Effects of resource quality on the fitness of collembola fed single and mixed diets from the green and brown food chain

https://doi.org/10.1016/j.soilbio.2021.108156Get rights and content

Highlights

  • Trophic shift of marker fatty acid can assess assimilation into consumer tissue.

  • Dietary ω3-fatty acid content and C/N ratio influence Collembola biomass/survival.

  • Effects of low-quality diet aren't compensated by mixing with high-quality diets.

Abstract

The effect of food resources, varying in C/N ratio, lipid and ω3 polyunsaturated fatty acid (ω3-PUFA) content, on the fitness of three Collembola species (the euedaphic Protaphorura fimata, hemiedpahic Folsomia candida and epedaphic Lepidocyrtus violaceus) was investigated. Dietary routing of fatty acids served as an indicator for resource consumption and assimilation. Laboratory feeding experiments were performed with single and mixed diets made from algae, cyanobacteria, fungi, soil bacteria or plant roots and leaves. Collembola exhibited species-specific responses in biomass and survival rate to the diets differing in quality, reflecting adaptations to their soil environment. Generally, wide dietary C/N ratios had a negative impact, with roots especially unfavorable, while the dependence on ω3-PUFAs varied. Mixing diets did mostly result in intermediate results where high-quality resources compensate for low-quality resources, with only mixes of resources favoured by Collembola in the wild showing synergistic positive effects. The results suggest that most resources of soil detritivores, irrespective of green or brown food chain, represent a non-optimal diet, with clear adaptations depending on habitat and the potential to truly exploit any resource mostly exhibited in euedaphic species.

Introduction

Dietary bottom-up effects of nutrients are widely reported for trophic interactions in terrestrial and aquatic ecology (e.g. Milton and Kaspari, 2007; Gliwicz, 2007). Particularly, the carbon to nitrogen ratio is a commonly accepted indicator for food quality, affecting consumer fitness and reproduction (Cruz-Rivera and Hay, 2000, 2001; Rosenblatt, 2018). Nitrogen is primarily limiting in terrestrial ecosystems, predominantly in the detritivore food chain based on recalcitrant resources (Paul, 2016; Zechmeister-Boltenstern et al., 2015).)

Besides element stoichiometry, food quality is determined by nutritionally valuable biomolecules such as amino acids, vitamins, sterols and fatty acids (Ruess and Müller-Navarra, 2019). In aquatic systems, ω3 polyunsaturated fatty acids (ω3-PUFAs) are a subset of fatty acids highly beneficial for membrane fluidity, cellular homeostasis and the overall growth and production rate of metazoic organisms (Brett and Müller-Navarra, 1997; Simopoulos, 2000). They are twice as efficiently assimilated in comparison bulk carbon (Mayor et al., 2011), and are selectively transported along the food chain (Müller-Navarra, 2006). The positive impact of ω3-PUFAs on the life cycle of marine consumers was frequently observed (Brett et al., 2009; Støttrup and McEvoy, 2007), but only recently reported for soil decomposers like Collembola (Menzel et al., 2018). However, the response of consumer fitness to diet mixtures strongly differing in elemental (i.e. C/N) and biochemical (i.e. ω3 content) quality has not been addressed in the soil fauna yet.

This work provides a broad overview on changes in biomass, survival rate and fatty acid signatures in Collembola, common and abundant soil microarthropods (Rusek, 1998) known to feed on a variety of food sources (Charhataghi et al., 2005), as a response to diets comprising single and multiple components varying in quality. As most soil consumers can obtain many PUFA only from food, the trophic shift of specific dietary fatty acids into consumer tissue was used as an indicator for feeding and assimilation (Ruess and Chamberlain, 2010). It is presumed that a high quality of the diet, expressed through a narrow C/N ratio and large proportion of w3-PUFAs (Buse et al., 2013), would be reflected in high biomass and survival rate of the Collembola. Thereby, diets mixed from multiple food sources would show intermediate effects between diets of singular components, as high-quality components compensate for low quality components through improving the nutrient profile or through secondary effects such as the dilution of toxic substances (Guglielmo et al., 1996). Alternatively, if all diet components are of sufficiently high quality, synergistic net-positive effects due to optimizing the nutrient profile (Rapport 1980) are expected. These responses should further differ in intensity between species as their habitat changes from above-ground epedaphic to below-ground euedaphic Collembola, as below-ground species are generally better adapted to varying diet sources due to the heterogeneity and food scarcity of their habitat (Ponge, 2000; Endlweber et al., 2009).

Section snippets

Materials & methods

The diets represent major resources in the soil food web: from the herbivore (“green”) food chain - green algae (Chlorella vulgaris), cyanobacteria (Spirulina platensis), leaves (sunflower, Helianthus annuus) and roots (mixture of H. annuus roots and potato fine hair roots, Solanum tuberosum, without tuber tissue), and from the detritivore (“brown”) food chain - fungi (Chaetomium globosum) and bacteria (Bacillus megaterium). They were either sourced from laboratory cultures (bacteria and

Results

The C/N ratio of the different diets fluctuated around five (cyanobacteria: 4.6 ± 0.04, green algae: 5.0 ± 0.04, bacteria: 5.0 ± 0.05, fungi: 6.1 ± 0.03), with only plants deviating (leaves: 8.4 ± 0.02, roots: 13.0 ± 0.03). Fat contents varied considerably, ranging from very low in fungi, roots and leaves (2.2 ± 0.5, 6.8 ± 0.8 and 17.5 ± 0.6 μMol g−1DW, respectively), to intermediate in bacteria (64.6 ± 11.4 μMol g−1DW), and high in cyanobacteria and green algae (140.6 ± 6.1 and 235.8 ± 17.3

Discussion

Considering the proxies for diet quality (i.e. C/N ratio and ω3-PUFA content), “microscopic” diet organisms comprised a narrow and “macroscopic” plant diets a wide C/N ratio, while “green” resources were ω3-rich and “brown” ω3-poor. Diets with both a narrow C/N ratio and a high ω3-PUFA content are assumed to increase biomass and survival of consumers (Rosenblatt, 2018; Menzel et al., 2018). However, highest Collembola biomass and survival rates were observed in diets containing bacteria (no

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

This work was funded by the German Science Foundation (DFG) with the grant RU 780/12–1 to support the work of JK. We extend gratitude to Kevin Tobias and Alexander Jähngen (Ecology Group, IfB, Humboldt-Universität zu Berlin) for their assistance in the laboratory work. We thank Dr. Kathlin Schweitzer (ADTI, Humboldt-Universität zu Berlin) for access to the experimental station Berlin-Dahlem to gain plant tissue of Helianthus annuus and Solanum tuberosum.

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