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Resource competition between two fungal parasites in subterranean termites

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Abstract

Subterranean termites live in large groups in underground nests where the pathogenic pressure of the soil environment has led to the evolution of a complex interaction among individual and social immune mechanisms in the colonies. However, groups of termites under stress can show increased susceptibility to opportunistic parasites. In this study, an isolate of Aspergillus nomius Kurtzman, Horn & Hessltine was obtained from a collapsed termite laboratory colony. We determined that it was primarily a saprophyte and, secondarily, a facultative parasite if the termite immunity is undergoing a form of stress. This was determined by stressing individuals of the Formosan subterranean termite Coptotermes formosanus Shiraki via a co-exposure to the virulent fungal parasite Metarhizium anisopliae (Metch.) Sorokin. We also examined the dynamics of a mixed infection of A. nomius and M. anisopliae in a single termite host. The virulent parasite M. anisopliae debilitated the termite immune system, but the facultative, fast growing parasite A. nomius dominated the mixed infection process. The resource utilization strategy of A. nomius during the infection resulted in successful conidia production, while the chance for M. anisopliae to complete its life cycle was reduced. Our results also suggest that the occurrence of opportunistic parasites such as A. nomius in collapsing termite laboratory colonies is the consequence of a previous stress, not the cause of the stress.

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References

  • Alizon S, van Baalen M (2008) Multiple infections, immune dynamics and virulence evolution. Am Nat 172:150–158

    Article  Google Scholar 

  • Anderson RM, May RM (1981) The population dynamics of microparasites and their invertebrate hosts. Phil Trans R Soc Lond 291:451–524

    Article  Google Scholar 

  • Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology 85:411–826

    Article  PubMed  Google Scholar 

  • Avulova S, Rosengaus RB (2011) Losing the battle against fungal infection: suppression of termite immune defenses during mycosis. J Insect Physiol 57:966–971

    Article  PubMed  CAS  Google Scholar 

  • Baverstock J, Roy HE, Pell JK (2010) Entomopathogenic fungi and insect behaviour: from unsuspecting hosts to targeted vectors. Biocontrol 55:103–112

    Article  Google Scholar 

  • Beal RH, Kais V (1962) Apparent infection of subterranean termites by Aspergillus flavus. Insect Pathol 4:488–489

    Google Scholar 

  • Becker G (1969) Rearing of termites and testing methods used in the laboratory. In: Krishna K, Weesner FM (eds) Biology of termites, vol 1. Academic Press, New York, pp 351–385

    Google Scholar 

  • Boucias DG, Pendland JC (1998) Principles of insect pathology. Kluwer Academic Publisher, Dordrecht

    Google Scholar 

  • Boucias DG, Stokes C, Storey G, Pendland JC (1996) The effects of imidacloprid on the termite, Reticulitermes flavipes and its interaction with the mycopathogen Beauveria bassiana. Pfanzenshutz-Natrichten Bayer 49:103–144

    Google Scholar 

  • Brown SP, Hochberg ME, Grenfell BT (2002) Does multiple infection select for raised virulence? Trend Microbiol 10:401–405

    Article  CAS  Google Scholar 

  • Caraco T, Glavanako S, Li S, Maniatty W, Szymanski BK (2006) Spatially structured superinfection and the evolution of disease virulence. Theor Popul Biol 69:367–384

    Article  PubMed  Google Scholar 

  • Chai YQ (1995) Preliminary studies on the pathogenicity of some entomopathogenous fungi to Coptotermes formosanus. Chin J Biol Control 11:68–69

    Google Scholar 

  • Chouvenc T, Su N-Y (2010) Apparent synergy among defense mechanisms in subterranean termites (Rhinotermitidae) against epizootic events – the limits and potential for biological control. J Econ Entomol 103:1327–1337

    Article  PubMed  Google Scholar 

  • Chouvenc T, Su N-Y (2012) When subterranean termites challenge the rules of fungal Epizootics. PLoS One 7:e34484. doi:10.1371/journal.pone.0034484

    Article  PubMed  CAS  Google Scholar 

  • Chouvenc T, Su N-Y, Elliott ML (2008a) Antifungal activity of the termite alkaloid norharmane against the mycelial growth of Metarhizium anisopliae and Aspergillus nomius. J Invertebr Pathol 99:345–347

    Article  PubMed  CAS  Google Scholar 

  • Chouvenc T, Su N-Y, Elliott ML (2008b) Interaction between the subterranean termite Reticulitermes flavipes (Isoptera: Rhinotermitidae) and the entomopathogenic fungus Metarhizium anisopliae in foraging arenas. J Econ Entomol 101:885–893

    Article  PubMed  CAS  Google Scholar 

  • Chouvenc T, Su N-Y, Robert A (2009a) Cellular encapsulation in the eastern subterranean termite, Reticulitermes flavipes (Isoptera), against infection by the entomopathogenic fungus Metarhizium anisopliae. J Invertebr Pathol 101:234–241

    Article  PubMed  Google Scholar 

  • Chouvenc T, Su N-Y, Robert A (2009b) Inhibition of Metarhizium anisopliae in the alimentary tract of the eastern subterranean termite Reticulitermes flavipes. J Invertebr Pathol 101:130–136

    Article  PubMed  CAS  Google Scholar 

  • Chouvenc T, Su N-Y, Robert A (2009c) Susceptibility of seven termite species (Isoptera) to the entomopathogenic fungus Metarhizium anisopliae. Sociobiology 54:723–748

    Google Scholar 

  • Chouvenc T, Bardunias P, Li H-F, Elliott ML, Su N-Y (2011a) Planar arenas for use in laboratory bioassay studies of subterranean termites (Rhinotermitidae). Florida Entomol 94:817–826

    Article  Google Scholar 

  • Chouvenc T, Grace JK, Su N-Y (2011b) Fifty years of attempted biological control of termites – analysis of a failure. Biol Contr 59:69–82

    Article  Google Scholar 

  • Chouvenc T, Su N-Y, Elliott ML (2011c) Rich microbial community associated with the nest material of Reticulitermes flavipes (Isoptera: Rhinotermitidae). Florida Entomol 94:115–116

    Article  Google Scholar 

  • Coley-Smith JR, Cooke RC (1971) Survival and germination of fungal sclerotia. Annu Rev Phytopathol 9:65–92

    Article  Google Scholar 

  • Cox FEG (2001) Concomitant infections, parasites and immune responses. Parasitology 122:S23–S38

    Article  PubMed  Google Scholar 

  • Cremer S, Armitage SAO, Schmid-Hempel P (2007) Social immunity. Curr Biol 17:693–702

    Article  Google Scholar 

  • Culliney TW, Grace JK (2000) Prospects for the biological control of subterranean termites (Isoptera: Rhinotermitidae), with special reference to Coptotermes formosanus. Bull Entomol Res 90:9–21

    Article  PubMed  CAS  Google Scholar 

  • Darlington JECP, Pomeroy WA (1977) Distribution of post-settlement survival in the field by reproductive pairs of Hodotermes mossambicus Hagen (Isopera: Hodotermitidae). Insect Soc 24:353–358

    Article  Google Scholar 

  • Dreizen S, McCredie K, Bodey G, Keating M (1986) Quantitative analysis of the oral complications of antileukemia chemotherapy. Oral Surg Oral Med Oral Pathol 62:650–653

    Article  PubMed  CAS  Google Scholar 

  • Ebert D, Weisser WW (1997) Optimal killing for obligate killers: the evolution of life histories and virulence of semelparous parasites. Proc R Soc Lond B 264:985–991

    Article  CAS  Google Scholar 

  • Godfray HCJ (1994) Parasitoids, behavioral and evolutionary ecology. Princeton University Press, Princeton

    Google Scholar 

  • Hamilton C, Lay F, Bulmer MS (2011) Subterranean termite prophylactic secretions and external antifungal defenses. J Insect Physiol 57:1259–1266

    Article  PubMed  CAS  Google Scholar 

  • Hughes WOH, Boomsma JJ (2004) Let your enemy do the work: within-host interactions between two fungal parasites of leaf-cutting ants. Proc R Soc Lonf B 271:S104–S106

    Article  Google Scholar 

  • Hughes WOH, Petersen KS, Ugelvig LV, Pedersen D, Thomsen L, Poulsen M, Boomsma JJ (2004a) Density-dependence and within-host competition in a semelparous parasite of leaf-cutting ants. BMC Evol Biol 4:45

    Article  PubMed  CAS  Google Scholar 

  • Hughes WOH, Thomsen L, Eilenberg J, Boomsma JJ (2004b) Diversity of entomopathogenic fungi near leaf-cutting ant nests in a neotropical forest, with particular reference to Metarhizium anisopliae var. anisopliae. J Invertebr Pathol 85:46–53

    Article  PubMed  CAS  Google Scholar 

  • Husseneder C, Ho H-Y, Blackwell M (2010) Comparison of the bacterial symbionts composition of the Formosan subterranean termite from its native and introduced range. Open Microbiol J 4:53–66

    Article  PubMed  CAS  Google Scholar 

  • Huxham IM, Lackie AM, McCorkindale NJ (1989) Inhibitory effects of cyclodepsipeptides, destruxins, from the fungus Metarhizium anisopliae on cellular immunity in insects. J Insect Physiol 35:97–105

    Google Scholar 

  • Ishii T, Takatsuka J, Nakai M, Kunimi Y (2002) Growth characteristics and competitive abilities of a nucleopolyhedrovirus and an entomopox virus in larvae of the smaller tea tortrix, Adoxophyes honmai (Lepidoptera: Tortricidae). Biol Contr 23:96–105

    Article  Google Scholar 

  • Jayasimha P, Henderson G (2007) Effect of Aspergillus flavus and Trichoderma harzianum on survival of Coptotermes formosanus (Isoptera: Rhinotermitidae). Sociobiology 49:135–141

    Google Scholar 

  • Kershaw MJ, Moorhouse ER, Bateman R, Reynolds SE, Charnley AK (1999) The role of destruxins in the pathogenicity of Metarhizium anisopliae for three species of insects. J Invertebr Pathol 74:213–223

    Article  PubMed  CAS  Google Scholar 

  • King EG, Spink WT (1969) Foraging galleries of the Formosan subterranean termite, Coptotermes formosanus, in Louisiana. Ann Entomol Soc Am 62:536–542

    Google Scholar 

  • Kurtz J, Reinhold K, Engqvist L (2000) Immunosuppression under stress: necessary for condition-dependant signalling? Trends Ecol Evol 15:418–419

    Article  Google Scholar 

  • Lenz M (1986) Principles behind the laboratory assessment of materials with subterranean termites. Recent perspectives and shifts in emphasis. Mater Org 21:123–137

    Google Scholar 

  • Lenz M (2009) Laboratory bioassays with subterranean termites (Isoptera). The importance of termite biology. Sociobiology 53:573–595

    Google Scholar 

  • Libshitz HI, Atkinson GW, Israel HL (1973) Pleural thickening as a manifestation of Aspergillus superinfection. Am J Radiol Radiother Nucl 120:883–886

    Google Scholar 

  • Lund AE (1965) Subterranean termites and fungal-bacterial relationships. Mater Org 32:497–502

    Google Scholar 

  • May RM, Anderson RM (1983) Epidemiology and genetics in the coevolution of parasites and hosts. Proc R Soc Lond B 219:281–313

    Article  PubMed  CAS  Google Scholar 

  • May RM, Nowak MA (1995) Coinfection and the evolution of parasite virulence. Proc R Soc Lond B 261:209–215

    Article  CAS  Google Scholar 

  • Nowak MA, May RM (1994) Superinfection and the evolution of parasite virulence. Proc R Soc Lond B 255:81–89

    Article  CAS  Google Scholar 

  • Nutting WL (1969) Flight and colony foundation. In: Krishna K, Weesner FM (eds) Biology of termites, vol 1. Academic Press, New York, pp 233–282

    Google Scholar 

  • Poulsen M, Hughes WOH, Boomsma JJ (2006) Differential resistance and the importance of antibiotic production in Acromyrmex echinatior leaf-cutting ant castes towards the entomopathogenic fungus Aspergillus nomius. Insect Soc 53:349–355

    Article  Google Scholar 

  • Read AF, Taylor LH (2001) The ecology of genetically diverse infections. Science 292:1099–1102

    Article  PubMed  CAS  Google Scholar 

  • Reber A, Chapuisat M (2012) Diversity, prevalence and virulence of fungal entomopathogens in colonies of the ant Formica selysi. Insect Soc (in press). doi: 10.1007/s00040-011-0209-3

  • Rigaud T, Perrot-Minnot M-J, Brown JF (2010) Parasite and host assemblages: embracing the reality will improve our knowledge of parasite transmission and virulence. Proc R Soc Lond B 277:3693–3702

    Article  Google Scholar 

  • Rolff J, Siva-Jothy MT (2003) Invertebrate ecological immunology. Science 301:472–475

    Article  PubMed  CAS  Google Scholar 

  • Rosengaus RB, Traniello JFA (1993) Disease risk as a cost of outbreeding in the termite Zootermopsis angusticollis. Proc Natl Acad Sci U S A 90:6641–6645

    Article  PubMed  CAS  Google Scholar 

  • Rosengaus RB, Traniello JFA, Leffebvre ML, Carlock DM (2000) The social transmission of diseases between adult male and female reproductive of the dampwood termite Zootermopsis angusticollis. Ethol Ecol Evol 12:419–433

    Article  Google Scholar 

  • Rosengaus RB, Traniello JFA, Bulmer MS (2011) Ecology, behavior and evolution of disease resistance in termite. In: Bignell DE, Roisin Y, Lo N (eds) Biology of termites: a modern synthesis. Springer, New York, pp 165–192

    Google Scholar 

  • SAS Institute (2002) SAS/STAT user’s guide, version 9.1. SAS Institute, Cary

    Google Scholar 

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

    Google Scholar 

  • Schmid-Hempel P (2008) Parasite immune evasion: a momentous molecular war. Trends Ecol Evol 23:318–326

    Article  PubMed  Google Scholar 

  • Schmid-Hempel P (2011) Evolutionary parasitology. Oxford University Press, New york

    Google Scholar 

  • Siderhurst MS, James DM, Blunt TD, Bjostad LB (2005) Antimicrobial activity of norharmane against the entomopathogenic fungus Metarhizium anisopliae (Metsch.) and the caste and phylogenetic distribution of this defense in termites (Insecta: Isoptera). Sociobiology 46:563–577

    Google Scholar 

  • Sikorowsky PP, Lawrence AM (1994) Microbial contamination and insect rearing. Am Entomol 40:240–253

    Google Scholar 

  • St Leger RJ, Screen SE, Shams-Pirzadsh B (2000) Lack of host specialization in Aspergillus flavus. Appl Environ Microbiol 66:320–324

    Article  PubMed  CAS  Google Scholar 

  • Staves PA, Knell RJ (2010) Virulence and competitiveness: testing the relationship during inter- and intraspecific mixed infections. Evolution 64:2643–2652

    Article  PubMed  Google Scholar 

  • Su N-Y, Scheffrahn RH (1986) A method to access, trap, and monitor field populations of the Formosan termite (Isoptera: Rhinotermitidae) in the urban environment. Sociobiology 12:299–304

    Google Scholar 

  • Su N-Y, Scheffrahn RH (1988) Foraging population and territory of the Formosan subterranean termite (Isoptera: Rhinotermitidae) in the urban environment. Sociobiology 14:353–359

    Google Scholar 

  • Tamashiro M, Fujii JK, Lai P-O (1973) A simple method to observe, trap, and prepare large numbers of subterranean termites for laboratory and field experiments. Environ Entomol 4:721–722

    Google Scholar 

  • Thomas MB, Watson EL, Valverde-Gracias (2003) Mixed infections and insect–pathogen interactions. Ecol Lett 6:183–188

    Article  Google Scholar 

  • Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago

    Google Scholar 

  • Toumanoff C, Rombaut J (1965) Action de certains champignons entomophages, cultivés sur les milieux appropriés attractifs, sur le termite de Saintonge Reticulitermes santonensis (de Feytaud). Ann Parasitol Hum Compar 40:605–609

    Google Scholar 

  • Vey A, Matha V, Dumas C (2002) Effects of the peptide mycotoxin destruxin E on insect haemocytes and on dynamics and efficiency of the multicellular immune reaction. J Invertebr Pathol 80:177–187

    Article  PubMed  CAS  Google Scholar 

  • Wicklow DT, Shotwell OL (1982) Intrafungal distribution of aflatoxins among conidia and sclerotia of Aspergillus flavus and Aspergillus parasiticus. Can J Microbiol 29:1–5

    Article  Google Scholar 

  • Wilson-Rich N, Stuart RJ, Rosengaus RB (2007) Susceptibility and behavioral response of the dampwood termite Zootermopsis angusticollis to the entomopathogenic nematode Steinernema carpocapsae. J Invertebr Pathol 95:17–25

    Article  PubMed  Google Scholar 

  • Zoberi MH, Grace JK (1990) Fungi associated with the subterranean termite Reticulitermes flavipes in Ontario. Mycologia 82:289–294

    Article  Google Scholar 

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Acknowledgments

We thank R. Pepin, A. Mullins and S. Osorio for technical assistance. We are grateful to W.O.H. Hughes (University of Leeds) for useful comments on a previous version of this manuscript, and to three anonymous reviewers. This study was supported in part by a grant from USDA-ARS under the grant agreement no. 58-6435-8-276 and a research opportunity fund of the University of Florida under the grant agreement no. 00094648.

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  1. Department of Entomology and Nematology, Fort Lauderdale Research and Education Center, Institute of Food and Agricultural Sciences, University of Florida, 3205 College Avenue, Fort Lauderdale, FL, 33314, USA

    Thomas Chouvenc, Caroline A. Efstathion & Nan-Yao Su

  2. Department of Plant Pathology, Fort Lauderdale Research and Education Center, Institute of Food and Agricultural Sciences, University of Florida, 3205 College Avenue, Fort Lauderdale, FL, 33314, USA

    Monica L. Elliott

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  1. Thomas Chouvenc
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Correspondence to Thomas Chouvenc.

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Communicated by: Sven Thatje

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Chouvenc, T., Efstathion, C.A., Elliott, M.L. et al. Resource competition between two fungal parasites in subterranean termites. Naturwissenschaften 99, 949–958 (2012). https://doi.org/10.1007/s00114-012-0977-2

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