Collembola as alternative prey sustaining spiders in arable ecosystems: prey detection within predators using molecular markers

Abstract

Collembola comprise a major source of alternative prey to linyphiid spiders in arable fields, helping to sustain and retain these predators as aphid control agents within the crop. Polymerase chain reaction primers were developed for the amplification, from spider gut samples, of DNA from three of the most abundant species of Collembola in wheat crops in Europe, namely Isotoma anglicana, Lepidocyrtus cyaneus and Entomobrya multifasciata. The primers amplified fragments of the mitochondrial cytochrome oxidase subunit I (COI) gene and were designed following alignment of comparable sequences for a range of predator and prey species. Each of the primer pairs proved to be species-specific to a Collembola species, amplifying DNA fragments from 211 to 276 base pairs in length. Following consumption of a single collembolan, prey DNA was detectable in 100% of spiders after 24 h of digestion. We report the first use of DNA-based techniques to detect predation by arthropods on natural populations of prey in the field. All three species of Collembola were consumed by the spiders. By comparing the ratios of the Collembola species in the field with the numbers of spiders that gave positive results for each of those species, it was possible to demonstrate that the spiders were exercising prey choice. Overall, a single target species of Collembola was eaten by 48% of spiders while a further 16% of spiders contained DNA from two different species of Collembola. Preference was particularly evident for I. anglicana, the species most frequently found in spider guts yet the least numerous of the three target species in the field.

Molecular analysis of the gut contents of Harmonia axyridis (Coleoptera: Coccinellidae) as a method for detecting intra-guild predation by this species on aphidophagous predators other than coccinellids

“…This is in agreement with similar studies on different predator groups (e.g. Agusti et al, 2003;Hosseini et al, 2008). The half-life of the period for which prey DNA could be detected for each predator-prey combination ranged from 8.9 to 52.4 h; the long half-life for fourth instar H. axyridis feeding on C. carnea indicates it is possible to detect relatively rare predation events (Gagnon et al, 2011a).…”

“…The primers also amplified sequences shorter than 250 bp. Amplifying a short DNA sequence of a target gene present in multiple copies in the cell has resulted in an increase in the likelihood of detecting the DNA of prey in the gut of a predator (Zaidi et al, 1999;Agusti et al, 2003).…”

Do spiders respond to global change? A study on the phenology of ballooning spiders in Switzerland

“…In our study, the Linyphiidae family, which is known to be susceptible to desiccation, represents 76% of all species in this group (Topping & Sunderland, 1998;Kumschick et al, 2009). Additionally, it is possible that mortality increased due to reductions in the populations of important prey like Collembola (Agustí et al, 2003;Nyffeler & Sunderland, 2003), which were shown by Aebischer (1991) to collapse during dry summers, and take 3 to 5 y to recover. Finally, the ballooning propensity and efficiency of spiders can decline with high temperatures (Reynolds, Bohan & Bell, 2007;Bonte et al, 2008).…”

Quantifying aphid predation rates of generalist predators in the field

“…Molecular markers have been utilized in entomology for many years (Loxdale & Lushai, 1998) but only recently have DNA-based approaches been applied to study invertebrate predation in the field (Agustí et al, 2003;Harper et al 2005). However, this is likely to change in light of the numerous laboratory studies which have demonstrated the ability to detect DNA remains within predator guts (Zaidi et al, 1999;Chen et al, 2000;Hoogendoorn & Heimpel, 2001;Cuthbertson et al, 2003;Grenstone & Shufran, 2003;Sheppard et al, 2004).…”

“…The application of multiplex-PCR's to separate species (Hinamoto et al, 2004) and its ability to simultaneously amplify degraded mitochondrial DNA of different prey (Harper et al, 2005) implicate these molecular techniques as having distinct advantages to biochemical analyses which have, to date, relied on running multiple assays against each target prey. Agustí et al (2003) designed primers to amplify fragments of the mitochondrial cytochrome oxidase subunit I gene to detect predation by linyphiid spiders on six species of Collembola in winter wheat. Following characterization of the primer system, spiders were collected and guts amplified by polymerase chain reaction.…”