Skip to main content
SpringerLink
Log in

Growth and reproduction of fungal feeding Collembola as affected by fungal species, melanin and mixed diets

  • Ecophysiology
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Fungal feeding soil invertebrates feed on a wide spectrum of fungal species suggesting that mixed diets increase fitness. We investigated relationships between food preferences for seven saprophytic fungal species/forms and fitness parameters (mortality, growth, time to reproduction, reproduction, egg size) in two Collembola species, Folsomia candida and Protaphorura armata. The fungal species/forms studied included the wild type and a melanin-deficient form of Aspergillus fumigatus to investigate the role of melanin in collembolan nutrition. Also, three mixed diets consisting of a preferred fungal species (Cladosporium cladosporioides) and species of intermediate or low food quality were investigated. Both Collembola species preferred similar fungal species/forms as food. Food preference generally matched fitness parameters, i.e. growth and reproduction of Collembola was at a maximum when feeding on preferred fungi. This was not the case for A. fumigatus. The wild type and the melanin-deficient form ranked among the least preferred fungi. Growth and reproduction of Collembola were low when feeding on the wild type but high when feeding on the melanin-deficient form indicating that the Collembola misjudged the food quality of the latter in the preference tests. The results show for the first time that genes driving melanin syntheses (pksP) strongly affect the food quality of fungi for fungal feeding invertebrates. Feeding on mixed diets generally increased growth and reproduction of Collembola except when the diets included toxic species (Penicillium sp.). The results support the nutrient balance hypothesis and also show that the detection of toxic species in the diet is important. They indicate that the widespread generalist feeding mode of Collembola maximizes fitness if toxic fungal species are avoided. The fitness parameters growth, reproduction and time until onset of reproduction were correlated closely but egg volume, which also varied with fungal diet, correlated poorly with the other fitness parameters. Variation in egg size with fungal diet shows that the diet of Collembola may have transgenerational effects.

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

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Addison JA, Parkinson D (1978) Influence of collembolan feeding activities on soil metabolism at a high arctic site. Oikos 30:529–538

    Google Scholar 

  • Anderson JM (1974) Succession, diversity and trophic relationships of some soil animals in decomposing leaf litter. J Anim Ecol 44:475–495

    Google Scholar 

  • Bengtsson G, Erlandsson A, Rundgren S (1988) Fungal odour attracts soils collembola. Soil Biol Biochem 20:25–30

    Article  Google Scholar 

  • Bengtsson G, Hedlund K, Rundgren S (1991) Selective odour perception in the soil collembola. J Chem Ecol 17:2113–2116

    CAS  Google Scholar 

  • Bernays EA, Bright KL (1993) Dietary mixing in grasshoppers: a review. Comp Biochem Physiol A 104:125–131

    Article  Google Scholar 

  • Bernays EA, Minkenberg OPJM (1997) Insect herbivores: different reasons for being a generalist. Ecology 78:1157–1169

    Google Scholar 

  • Bernays EA, Bright KL, Gonzales N, Angel J (1994) Dietary mixing in a generalist herbivore: tests of two hypotheses. Ecology 75:1997–2006

    Google Scholar 

  • Bonkowski M, Griffiths BS, Ritz K (2000) Food preferences of earthworms for soil fungi. Pedobiologia 44:666–676

    Google Scholar 

  • Booth RG, Anderson JM (1979) The influence of fungal food quality on the growth and fecundity of Folsomia candida (Collembola: Isotomidae). Oecologia 38:317–323

    Google Scholar 

  • Brakhage AA, Jahn B (2001) Molecular mechanisms of pathogenicity of Aspergillus fumigatus. In: Osiewacz HD (ed) Molecular biology of fungal development. Dekker, New York, pp 559–582

  • Butcher JW, Snider R, Snider RJ (1971) Bioecology of edaphic collembola and acarina. Annu Rev Entomol 16:249–288

    Article  Google Scholar 

  • Butler MJ, Day AW (1998) Fungal melanins: a review. Can J Microbiol 44:1115–1136

    Article  CAS  Google Scholar 

  • Chen B, Snider RJ, Snider RM (1995) Food preference and effects of food type on the life history of some soil Collembola. Pedobiologia 39:496–505

    Google Scholar 

  • Chen B, Snider RJ, Snider RM (1996) Food consumption by Collembola from northern Michigan deciduous forest. Pedobiologia 40:149–161

    Google Scholar 

  • Freeland WJ, Janzen DH (1974) Strategies in herbivory by mammals: the role of plant secondary compounds. Am Nat 108:269–289

    CAS  Google Scholar 

  • Gams W, Domsch K-H (1967) Beiträge zur Anwendung der Bodenwaschtechnik für die Isolierung von Bodenpilzen. Arch Mikrobiol 58:134–144

    Google Scholar 

  • Hägele BF, Rowell-Rahier M (1999) Dietary mixing in three generalist herbivores: nutrient complementation or toxin dilution? Oecologia 119:521–533

    Article  Google Scholar 

  • Hedlund K, Bengtsson G, Rundgren S (1995) Fungal odour discrimination in two sympatric species of fungivorous collembolans. Funct Ecol 9:869–875

    Google Scholar 

  • Hopkin SP (1997) Biology of the springtails Insecta: Collembola. Oxford University Press, Oxford

    Google Scholar 

  • Jaenike J (1990) Host specialization in phytophagous insects. Annu Rev Ecol Syst 21:243–273

    Article  Google Scholar 

  • Joose ENG, Testerink GJ (1977) The role of food in the population dynamics of Orchesella cincta (Linne) (Collembola). Oecologia 29:189–204

    Google Scholar 

  • Kaneko N, McLean MA, Parkinson D (1995) Grazing preference of Onychiurus subtenuis (Collembola) and Oppiella nova (Oribatei) for fungal species inoculated on pine needles. Pedobiologia 9:538–546

    Google Scholar 

  • Klironomos JN, Kendrick B (1995) Relationships among microarthropods, fungi, and their environment. Plant Soil 170:183–197

    CAS  Google Scholar 

  • Klironomos JN, Widden P, Deslandes I (1992) Feeding preferences of the collembolan Folsomia candida in relation to microfungal successions on decaying litter. Soil Biol Biochem 24:685–692

    Article  Google Scholar 

  • Lee Q, Widden P (1996) Folsomia candida, a ‘‘fungivorous’’ collembolan, feeds preferentially on nematodes rather than soil fungi. Soil Biol Biochem 28:689–690

    Article  CAS  Google Scholar 

  • Leonard MA (1984) Observations on the influence of culture conditions on the fungal feeding preferences of Folsomia candida (Collembola: Isotomidae). Pedobiologia 26:361–367

    Google Scholar 

  • Maraun M, Migge S, Schaefer M, Scheu S (1998) Selection of microfungal food by six oribatid mite species (Oribatida, Acari) from two different beech forests. Pedobiologia 42:232–240

    Google Scholar 

  • Maraun M, Martens H, Migge S, Theenhaus A, Scheu S (2003) Adding to “the enigma of soil animal diversity”: fungal feeders and saprophagous soil invertebrates prefer similar food substrates. Eur J Soil Biol 39:85–95

    Article  Google Scholar 

  • Moore JC, Ingham ER, Coleman DC (1987) Interspecific and intraspecific feeding selectivity of Folsomia candida (Willem) (Collembola, Isotomidae) on fungi. Biol Fertil Soils 5:6–12

    Google Scholar 

  • Newell K (1984) Interactions between two decomposer basidiomycetes and a collembolan under Sitka spruce: grazing and its potential effects on fungal distribution and litter decomposition. Soil Biol Biochem 16:235–239

    Article  Google Scholar 

  • Oelbermann K, Scheu S (2002) Effects of prey type and mixed dites on survival, growth and development of a generalist predator, Pardosa lugubris (Araneae: Lycosidae). Basic Appl Ecol 3:285–291

    Google Scholar 

  • Petersen H (1975) Estimation of dry weight, fresh weight, and caloric content of various Collembola species. Pedobiologia 15:222–243

    Google Scholar 

  • Petersen H (2002) General aspects of collembolan ecology at the turn of the millennium. Pedobiologia 46:246–260

    Google Scholar 

  • Ponge JF (2000) Vertical distribution of Collembola (Hexapoda) and their food resources in organic horizons of beech forests. Biol Fertil Soils 32:508–522

    Article  Google Scholar 

  • Pulliam HR (1975) Diet optimization with nutrient constraints. Am Nat 109:765–768

    Article  Google Scholar 

  • Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and test. Quart Rev Biol 52:137–152

    Article  Google Scholar 

  • Rapport DJ (1980) Optimal foraging for complementary resources. Am Nat 116:324–346

    Article  Google Scholar 

  • Sadaka-Laulan N, Ponge JF, Roquebert MF, Bury E, Boumezzough A (1998) Feeding preferences of the collembolan Onychiurus sinensis for fungi colonizing holm oak litter (Quercus rotundifolia Lam.). Eur J Soil Biol 34:179–188

    Article  Google Scholar 

  • Scheu S, Setälä H (2002) Multitrophic interactions in decomposer communities. In: Tscharntke T, Hawkins BA (eds) Multitrophic level interactions. Cambridge University Press, Cambridge, pp 223–264

  • Shaw PJA (1988) A consistent hierarchy in the fungal feeding preferences of the collembolan Protaphorura armata. Pedobiologia 31:179–187

    Google Scholar 

  • Singer MS (2001) Determinants of polyphagy by a woolly beak caterpillar: a test of the physiological efficiency hypothesis. Oikos 93:194–204

    Google Scholar 

  • Toft S, Wise DH (1999) Growth, development, and survival of a generalist predator fed single- and mixed-species diets of different quality. Oecologia 119:191–197

    Article  Google Scholar 

  • Verhoef HA, Prast JE, Verweij RA (1988) Relative importance of fungi and algae in the diet and nitrogen nutrition of Orchesella cincta (L.) and Tomocerus minor (Lubbock) (Collembola). Funct Ecol 2:195–201.

    Google Scholar 

  • Via S (1990) Ecological genetics and host adaptation in herbivorous insects: the experimental study of evolution in natural and agricultural systems. Annu Rev Entomol 35:421–446

    Google Scholar 

  • Visser S, Whittaker JB (1977) Feeding preferences for certain litter fungi by Onychiurus subtenuis (Collembola). Oikos 29:320–325

    Google Scholar 

  • Walsh MI, Bolger T (1990) Effects of diet on the growth and reproduction of some Collembola in laboratory cultures. Pedobiologia 334:161–171

    Google Scholar 

Download references

Acknowledgements

Financial support by the Deutsche Forschungsgemeinschaft (Graduiertenkolleg 340, Technische Universität Darmstadt) is gratefully acknowledged. Helpful comments by Liliane Ruess are appreciated.

Author information

Authors and Affiliations

  1. Institut für Zoologie, Technische Universität Darmstadt, Schnittspahnstrasse 3, 64287, Darmstadt, Germany

    Stefan Scheu & Frauke Simmerling

Authors
  1. Stefan Scheu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Frauke Simmerling
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stefan Scheu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Scheu, S., Simmerling, F. Growth and reproduction of fungal feeding Collembola as affected by fungal species, melanin and mixed diets. Oecologia 139, 347–353 (2004). https://doi.org/10.1007/s00442-004-1513-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-004-1513-7

Keywords

Search

Navigation