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Deterrent Activities in the Crude Lipophilic Fractions

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Deterrent Activities in the Crude Lipophilic Fractions RESEARCH/REVIEW ARTICLE Deterrent activities in the crude lipophilic fractions of Antarctic benthic organisms: chemical defences against keystone predators Laura Nu´n˜ ez-Pons & Conxita Avila Department of Animal Biology (Invertebrates) & Biodiversity Research Institute, Faculty of Biology, University of Barcelona, Av. Diagonal 643, ES-08028 Barcelona, Catalonia, Spain Keywords Abstract Antarctic invertebrates; Antarctic algae; chemical ecology; sea star Odontaster Generalist predation constitutes a driving force for the evolution of chemical validus; amphipod Cheirimedon femoratus; defences. In the Antarctic benthos, asteroids and omnivore amphipods are chemical defence. keystone opportunistic predators. Sessile organisms are therefore expected to develop defensive mechanisms mainly against such consumers. However, the Correspondence different habits characterizing each predator may promote variable responses Laura Nu´ n˜ ez-Pons, Department of Animal in prey. Feeding-deterrence experiments were performed with the circumpolar Biology (Invertebrates) & Biodiversity asteroid macropredator Odontaster validus to evaluate the presence of defences Research Institute, Faculty of Biology, University of Barcelona, Av. Diagonal 643, within the apolar lipophilic fraction of Antarctic invertebrates and macroalgae. ES-08028 Barcelona, Catalonia, Spain. A total of 51% of the extracts were repellent, yielding a proportion of 17 E-mail: [email protected] defended species out of the 31 assessed. These results are compared with a previous study in which the same fractions were offered to the abundant circum-Antarctic amphipod Cheirimedon femoratus. Overall, less deterrence was reported towards asteroids (51%) than against amphipods (80.8%), principally in sponge and algal extracts. Generalist amphipods, which establish casual hostÁprey sedentary associations with biosubstrata (preferentially sponges and macroalgae), may exert more localized predation pressure than sea stars on certain sessile prey, which would partly explain these results. The nutritional quality of prey may interact with feeding deterrents, whose production is presumed to be metabolically expensive. Although optimal defence theory posits that chemical defences are managed and distributed as to guarantee protection at the lowest cost, we found that only a few organisms localized feeding deterrents towards most exposed and/or valuable body regions. Lipophilic defensive metabolites are broadly produced in Antarctic commu- nities to deter opportunistic predators, although several species combine different defensive traits. Predation constitutes an interaction in which an organism have no known primary metabolic function. These are attacks another, resulting in its eventual digestion. In prey considered secondary metabolites and are presumably with clonal growth, predation normally occurs only on a costly but essential for fitness. Anti-feedant chemical part of the victim, rarely invoking death (Heck & Valentine defences have been described in marine organisms, such 1995; Sa´nchez et al. 2004). After sub-lethal attacks, this as phlorotannins and terpene alcohols in algae, alkaloids type of prey may respond with plastic anti-predatory in poriferans and dithiocarbamates in hydrozoans, which behaviour, morphology or chemistry, or a combination decrease the vulnerability of susceptible prey to future (Harvell 1984; Vermeij 1994). One efficient weapon attacks (Cronin & Hay 1996; Lindquist 2002; Thoms et al. against predation is chemical defence. Many natural 2007; Toth et al. 2007). Chemical defences are an invest- substances that display allelochemical (signalling) roles ment, as organisms must divert energy otherwise assigned Polar Research 2014. # 2014 L. Nu´ n˜ ez-Pons & C. Avila. This is an Open Access article distributed under the terms of the Creative Commons Attribution-Noncommercial 1 3.0 Unported License (http://creativecommons.org/licenses/by-nc/3.0/), permitting all non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. Citation: Polar Research 2014, 33, 21624, http://dx.doi.org/10.3402/polar.v33.21624 (page number not for citation purpose) Chemical defences towards Antarctic keystone predators L. Nu´ n˜ ez-Pons & C. Avila to growth or reproduction and its cost is compensated by larger wandering predators, such as echinoderms or fish greater survival potential (Harvell 1990). Several theories (Hay et al. 1987; McClintock & Baker 2001; Toth et al. have been formulated to explain where energy is saved 2007). and the costs of chemical defence minimized. The optim- Sea stars feed by extruding the cardiac stomach against ality theory (OT) proposes the use of all-purpose defensive their food items (Sloan 1980; Brusca & Brusca 2003). tactics against a variety of enemies (Herms & Mattson Hence, in Antarctic waters, where sea stars are keystone 1992). The optimal defence theory (ODT) postulates that predators (McClintock 1994), ODT would predict that deterrent metabolites are directed to particular types of defences would be concentrated primarily in the outer- predator and that they work together with other defensive most body parts of prey. However, it should be noted traits to assure survival. According to the ODT, defensive that other effective consumers of smaller size, like small chemicals are allocated to the most valuable or vulnerable crustaceans, may promote different types of defence tissues (Rhoades & Gates 1976). distribution, especially in prey with large body perfora- The mechanisms by which defensive metabolites tions (i.e., oscula), like hexactinellid sponges that may be promote predation avoidance are still unknown since attacked from the inside (Peters et al. 2009). many are not highly poisonous but instead seem to have In Antarctic marine organisms, measures to deter an effect promoting bad taste (Paul 1992; McClintock & consumption have been well documented by research Baker 2001). Nutritional quality must also be taken into using sea stars as model consumers; however, post- consideration since some repellents are more (or only) ingestion repulsive reactions have been scarcely tested effective in low-quality foods. This is likely because (for reviews see Avila et al. 2008; McClintock et al. 2010; nutrients may bind to deterrent molecules or compete Taboada et al. 2012). The current study evaluates the with these for enzymes, masking the stimuli that elicit palatability of Antarctic benthic invertebrates and algae rejection (Duffy & Paul 1992; Cruz-Rivera & Hay 2003). with respect to the sympatric asteroid predator, Odontaster Hence, highly nutritive potential prey likely require validus. Our past research has focused on the ecological larger amounts of, or more potent, defences to avoid role of lipidic metabolites in Southern Ocean organisms, consumption, while prey items of lower nutrient content in part because known feeding deterrents in marine tend to develop weaker defensive systems. For this environments are mostly lipid-soluble (Sotka et al. reason, there are also costs for consumers: because they 2009). In this study, we sought to evaluate defensive may need energetically expensive detoxification me- strategies developed against a common consumer*O. chanisms when ingesting chemically defended organ- validus*in Antarctic waters by using the lipophilic isms, they often eat poor-quality foods made up of fractions of selected organisms to determine the presence undefended organisms (Hay et al. 1987; Lindquist & of apolar defences and the hypothetical within-body Hay 1995; Cruz-Rivera & Hay 2003). By consuming small allocation of deterrents. The results are discussed and amounts of a variety of foods, predators may dilute the compared with previous experiments with another im- possible negative effects derived from ingesting defen- portant predator, the amphipod Cheirimedon femoratus. sive metabolites, while also accruing the nutritional benefits derived from a mixed diet (Bernays et al. 1994; Materials and methods Stachowicz et al. 2007; Sotka et al. 2009). As generalist predators are more prevalent, defences tend to be de- Field collection of Antarctic benthic samples veloped against them as opposed to specialists (Paul et al. 2007). Benthic invertebrates and algae were collected during Antarctic sea floors are characterized by unpredictable four Antarctic cruises: two in the Eastern Weddell Sea on food availability, driving most consumers to develop board the RV Polarstern (ANT XV/3 and ANT XXI/2 flexible opportunistic foraging strategies. There is a pre- cruises); a third one on board the RV BIO Hespe´rides dominantly circumpolar distribution of many of the around the South Shetland Islands (ECOQUIM-2 cruise); dominant benthic organisms including keystone macro- and the fourth at Deception Island (ACTIQUIM-1 invertebrate predators, mainly asteroids (Dayton et al. campaign). Sampling took place at a total of 24 stations 1974; McClintock 1994). Populations of amphipods with between 0 and 1524 m depth by using bottom and diversified diets are found in extremely high densities in Agassiz trawls (AGTs) and an epibenthic sledge (ES) and, association with biosubstrata, which often represent their at shallow sites, by scuba diving (SD). At collection, all potential prey as well as their shelter (see De Broyer et al. invertebrate and macroalgal samples exhibited a healthy, 2007 for a review). In this case, small sedentary consumers fresh appearance; none of them showed signs of decom- could constitute
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