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Chilopoda, Geophilomorpha) Using a DNA-Based Approach T Soil Biology and Biochemistry 127 (2018) 223–229 Contents lists available at ScienceDirect Soil Biology and Biochemistry journal homepage: www.elsevier.com/locate/soilbio Comparative analysis of diet in syntopic geophilomorph species (Chilopoda, Geophilomorpha) using a DNA-based approach T ∗ Francesca Bortolin , Giuseppe Fusco, Lucio Bonato Department of Biology, University of Padova, Italy ARTICLE INFO ABSTRACT Keywords: Trophic niche partitioning between potentially competing species within the same coenosis has been little ex- Centipedes plored for most of the major groups of arthropod soil predators, among which are the geophilomorph centipedes. Niche overlap We performed a comparative study in nature on the diet of three species of Geophilomorpha living in the same Niche width site in Southern Europe. Through PCR-based molecular gut content analysis, we estimated trophic niche width Gut content analysis and overlap with respect to three common prey groups: lumbricids, collembolans and dipteran larvae. Results Prey spectrum show that apparently similar geophilomorph species differ significantly in prey spectrum, with quite different Soil food web niche widths. Estimates of predator diet overlap gave moderate values, non-significantly different from null expectations. Within-species diet composition does not vary significantly with sex. This work, while providing the first evidence of trophic niche partitioning among coexisting geophilomorph species, contributes to recent progresses in the understanding of intra-guild interactions between predators in the soil food webs. 1. Introduction requirements (Pekár et al., 2011). Among arthropod soil predators, trophic niche partitioning has been A large number of arthropod generalist predators populate the soil largely investigated in a few groups only, especially spiders, where of temperate forests (Polis, 1994), and guilds of similar species can live coexisting species have been found either to differ in prey use in rela- syntopically despite interspecific competition for prey (e.g., Toju and tion to differences in foraging strategies, in microhabitat or in circadian Baba, 2018; Peretti and Bonato, submitted). Although highly similar activity (e.g., Michalko and Pekár, 2015), or to show substantial niche predator species may avoid competitive exclusion through nearly overlap, possibly explained by environmental constraints (Wirta et al., neutral dynamics (i.e., random demographic mechanisms and processes 2015). However, studies about the trophic interactions that regulate the of spatial dispersal; Hubbell, 2001), several evidences support the idea coexistence of species of other predator major taxa, such as centipedes, that trophic differences are ultimately required for stable coexistence are still lacking. (e.g., Chesson, 2000; Levine and HilleRisLambers, 2009). To reduce We performed a comparative study in nature on the diet of different competition for prey, syntopic predator species can differ in times of species of geophilomorph centipedes. Geophilomorpha are one of the activity, in microhabitat and in the food they consume. This phenom- major groups of predators in the forest soil ecosystems worldwide enon is generally referred to as niche partitioning (Schoener, 1974). (Albert, 1979; Petersen and Luxton, 1982) and up to ca. 20 species have In evaluating trophic niche partitioning, measures of niche overlap been repeatedly found to coexist in the same soil community in tem- quantify the similarity of resources used by different species in terms of perate forests (Grgič and Kos, 2003; Peretti and Bonato, submitted). food consumption (Abrams, 1980). High values of niche overlap suggest Some geophilomorphs live permanently inside the soil (strictly en- high level of interspecific competition (see Krebs, 1999 and reference dogeic species) while others hunt regularly on the soil surface (reg- therein). In parallel, trophic niche width quantifies the range of food that ularly epigeic species). They are supposed to be generalist predators a species uses (Levins, 1968). Extent and composition of trophic niche (e.g., Klarner et al., 2017), feeding on invertebrates of smaller or similar can vary with predator features like size and age, or with season body size, including annelids, molluscs and arthropods (reviewed in: (Bolnick et al., 2011; Haddad et al., 2016). In addition, sex differences Lewis, 1981; Voigtländer, 2011). However, despite their important and in trophic niche can occur, possibly associated to sex-specific strategies widespread ecological role in forest soil ecosystems, very few data are to maximize fitness, through divergent habitat choice or nutritional available on their diet. ∗ Corresponding author. Department of Biology, University of Padova, Via U. Bassi 58/B, I-35131, Padova, Italy. E-mail address: [email protected] (F. Bortolin). https://doi.org/10.1016/j.soilbio.2018.09.021 Received 17 May 2018; Received in revised form 13 September 2018; Accepted 22 September 2018 Available online 24 September 2018 0038-0717/ © 2018 Elsevier Ltd. All rights reserved. F. Bortolin et al. Soil Biology and Biochemistry 127 (2018) 223–229 In recent years, significant methodological advances have been litter and soil, and by turning stones, pieces of wood and barks found on made for studying feeding interactions in the soil webs, opening new the ground. The centipedes were fixed in 100% ethanol immediately prospective in trophic ecology. Fatty acids (FAs) can be traced over upon collection. more than one trophic level, allowing to distinguish energy channels An additional species, Pleurogeophilus mediterraneus, was sampled in based on bacteria from those based on fungi in the soil (Pollierer et al., a site with similar habitat and climatic conditions (Monte Castello, near 2010). FAs analysis carried out on two geophilomorph species and two Monselice, 45.2556° N, 11.7368° E, only 4 km apart from the other other centipede species from a forest soil community showed different study area), during the same period (3 days in spring and 1 in autumn) FA composition between species, suggesting trophic niche differentia- and with the same methodology. Some specimens of P. mediterraneus tion (Ferlian et al., 2012). This approach can contribute to uncover the were kept alive until they reached the laboratory, where their gut was food web structure, but it is not sensitive enough to accurately define dissected and fixed in RNAlater (Sigma Aldrich, St. Louis, USA) at the prey spectrum of different predators. Instead, DNA-based gut con- −20 °C. The two storage methods (100% ethanol and RNAlater) gave tent analysis allows the taxonomic identification of prey from small DNA with comparable concentration and purity (considering A260/280 amounts of DNA detected in the predator gut, and is particularly useful and A260/230 absorbance values). for determining the prey spectrum in fluid-feeding predators Species were identified using ChiloKey (Bonato et al., 2014) and sex (Pompanon et al., 2012), like geophilomorphs (see Koch and was determined based on gonopod morphology (Minelli, 2011). Head Edgecombe, 2012). DNA-based studies have been carried out on a few maximum width, used as a proxy for body size and age, was measured geophilomorphs and other centipedes through feeding laboratory ex- by means of a micrometre applied to a microscope to the nearest 10 μm. periments. These have shown that specific characteristics of the pre- In order to reduce the expected intraspecific variation of diet asso- dator (such as the feeding mode) as well as of the prey (such as the ciated with body size and/or age (Eitzinger et al., 2018), we considered tissue physicochemical qualities) may influence the post-feeding timing only adult and subadult specimens with head width in the following of DNA degradation, and thus the efficacy of the method in detecting species-specific ranges (from the minimum size, up to twice the prey DNA (Waldner et al., 2013; Eitzinger et al., 2014). However, it minimum size): 400–800 μm for H. vesuviana and S. gracilis, remains largely unexplored whether these insights may be generalized 1200–2400 μm for H. gabrielis and 800–1600 μm for P. mediterraneus. to other prey and predator species, and also to a natural environment context. Indeed, DNA-based gut content analyses have been carried out 2.2. DNA extraction on some centipede species in the field (Günther et al., 2014; Eitzinger et al., 2018), but diet differences between coexisting geophilomorph DNA was extracted from the dissected gut of large geophilomorph species have not been investigated so far. specimens, in order to reduce carry-over contamination from the an- We used a PCR-based gut content analysis to comparatively in- imal body surface. Differently, for smaller specimens, DNA was ex- vestigate predation, through determining trophic niche width and tracted from the intermediate portion of the body trunk, as accurate gut overlap, in a sample of species of geophilomorphs living in the same dissection was problematic. Dissection was executed by a single person site. Specifically, we analysed the frequency of detection of earthworms (FB) under sterile conditions, using flamed instruments. (Lumbricidae), springtails (Collembola) and fly larvae (Diptera), which DNA extraction was performed using the DNeasy Blood and Tissue are usually reported as the most frequently exploited prey groups (e.g., kit (Qiagen, Hilden, Germany) and negative controls (i.e., no animal Eitzinger et al., 2018). At the intraspecific level, we tested for variation tissue) were included
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