Multi-locus DNA metabarcoding of zooplankton communities and scat reveal trophic interactions of a generalist predator

Abstract

To understand the ecosystem dynamics that underpin the year-round presence of a large generalist consumer, the Bryde’s whale (Balaenoptera edeni brydei), we use a DNA metabarcoding approach and systematic zooplankton surveys to investigate seasonal and regional changes in zooplankton communities and if whale diet reflects such changes. Twenty-four zooplankton community samples were collected from three regions throughout the Hauraki Gulf, New Zealand, over two temperature regimes (warm and cool seasons), as well as 20 samples of opportunistically collected Bryde’s whale scat. Multi-locus DNA barcode libraries were constructed from 18S and COI gene fragments, representing a trade-off between identification and resolution of metazoan taxa. Zooplankton community OTU occurrence and relative read abundance showed regional and seasonal differences based on permutational analyses of variance in both DNA barcodes, with significant changes in biodiversity indices linked to season in COI only. In contrast, we did not find evidence that Bryde’s whale diet shows seasonal or regional trends, but instead indicated clear prey preferences for krill-like crustaceans, copepods, salps and ray-finned fishes independent of prey availability. The year-round presence of Bryde’s whales in the Hauraki Gulf is likely associated with the patterns of distribution and abundance of these key prey items.

Modelling the spatial distribution of cetaceans in New Zealand waters

“…This was particularly the case for species which frequently inhabit inshore areas where environmental gradients were steepest. For the more coastal species such as Māui and bottlenose dolphins and Bryde's whales, sufficient nearshore prey is available for year-round populations to persist (Carroll et al, 2019;Constantine, Iwata, Nieukirk, & Penry, 2018;Hartel, Constantine, & Torres, 2014;Miller, Lalas, Dawson, Ratz, & Slooten, 2013). Blue whales frequently aggregate in areas of nearshore upwelling that drive zooplankton productivity during the austral summer months from approximately January to April (Barlow et al, 2018;Torres, 2013 Miller et al, 2013).…”

DNA metabarcoding in diet studies: Unveiling ecological aspects in aquatic and terrestrial ecosystems

“…For instance, the authors recommended the use of universal primers for species inventory and estimates of local species abundances, whereas more specific primers should be preferred for dietary and food web assessments (Boyer et al, ). Although this approach has still limited empirical application and has been mostly viewed as a promising tool (Berry et al, ), a similar methodology has been applied to determine whether fecal samples from the generalist Bryde's whale Balaenoptera edeni brydai could be used as proxies for zooplankton diversity across seasons (Carroll et al, ). However, despite being generalists, Bryde's whales show preferences for certain prey, irrespectively of their availability in the environment, which could result in biased estimates of local prey availability (Carroll et al, ).…”

“…Although this approach has still limited empirical application and has been mostly viewed as a promising tool (Berry et al, ), a similar methodology has been applied to determine whether fecal samples from the generalist Bryde's whale Balaenoptera edeni brydai could be used as proxies for zooplankton diversity across seasons (Carroll et al, ). However, despite being generalists, Bryde's whales show preferences for certain prey, irrespectively of their availability in the environment, which could result in biased estimates of local prey availability (Carroll et al, ). We consider that, as the knowledge on species dietary habits progresses, more informed choices on the biological models will allow successful spatiotemporal biodiversity assessments.…”

“…Comparatively to fecal, DNA from stomach contents is of better quality due to its collection at an earlier stage of digestion. Additionally, although the use of this “biodiversity capsules” method is ideal to study terrestrial ecosystems, it is only applicable to a small fraction of aquatic organisms, such as sea lions (Berry et al, ), as access to scats from other organisms is mostly restricted to opportunistic sampling (Carroll et al, ). In aquatic systems, especially the deep sea, where sampling can be more challenging, the use of gut and stomach contents could be highly valuable as a biodiversity information source.…”

“…However, accounting for and even targeting secondary preyed items, for instance by complementing the sampling of top predator(s) with that of potential prey(s), brings a broader view on species interactions and consequently a better understanding of food webs (Bowser et al, 2013;Galan et al, 2018). In this regard, dDNA approaches simultaneously targeting multiple species (both top predators and prey) (e.g., Bowser et al, 2013;Carroll et al, 2019), combined with environmental samples (e.g., samples from water column and/or soil) to determine prey availability (e.g., Willerslev et al, 2014), can be tremendous robust in providing comprehensive species inventories and provide insights regarding their interactions. We thus predict that in a near future, studies using dDNA will assist on regional and global biodiversity surveys, contributing to the identification of potentially undescribed species (e.g., Corley et al, 2019;de Luna Sales et al, 2019), as well as foster new hypotheses on the hierarchical organization of the trophic webs.…”