Trophic ecology of groundwater species reveals specialization in a low‐productivity environment

Abstract

International audience1. Identifying feeding strategies at lower bounds of habitat productivity is fundamental to understand the relationship between energy availability and trophic specialization. Low pro- ductivity is expected to severely constrain trophic specialization because organisms may no longer be able to fulfil their energy requirements by feeding on a reduced set of resources. However, species living in low-productivity habitats often exhibit particular biological traits such as low metabolic rates and high food-finding abilities, which may release constraints on trophic specialization.2. In the present study, we used carbon (C) and nitrogen (N) stable isotopes to measure the degree of trophic specialization in two species of isopods (Proasellus valdensis and Proasellus cavaticus) living in groundwater, one of the most energy-limited environments on earth. Fun- damental specialization was obtained from a 13C/15N-labelling experiment in the laboratory: we measured separately the carbon and nitrogen assimilation rates of the two species across the three food sources encountered in their natural cave habitats (fine and coarse particulate organic matter and sedimentary biofilm). Then, for each species, we tested for variation in diet composition among individuals and populations by quantifying the relative contribution of the three food sources to the diet of multiple individuals within 5 cave populations.3. The labelling experiment showed that both species assimilated about 10 times more carbon and at least 4 times more nitrogen from sedimentary biofilm than from both forms of particu- late organic matter. Field samplings showed that sedimentary biofilm made up, on average, 83% of the diet of isopods. Moreover, we found almost no variation in diet among individuals of a cave population as well as among cave populations within species.4. This study provides the first evidence of a high degree of trophic specialization in a low- productivity cave environment. Both species exhibited a strong fundamental specialization on sedimentary biofilm and most probably fed selectively on this food source in their natural environment. Our findings challenge the prediction that species would adopt generalist feeding strategies at lower bounds of habitat productivity

Niches within a niche: ecological differentiation of subterranean amphipods across Europe's interstitial waters

“…In this last scenario, interspecific competition leads to ecological differentiation (Schluter 2000, Martin and Pfennig 2009, Pfennig and Pfennig 2010, reducing the relative importance of interspecific competition as compared to intraspecific competition (Chesson 2000). In subterranean species, possible differentiations include adaptations to physical-chemical conditions of subterranean microhabitats, spatial segregation within a single locality (Trontelj et al 2012, Delić et al 2016, Mammola and Isaia 2016, and differential resource-use (Vergnon et al 2013, Hutchins et al 2014, Francois et al 2016. In such an ecological niche differentiation scenario, subterranean organisms may experience both convergent and divergent selection due to similar environmental conditions and interspecific competition for the limited resources, respectively.…”

Trophic plasticity among spring vs. cave populations of Gammarus minus: examining functional niches using stable isotopes and C/N ratios

“…Although the bulk leaf tissue d 15 N reflects plant tissue N, it also reflects the nutritionally important biofilm (Francois et al 2015), which is also 15 N-depleted. Regardless whether leaf tissue or biofilm is their N source, the data clearly indicates surface populations of G. minus are not predaceous.…”

“…This species inhabits both surface spring runs and cave stream environments throughout the Appalachians (Culver et al 1995), with different cave populations having evolved independently from surface populations (Carlini et al 2009). Surface populations of G. minus, usually classified as ''detritivore'' or ''shredder'', readily skeletonized leaves but derived their nutrition from the bacteria and fungi that have colonized the decaying leaves (Kostalos and Seymour 1976;Francois et al 2015). Cave populations of G. minus may obtain part of their nutrition in a similar way because they also skeletonize leaves in the laboratory (Culver et al 1995;Fong personal observation).…”

Finding answers in the dark: caves as models in ecology fifty years after Poulson and White

“…Up to now, characterizations of subterranean trophic webs have been few and mostly focused on specific habitats, including different cave aquatic environments (Culver 1985, Simon et al 2003, Venarsky et al 2014, Francois et al 2016, sulfur-based caves (Barton andNorthup 2007, Chen et al 2009) and guano-rich caves (Ferreira and Martins 1999). However, no one has yet attempted to construct a comprehensive ecological network representing the interactions between all the biological actors playing a role in a subterranean trophic web.…”

“…However, no one has yet attempted to construct a comprehensive ecological network representing the interactions between all the biological actors playing a role in a subterranean trophic web. Nonetheless, the possibility to obtain large amounts of data from stable isotopes (Simon et al 2003, Francois et al 2016, metagenomic tools (Ortiz et al 2014) and manipulative experiments (Schneider et al 2011, Venarsky et al 2012b and to rely on a wide variety of modern analytical tools able to realistically parameterize the complexity of ecological networks (Proulx et al 2005, Baselga and Araújo 2009, Morales-Castilla et al 2015, Grimm et al 2017, yields a great potential for deciphering the intricate food web of predator and prey interactions in subterranean systems. The exploration of differences between trophic webs in cave and subsurface habitats may hold promise for unlocking some of the unresolved questions in general network theory, in particular the study of nature and ramifications of the networks and the quantification of the importance of rare species in the functioning of ecological communities (Sutherland et al 2013).…”