence (proportion of adults infected). Foraging rates in marked individuals were negatively correlated with the intensity of gregarine infection. Infected colonies with high gregarine prevalence constructed nests with fewer brood cells per capita, produced less brood biomass per capita, and, surprisingly, experienced lower adult mortality rates than did uninfected or lightly infected colonies. These data strongly suggest that gregarine infection lowers foraging rates, thus reducing risk to foragers and, consequently, reducing adult mortality rates, while at the same time lowering per-capita input of materials and colony productivity. In infected colonies, queen populations were infected with a lower prevalence than were workers. Intra-colony infection prevalence decreased dramatically in the P. occidentalis population during the wet season.

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References

  • Aliabadi BW, Juliano SA (2002) Escape from gregarine parasites affects the competitive interactions of an invasive mosquito. Biol Invasions 4:283–297

    Article  PubMed  Google Scholar 

  • Bailey L, Ball BV (1991) Honey bee pathology, 2nd edn. Academic Press, London, UK

    Google Scholar 

  • Bordenstein SR, O'Hara FP, Werren JH (2001) Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia. Nature 409(6821):707–710

    Article  PubMed  CAS  Google Scholar 

  • Bouwma PE, Bouwma AM, Jeanne RL (2000) Social wasp swarm emigration: males stay behind. Ethol Ecol Evol 12:35–42

    Google Scholar 

  • Bouwma AM, Bouwma PE, Nordheim EV, Jeanne RL (2003a) Founding swarms in a tropical social wasp: adult mortality, emigration distance, and swarm size. J Insect Behav 16:439–452

    Article  Google Scholar 

  • Bouwma AM, Bouwma PE, Nordheim EV, Jeanne RL (2003b) Adult mortality rates in young colonies of a swarm-founding social wasp. J Zool 260:11–16

    Google Scholar 

  • Brown MJF, Loosli R, Schmid-Hempel P (2000) Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91:421–427

    Article  Google Scholar 

  • Brown MJF, Schmid-Hempel R, Schmid-Hempel P (2003) Strong context-dependent virulence in a host–parasite system: reconciling genetic evidence with theory. J Anim Ecol 72:994–1002

    Article  Google Scholar 

  • Buschinger A, Kleespies RG (1999) Host range specificity of an ant-pathogenic gregarine parasite Mattesia geminata (Neogregarinida: Lipotrophidae). Entomol Gen 24:93–104

    Google Scholar 

  • Chatterjee S, Hadi AS, Price B (2000) Regression analysis by example, 3rd edn. Wiley, New York, NY

    Google Scholar 

  • Combes C (2001) Parasitism: the ecology and evolution of intimate interactions. University of Chicago Press, Chicago, IL

    Google Scholar 

  • Crosland MWJ (1988) Effect of a gregarine parasite on the color of Myrmecia pilosula (Hymenoptera: Formicidae). Ann Entomol Soc Am 81:481–484

    Google Scholar 

  • Dejean A, Canard M (1990) Reproductive behaviour of Trichoscelia santareni (Navas) (Neuroptera: Mantispidae) and parasitization of the colonies of Polybia diguetana R. du Buysson (Hymenoptera: Vespidae). Neuroptera Int 6:19–26

    Google Scholar 

  • Durrer S, Schmid-Hempel P (1995) Parasites and the regional distribution of bumble bee species. Ecography 18:114–122

    Article  Google Scholar 

  • Forsyth AB (1978) Studies on the behavioral ecology of polygynous social wasps. PhD Dissertation, Harvard University, Cambridge, MA

    Google Scholar 

  • Hamilton WD (1980) Sex vs. non-sex vs. parasite. Oikos 35:282–290

    Article  Google Scholar 

  • Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science 218:384–387

    Article  PubMed  CAS  Google Scholar 

  • Howard KJ, Jeanne RL (2004) Rates of brood development in a social wasp: effects of colony size and parasite infection. Insectes Soc 51:179–185

    Article  Google Scholar 

  • Howard KJ, Jeanne RL (2005) Shifting foraging strategies in colonies of the social wasp Polybia occidentalis (Hymenoptera: Vespidae). Behav Ecol Sociobiol 57:481–489

    Article  Google Scholar 

  • Huger AM, Lenz M (1976) Occurrence of a coelomic gregarine (Protozoa: Sporozoa) with the Australian termite Coptotermes acinaciformis (Isoptera: Rhinotermitidae). Zeitschrift für Angewandte Entomologie 81:252–258

    Article  Google Scholar 

  • Imhoof B, Schmid-Hempel P (1999) Colony success of the bumble bee, Bombus terrestris, in relation to infections by two protozoan parasites, Crithidia bombi and Nosema bombi. Insectes Soc 46:233–238

    Article  Google Scholar 

  • Jeanne RL (1991a) The swarm-founding Polistinae. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, Ithaca, pp 191–231

    Google Scholar 

  • Jeanne RL (1991b) Polyethism. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, Ithaca, pp 389–425

    Google Scholar 

  • Jeanne RL (1996) Regulation of nest construction behaviour in Polybia occidentalis. Anim Behav 52:473–488

    Article  Google Scholar 

  • Jeanne RL (1999) Group size, productivity, and information flow in social wasps. In: Detrain C, Pasteels JM, Deneubourg JL (eds) Information processing in social insects. Birkhäuser Verlag, Basel, pp 3–30

    Google Scholar 

  • Jeanne RL, Nordheim EV (1996) Productivity in a social wasp: per capita output increases with swarm size. Behav Ecol 7:43–48

    Article  Google Scholar 

  • Jeanne RL, Bouwma AM (2004) Divergent patterns of nest construction in eusocial wasps. J Kan Ent Soc 77:429–447

    Article  Google Scholar 

  • Jouvenaz DP, Anthony DW (1979) Mattesia geminata sp. n. (Neogregarinida: Ophrocystidae) a parasite of the tropical fire ant, Solenopsis geminata (Fabricius). J Protozool 26:354–356

    Google Scholar 

  • Kleespies RG, Huger AM, Buschinger A, Nähring S, Schumann RD (1997) Studies on the life history of a neogregarine parasite found in Leptothorax ants from North America. Biocont Sci Technol 7:117–129

    Article  Google Scholar 

  • Kudô K, Yamane So, Mateus S, Tsuchida K, Itô Y, Miyano S, Zucchi R (2004) Parasitism affects worker size in the Neotropical swarm-founding wasp, Polybia paulista (Hymenoptera, Vespidae). Insectes Soc 51:221–225

    Article  Google Scholar 

  • Levine ND (1988) The protozoan phylum of Apicomplexa, vol. I. CRC Press, Boca Raton, FL

    Google Scholar 

  • Lipa JJ, Triggiani O (1992) A newly recorded neogregarine (Protozoa, Apicomplexa), parasite in honey bees (Apis mellifera) and bumble bees (Bombus spp.). Apidologie 23:533–536

    Article  Google Scholar 

  • Lipa JJ, Triggiani O (1996) Apicystis gen. nov. and Apicystis bombi (Liu, Macfarlane & Pengelly) comb. nov. (Protozoa: Neogregarinida), a cosmopolitan parasite of Bombus and Apis (Hymenoptera: Apidae). Apidologie 27:29–34

    Article  Google Scholar 

  • Liu HJ, Macfarlane RP, Pengelly DH (1974) Mattesia bombi n. sp. (Neogregarinida: Ophrocystidae), a parasite of Bombus (Hymenoptera: Apidae). J Invert Pathol 23:225–231

    Article  CAS  Google Scholar 

  • Lively CM (1992) Parthenogenesis in a freshwater snail: reproductive assurance versus parasitic release. Evolution 46:907–913

    Article  Google Scholar 

  • London KB, Jeanne RL (1998) Envelopes protect social wasps' nests from phorid infestation (Hymenoptera: Vespidae, Diptera: Phoridae). J Kan Ent Soc 71:175–182

    Google Scholar 

  • McCullagh P, Nelder JA (1983) Generalized linear models. Chapman and Hall, London, UK

    Google Scholar 

  • Michener CD (1964) Reproductive efficiency in relation to colony size in hymenopterous societies. Insectes Soc 11:317–342

    Article  Google Scholar 

  • Möller AP (1990) Effects of a hematophagous mite on the barn swallow (Hirundo rustica)—A test of the Hamilton and Zuk hypothesis. Evolution 44:771–784

    Article  Google Scholar 

  • Moore J (2002) Parasites and the behavior of animals. Oxford University Press, Oxford, UK

    Google Scholar 

  • Naug D, Camazine S (2002) The role of colony organization on pathogen transmission in social insects. J Theor Biol 215:427–439

    Article  PubMed  Google Scholar 

  • O'Donnell S, Jeanne RL (1990) Forager specialization and the control of nest repair in Polybia occidentalis Olivier (Hymenoptera: Vespidae). Behav Ecol Sociobiol 27:359–364

    Article  Google Scholar 

  • O'Donnell S, Jeanne RL (1992) Life-long patterns of forager behaviour in a tropical swarm-founding wasp: effects of specialization and activity level on longevity. Anim Behav 44:1021–1027

    Article  Google Scholar 

  • O'Donnell S, Jeanne RL (1995) Implications of senescence patterns for the evolution of age polyethism in eusocial insects. Behav Ecol 6:269–273

    Article  Google Scholar 

  • O'Donnell S (1997) How parasites can promote the expression of social behaviour in their hosts. Proc R Soc Lond B 264:689–694

    Article  Google Scholar 

  • O'Donnell S (2001) Worker biting interactions and task performance in a swarm-founding eusocial wasp (Polybia occidentalis, Hymenoptera: Vespidae). Behav Ecol 12:353–359

    Article  Google Scholar 

  • Parfin S (1958) Notes on the bionomics of the Mantispidae (Neuroptera: Planipennia). Entomol News 69:203–207

    Google Scholar 

  • Pie MR, Rosengaus RB, Traniello JFA (2004) Nest architecture, activity pattern, worker density and the dynamics of disease transmission in social insects. J Theor Biol 226:45–51

    Article  PubMed  Google Scholar 

  • Richards OW, Richards MJ (1951) Observations on the social wasps of South America (Hymenoptera: Vespidae). Trans R Entomol Soc Lond 102:1–170

    Google Scholar 

  • Richards OW (1978) The social wasps of the Americas, excluding the Vespinae. British Museum of Natural History, London, UK

    Google Scholar 

  • Roberts LS, Janovy JJ (2000) Gerald D. Schmidt & Larry S. Roberts' foundations of parasitology, 6th edn. McGraw-Hill, Boston, MA

    Google Scholar 

  • Rodrigues VM, de Moraes RAO (1981) Social wasps—observations on Polybia (Apopolybia) jurinei de Saussure, 1854 (Polistinae – Polybiini). An Soc Entomol Brasil 10:3–7

    Google Scholar 

  • Rosengaus RB, Maxmen AB, Coates LE, Traniello JFA (1998) Disease resistance: a benefit of sociality in the dampwood termite Zootermopsis angusticollis (Isoptera:Termopsidae). Behav Ecol Sociobiol 44:125–134

    Article  Google Scholar 

  • Schmid-Hempel P (1995) Parasites and social insects. Apidologie 26:255–271

    Article  Google Scholar 

  • Schmid-Hempel P (1998) Parasites in social insects. Princeton University Press, Princeton, NJ

    Google Scholar 

  • Schmid-Hempel P (2001) On the evolutionary ecology of host-parasite interactions: addressing the question with regard to bumblebees and their parasites. Naturwissenschaften 88:147–158

    Article  PubMed  CAS  Google Scholar 

  • Seger J, Hamilton WD (1988) Parasites and sex. In: Michod RE, Levin BR (eds) The evolution of sex. Sinauer, Sunderland, MA, pp 176–193

    Google Scholar 

  • Shoemaker DD, Katju V, Jaenike J (1999) Wolbachia and the evolution of reproductive isolation between Drosophila recens and Drosophila subquinaria. Evolution 53:1157–1164

    Article  Google Scholar 

  • Shykoff JA, Schmid-Hempel P (1991) Parasites delay worker reproduction in the bumblebee: consequences for eusociality. Behav Ecol 2:242–248

    Article  Google Scholar 

  • Stejskal M (1955) Gregarines found in the honey bee (Apis mellifera Linnaeus) in Venezuela. J Protozool 2:185–188

    Google Scholar 

  • Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc R Soc Lond B Bio 270:99–103

    Article  Google Scholar 

  • Thomas F, Oget E, Gente P, Desmots D, Renaud F (1999) Assortative pairing with respect to parasite load in the beetle Timarcha maritima (Chrysomelidae). J Evol Biol 12:385–390

    Article  Google Scholar 

  • Tosi JAJ (1969) Ecological map of Costa Rica. Tropical Science Center, San Jose, Costa Rica

  • Traniello JFA, Rosengaus RB, Savoie K (2002) Group living enhances immunity in a social insect. Proc Soc Natl Acad Sci USA 99:6838–6842

    Article  CAS  Google Scholar 

  • Weiser J, Briggs JD (1971) Identification of pathogens. In: Burges HD, Hussey NW (eds) Microbial control of insects and mites. Academic Press, London, pp 13–66

    Google Scholar 

  • Wenseleers T, Sundstrom L, Billen J (2002) Deleterious Wolbachia in the ant Formica truncorum. Proc R Soc Lond B Bio 269:623–629

    Article  CAS  Google Scholar 

  • West-Eberhard MJ (1978) Temporary queens in Metapolybia wasps: non-reproductive helpers without altruism? Science 200:441–443

    Article  PubMed  CAS  Google Scholar 

  • Williams DF, Oi DH, Knue GJ (1999) Infection of red imported fire ant (Hymenoptera: Formicidae) colonies with the entomopathogen Thelohania solenopsae (Microsporidia: Thelohaniidae) J Econ Entomol 92:830–836

    Google Scholar 

  • Zuk M (1987a) The effects of gregarine parasites, body size, and time of day on spermatophore production and sexual selection in field crickets. Behav Ecol Sociobiol 21:65–72

    Article  Google Scholar 

  • Zuk M (1987b) The effects of gregarine parasites on longevity, weight loss, fecundity and developmental time in the field crickets Gryllus veletis and G. pennsylvanicus. Ecol Entomol 12:349–354

    Article  Google Scholar 

  • Zuk M (1988) Parasite load, body size, and age of wild-caught male field crickets (Orthoptera: Gryllidae): effects on sexual selection. Evolution 42:969–976

    Article  Google Scholar 

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Acknowledgements

Our thanks go to Paul Hanson, curator of the Museo de Insectos of the Universidad de Costa Rica–San Pedro, for providing us with chemicals, for logistical support, and for the loan of specimens. We collected all specimens under the auspices of the Escuela de Biología and the Museo de Insectos of the Universidad de Costa Rica. We are grateful to the Hagnauer family in Costa Rica for permission to work on their property and for providing constant logistical support. Peter Bouwma, Andrew Carmichael, Kory Kramer and Miranda Moon provided invaluable assistance with data collection. Adam Smith shared methods for etherizing and marking wasps. Sean O'Donnell shared methods and provided valuable feedback on the ideas herein. Kevin Gross and Erik Nordheim provided statistical advice. James Traniello and two anonymous reviewers suggested ways to improve the manuscript. John Janovy Jr determined the gregarines as an undescribed species and was helpful and generous with his time in discussions of these results. This research was supported by National Science Foundation grant IBN-9514010 to RLJ, a Smithsonian Tropical Research Institute Short-Term Fellowship to AMB, University of Wisconsin–Madison Department of Zoology research grants to AMB and KJH, a National Science Foundation Pre-doctoral Fellowship to KJH, and by the College of Agricultural and Life Sciences, University of Wisconsin–Madison. The experiments performed comply with the current laws of Costa Rica.

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  1. Department of Entomology, University of Wisconsin, Madison, WI, 53706, USA

    Andrew M. Bouwma & Robert L. Jeanne

  2. Department of Zoology, University of Wisconsin, Madison, WI, 53706, USA

    Kenneth J. Howard

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  1. Andrew M. Bouwma
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  2. Kenneth J. Howard
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Correspondence to Andrew M. Bouwma.

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Communicated by J. F. A. Traniello

An erratum to this article can be found at http://dx.doi.org/10.1007/s00265-006-0205-1

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Bouwma, A.M., Howard, K.J. & Jeanne, R.L. Parasitism in a social wasp: effect of gregarines on foraging behavior, colony productivity, and adult mortality. Behav Ecol Sociobiol 59, 222–233 (2005). https://doi.org/10.1007/s00265-005-0028-5

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