Skip to main content
SpringerLink
Log in

Leaf-Associated Bacterial and Fungal Taxa Shifts in Response to Larvae of the Tree Hole Mosquito, Ochlerotatus triseriatus

  • Original Article
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Larvae of the eastern tree hole mosquito, Ochlerotatus triseriatus (Say), and related container-breeding species are known to feed upon substrate-associated microorganisms. Although the importance of these microbial resources to larval growth has been established, almost nothing is known about the taxonomic composition and dynamics of these critical microbial food sources. We examined bacterial and fungal community compositional changes on oak leaves tethered in natural tree hole habitats of O. triseriatus. We eliminated larvae experimentally in a subset of the tree holes and examined 16S rDNA gene sequences for bacteria and ergosterol concentrations and 18S rRNA gene sequences for fungi collected from leaf material subsamples. Leaf ergosterol content varied significantly with time, but not treatment. Principal component analysis (PCA) was used to compare microbial taxonomic patterns found in leaves incubated with or without larvae present, and we found that larval presence affected both bacterial and fungal groups, either from loosely attached or strongly adherent categories. Bacterial communities generally grouped more tightly when larvae were present, and class level taxa proportions changed when larvae were present, suggesting selection by larval feeding or activities for particular taxa such as members of the Bacteroidetes, Alphaproteobacteria, and Betaproteobacteria classes. Fungal taxa composite scores also separated along PC axes related to the presence of larvae and indicated larval feeding effects on several higher taxonomic groups, including Saccharomycetes, Dothideomycetes, and Chytridiomycota. These results support the hypothesis that larval mosquito feeding and activities altered microbial communities associated with substrate surfaces, potentially leading to decreased food value of the resource and affecting decomposition of particulate matter in the system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
Figure 7

Similar content being viewed by others

References

  1. Alexopoulous CJ, Mims CW, Blackwell M (1996) Phylum Chytridiomycota. In: Introductory Mycology. John Wiley & Sons, New York, pp 86–126

  2. Amann R, Ludwig W (2000) Ribosomal RNA-targeted nucleic acid probes for studies in microbial ecology. FEMS Microbiol Rev 24: 555–565

    Article  PubMed  CAS  Google Scholar 

  3. Bell T, Ager D, Song JI, Newman JA, Thompson IP, Lilley AK, van der Gast CJ (2005) Larger islands house more bacterial taxa. Science 308:1884

    Article  PubMed  CAS  Google Scholar 

  4. Borneman J, Hartin RJ (2000) PCR primers that amplify fungal rRNA genes from environmental samples. Appl Environ Microbiol 66:4356–4360

    Article  PubMed  CAS  Google Scholar 

  5. Case RJ, Boucher Y, Dahllo I, Holmström C, Doolittle WF, Kjelleberg S (2007) Use of 16S rRNA and rpoB genes as molecular markers for microbial ecology studies. Appl Environ Microbiol 73:278–288

    Article  PubMed  CAS  Google Scholar 

  6. Chen S, Bagdasarian M, Kaufman MG, Walker E (2007) Characterization of strong promoters from an environmental Flavobacterium hibernum strain by using a Green Fluorescent Protein-based reporter system. Appl Environ Microbiol 73:1089–1100

    Article  PubMed  CAS  Google Scholar 

  7. Cochran-Stafira DL, von Ende CN (1998) Integrating bacteria into food webs: Studies with Sarracenia purpurea inquilines. Ecology 79:880–898

    Google Scholar 

  8. Crosby LD, Criddle CS (2003) Understanding bias in microbial community analysis techniques due to rrn operon copy number heterogeneity. BioTechniques 34:790–794

    PubMed  CAS  Google Scholar 

  9. Fish D, Carpenter SR (1982) Leaf litter and larval mosquito dynamics in tree-hole ecosystems. Ecology 63:283–288

    Article  Google Scholar 

  10. Gessner MO, Chauvet E (1993) Ergosterol-to-biomass conversion factors for aquatic hyphomycetes. Appl Environ Microbiol 59:502–507

    PubMed  CAS  Google Scholar 

  11. Gönczöl J, Révay A (2003) Treehole fungal communities: aquatic, aero-aquatic, and dematiaceous hyphomycetes. Fungal Divers 12:19–34

    Google Scholar 

  12. Graça MA (2001) The role of invertebrates on leaf litter decomposition in streams—a review. Int Rev Hydrobiol 86:383–393

    Article  Google Scholar 

  13. Gulis V (2001) Are there any substrate preferences in aquatic hyphomycetes? Mycol Res 105:1088–1093

    Article  Google Scholar 

  14. Gulis V, Suberkropp K (2003) Leaf litter decomposition and microbial activity in nutrient-enriched and unaltered reaches of a headwater stream. Freshw Biol 48:123–134

    Article  Google Scholar 

  15. Hahn MW, Höfle MG (2001) Grazing of protozoa and its effect on populations of aquatic bacteria. FEMS Microbiol Ecol 35:113–121

    Article  PubMed  CAS  Google Scholar 

  16. Hutter G, Schlagenhauf U, Valenza G, Horn M, Burgemeister S, Claus H, Vogel U (2003) Molecular analysis of bacteria in periodontitis: evaluation of clone libraries, novel phylotypes and putative pathogens. Microbiol-SGM 149:67–75

    Article  CAS  Google Scholar 

  17. Huws SA, McBain AJ, Gilbert P (2005) Protozoan grazing and its impact upon population dynamics in biofilm communities. J Appl Microbiol: 98:238–244

    Article  PubMed  CAS  Google Scholar 

  18. Joubert J-M, Wolfaardt GM, Botha A (2006) Microbial exopolymers link predator and prey in a model yeast biofilm system. Microb Ecol 52:187–197

    Article  PubMed  Google Scholar 

  19. Jürgens K (1994) Impact of Daphnia on planktonic microbial food webs—a review. Mar Microb Food Webs 8:295–324

    Google Scholar 

  20. Jürgens K, Matz C (2002) Predation as a shaping force for the phenotypic and genotypic composition of planktonic bacteria. Antonie Van Leeuwenhoek. 81:413–434

    Article  PubMed  Google Scholar 

  21. Kaufman MG, Walker ED, Smith TW, Merritt RW, Klug MJ (1999) The effects of larval mosquitoes Aedes triseriatus and stemflow on microbial community dynamics in container habitats. Appl Environ Microbiol 65:2661–2673

    PubMed  CAS  Google Scholar 

  22. Kaufman MG, Bland SN, Worthen ME, Walker ED, Klug MJ (2001) Bacterial and fungal biomass responses to feeding by larval Aedes triseriatus (Diptera: Culicidae). J Med Entomol 38:711–719

    Article  PubMed  CAS  Google Scholar 

  23. Kaufman MG, Goodfriend W, Kohler-Garrigan A, Walker ED, Klug MJ (2002) Soluble nutrient effects on microbial communities and mosquito production in Ochlerotatus triseriatus habitats. Aquat Microb Ecol 29:73–88

    Article  Google Scholar 

  24. Kaufman MG, Walker ED (2006) Indirect effects of soluble nitrogen on growth of Ochlerotatus triseriatus larvae in container habitats. J Med Ent 43:677–688

    Article  CAS  Google Scholar 

  25. King CH, Sanders RW, Shotts Jr. KG, Porter KG (1991) Differential survival of bacteria ingested by zooplankton from a stratified eutrophic lake. Limnol Oceanogr 36:829–845

    Article  Google Scholar 

  26. Kirchman DL (2002) The ecology of Cytophaga–Flavobacteria in aquatic environments. FEMS Microbiology Ecology 39:91–100

    CAS  PubMed  Google Scholar 

  27. Kitching RL (2001) Food webs in phytotelmata: “Bottom–up” and “top–down” explanations for community structure. Annu Rev Entomol 46:729–760

    Article  PubMed  CAS  Google Scholar 

  28. Kneitel JM, Miller TE (2002) Resource and top-predator regulation in the pitcher plant Sarracenia purpurea inquiline community. Ecology 83:680–688

    Google Scholar 

  29. Langenheder S, Jürgens K (2001) Regulation of bacterial biomass and community structure by metazoan and protozoan predation. Limnol Oceanogr 46: 121–134

    Article  Google Scholar 

  30. Leonard PM, Juliano, SA (1995) Effect of leaf litter and density on fitness and population performance of the treehole mosquito Aedes triseriatus. Ecol Entomol 20:125–136

    Article  Google Scholar 

  31. Lounibos LP, Nishimura N, Escher RL (1992) Seasonality and components of oak litterfall in southeastern Florida. Florida Scientist 55(2):92–98

    Google Scholar 

  32. Marchesi JR, Sato T, Weightman AJ, Martin TA, Fry JC, Hiom SJ, Wade WG (1998) Design and evaluation of useful bacterium-specific PCR primers that amplify genes coding for bacterial 16S rDNA. Appl Environ Microbiol 64:795–799

    PubMed  CAS  Google Scholar 

  33. Matz C, McDougald D, Moreno AM, Yung PY, Yildiz FH, Kjelleberg S (2005) Biofilm formation and phenotypic variation enhance predation-driven persistence of Vibrio cholerae. Proc Natl Acad Sci U S A 102:16819–16824

    Article  PubMed  CAS  Google Scholar 

  34. Merritt RW, Walker ED, Cummins K, Wilzbach M, Morgan WT (1989) A broad evaluation of B.t.i. for black fly (Diptera: Simuliidae) control in a Michigan river: efficacy, carry, and non-target effects on invertebrates and fish. J Amer Mosq Control Assoc 5:397–415

    CAS  Google Scholar 

  35. Merritt RW, Dadd RH, Walker ED (1992) Feeding behavior natural food and nutritional relationships of larval mosquitoes. Annu Rev Entomol 37:349–376

    PubMed  CAS  Google Scholar 

  36. Paradise CJ, Dunson WA (1997) Insect species interactions and resource effects in treeholes: are helodid beetles bottom–up facilitators of midge populations? Oecologia 109:303–312

    Article  Google Scholar 

  37. Pernthaler J (2005) Predation on prokaryotes in the water column and its ecological implications. Nature Rev Microbiol 3:537–546

    Article  CAS  Google Scholar 

  38. Rossi L (1985) Interaction of invertebrates and microfungi in freshwater ecosystems. Oikos 44:175–84

    Article  Google Scholar 

  39. Sakamoto M, Lan PTN, Benno Y (2007) Barnesiella viscericola gen. nov., sp nov., a novel member of the family Porphyromonadaceae isolated from chicken caecum. Int J Sys Evol Microbiol 57:342–346

    Article  CAS  Google Scholar 

  40. Tall L, Cattaneo A, Cloutier L, Dray S, Legendre P (2006) Resource partitioning in a grazer guild feeding on a multilayer diatom mat. J N Am Benthol Soc 25:800–810

    Article  Google Scholar 

  41. Trzcinski MK, Walde SJ, Taylor PD (2005) Stability of pitcher-plant microfaunal populations depends on food web structure. Oikos 110:146–154

    Article  Google Scholar 

  42. Walker ED, Merritt RW (1991) “Behavior of larval Aedes triseriatus Diptera: Culicidae.” J Med Entomol 28:581–589

    PubMed  CAS  Google Scholar 

  43. Walker ED, Lawson DL, Morgan WT, Klug MJ (1991) Nutrient dynamics, bacterial populations, and mosquito productivity in tree hole ecosystems. Ecology 72:1529–1546

    Article  Google Scholar 

  44. Wong MKM, Goh TK, Hodgkiss IJ, Hyde KD, Ranghoo VM, Tsui CKM, Ho WH, Wong WSW, Yuen TK (1998) Role of fungi in freshwater ecosystems. Biodivers Conserv 7:1187–1206

    Article  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge the technical assistance of Blair Bullard, Robert Burns, Joel Stouten, and Amy Rogers. We would also like to thank the staff at the Ribosomal Database Project at MSU for their help with various aspects of sequence file analyses. This project was funded by NIH award AI21884.

Author information

Authors and Affiliations

  1. Department of Entomology, Michigan State University, East Lansing, MI, 48824, USA

    Michael G. Kaufman & Edward D. Walker

  2. Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, MI, 48824, USA

    Shicheng Chen & Edward D. Walker

Authors
  1. Michael G. Kaufman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shicheng Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Edward D. Walker
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Michael G. Kaufman.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kaufman, M.G., Chen, S. & Walker, E.D. Leaf-Associated Bacterial and Fungal Taxa Shifts in Response to Larvae of the Tree Hole Mosquito, Ochlerotatus triseriatus . Microb Ecol 55, 673–684 (2008). https://doi.org/10.1007/s00248-007-9310-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-007-9310-6

Keywords

Search

Navigation