Molecular detection of trophic interactions: emerging trends, distinct advantages, significant considerations and conservation applications

Abstract

The emerging field of ecological genomics contains several broad research areas. Comparative genomic and conservation genetic analyses are providing great insight into adaptive processes, species bottlenecks, population dynamics and areas of conservation priority. Now the same technological advances in high-throughput sequencing, coupled with taxonomically broad sequence repositories, are providing greater resolution and fundamentally new insights into functional ecology. In particular, we now have the capacity in some systems to rapidly identify thousands of species-level interactions using non-invasive methods based on the detection of trace DNA. This represents a powerful tool for conservation biology, for example allowing the identification of species with particularly inflexible niches and the investigation of food-webs or interaction networks with unusual or vulnerable dynamics. As they develop, these analyses will no doubt provide significant advances in the field of restoration ecology and the identification of appropriate locations for species reintroduction, as well as highlighting species at ecological risk. Here, I describe emerging patterns that have come from the various initial model systems, the advantages and limitations of the technique and key areas where these methods may significantly advance our empirical and applied conservation practices.

Keywords: conservation biology; ecological genetics; metabarcoding; molecular dietary analysis; species interactions.

Figure 1

A wide variety of interactions occur in nature and all cases leave behind traces of environmental DNA. Clockwise starting at top left, DNA from crushed insects (B, C, D) in faeces can identify the insect prey and the predators DNA is present in traces, bees carry pollen, which provides plant DNA, parasites blood meals are a source of DNA from visited animals, chewed seeds have saliva and deposited seeds epithelial cells, which can be used to identify the dispersing animal (Photographs used with permission: mosquito – M. Brock Fenton, bee – L. Packer and Bee Tribes of the World, all others E.L. Clare).

Figure 2

The analytical chain for molecular analysis. High-throughput sequencing platforms coupled with the public databases of sequences from a wide variety of taxa allow us to document species interactions. An unobserved event can be identified by sequencing eDNA (e.g. from pollen on a bat). The resulting unknown sequence can be compared against collections of taxonomically validated references for species-level documentation of the ecological event. This enables large-scale measurements of species’ interactions to be partly automated. The resulting databases can be used to quantitatively measure a variety of ecologically and evolutionarily important events, such as the relative niche flexibility of taxa, competition between taxa or the response of an ecological system to disruption. For example, resource use by bats in Jamaican cave systems have been a particular target of molecular studies (Emrich et al. 2014). Photographs used with permission: mosquito – M. Brock Fenton, bat with pollen – J. Nagel, fox snake – C. Davy all others E.L. Clare.

Figure 3

Conservation in action. The application of molecular detection of trophic links is already gaining specific conservation attention. Clockwise from upper left: to look at potential competition for resources between native skinks and invasive shrews on Ile aux Aigrettes, to determine mechanisms of range limitation in smooth snakes and for managed reintroductions of the endangered snail Powelliphanta augusta. Photographs used with permission: skink and shrew – Nik Cole – Durrell/MWF, smooth snake – W.O. Symondson, P. augusta – Stephane Boyer.

Figure 4

The accumulation of molecular data to assess species inventories has given us the capacity to assemble high-resolution measures of ecological structure such as food webs. From these, we can measure specific aspects of biological function such as specific cases in functional ecology. However, the analytical continuum should also allow us to use functional ecological principles to predict aspects of network structure, expected species interactions and in turn actually predict or identify missing species from inventories. This last point is critical in conservation biology allowing us to identify key factors promoting species vulnerability or persistence (Photographs used with permission: M. Brock Fenton).