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Tolerance and Sequestration of Macroalgal Chemical Defenses by an Antarctic Amphipod: a ‘Cheater’ Among Mutualists

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Tolerance and Sequestration of Macroalgal Chemical Defenses by an Antarctic Amphipod: a ‘Cheater’ Among Mutualists Vol. 490: 79–90, 2013 MARINE ECOLOGY PROGRESS SERIES Published September 17 doi: 10.3354/meps10446 Mar Ecol Prog Ser FREEREE ACCESSCCESS Tolerance and sequestration of macroalgal chemical defenses by an Antarctic amphipod: a ‘cheater’ among mutualists Margaret O. Amsler1, Charles D. Amsler1,*, Jacqueline L. von Salm2, Craig F. Aumack1,3, James B. McClintock1, Ryan M. Young2, Bill J. Baker2 1Department of Biology, University of Alabama at Birmingham, Birmingham, Alabama 35294-1170, USA 2Department of Chemistry, University of South Florida, Tampa, Florida 33620, USA 3Present address: Department of Biology and Paleo Environment, Lamont-Doherty Earth Observatory, Palisades, New York 10964-8000, USA ABSTRACT: Shallow-water communities along the western Antarctic Peninsula support forests of large, mostly chemically defended macroalgae and dense assemblages of macroalgal-associated amphipods, which are thought to exist together in a community-wide mutualism. The amphipods benefit the chemically defended macrophytes by consuming epiphytic algae and in turn benefit from an associational refuge from fish predation. In the present study, we document an exception to this pattern. The amphipod Paradexamine fissicauda is able to consume Plocamium carti- lagineum and Picconiella plumosa, 2 species of sympatric, chemically defended red macroalgae. In previous studies, Plocamium cartilagineum was one of the most strongly deterrent algae in the community to multiple consumers, and was found here to be unpalatable to 5 other amphipod spe- cies which utilize it as a host in nature. Paradexamine fissicauda maintained on a diet of Ploca - mium cartilagineum for 2 mo were much less likely to be eaten by fish than Paradexamine fissi- cauda maintained on a red alga which does not elaborate chemical defenses, or than a different but morphologically similar sympatric amphipod species. Halogenated secondary metabolites pro- duced by Plocamium cartilagineum were identified from tissues of the Paradexamine fissicauda that had eaten it but not those which had eaten the undefended red alga. This indicates that P. fissi- cauda is sequestering the potent chemical defenses of Plocamium cartilagineum for its own use. KEY WORDS: Chemical defenses · Macroalgae · Amphipods · Sequestration · Antarctic ecology Resale or republication not permitted without written consent of the publisher INTRODUCTION Subtidal communities on hard substrata along the western Antarctic Peninsula support lush undersea Small consumers, generally referred to as meso- macroalgal forests which are dominated by large, herbivores or mesograzers, can have major influ- perennial brown algae (Wiencke & Amsler 2012) and ences on the composition and/or structure of marine which support exceptionally dense amphipod assem- communities (Brawley 1992, Heck & Valentine 2006, blages (Richardson 1971, 1977, Huang et al. 2007, Hillebrand 2009). This is particularly true with Aumack et al. 2011a). Estimated amphipod densities respect to macroalgal-associated amphipods (Duffy range up to tens to hundreds of thousands of & Hay 1991, 2000), which can have positive, nega- amphipods per m2 of the bottom in pure stands of tive, or neutral impacts on their host macrophytes their preferred macroalgal hosts (Amsler et al. 2008). (e.g. Duffy 1990, Buschmann & Vergara 1993, Sotka Most of the macroalgae, including all of the ecologi- et al. 1999, Poore et al. 2009). cally dominant taxa, are chemically defended from *Corresponding author. Email: [email protected] © Inter-Research 2013 · www.int-res.com 80 Mar Ecol Prog Ser 490: 79–90, 2013 being consumed by both macrograzers and meso- the algae provide a refuge from omnivorous fish grazers (Amsler et al. 2005, 2008, 2009a, Aumack et predators. Along the western Antarctic Peninsula, al. 2010). Amphipods and other small marine grazers densities of amphipods during daylight hours can be can benefit from associating with chemically de - orders of magnitude higher on chemically defended fended macroalgae because the algae can provide a macrophytes, particularly those with branching refuge from omnivorous macrograzers such as fish morpho logy, than on palatable macroalgae (Huang (Hay 1992, 1996). The relative mobility of the meso- et al. 2007). Amphipod densities on Desmarestia grazers, morphology of the macroalgae, and geo- menziesii, a chemically defended macrophyte sup- graphic location also are important (Holmlund et al. porting the greatest daytime amphipod densities, 1990, Duffy & Hay 1994, Taylor & Steinberg 2005, significantly decrease at night (Aumack et al. 2011a) Zamzow et al. 2010). In some cases the mesograzers when visual predators such are fish are less of a may be dietary specialists on the chemically de - threat, while amphipod densities on blade-forming, fended macroalgae (Hay 1992). Such dietary special- chemically defended macrophytes and on palatable ists not only benefit from an associational refuge macrophytes increase. Zamzow et al. (2010) demon- from predators but also in having an additional food strated that amphipods associated with D. menziesii source (cf. Sotka & Whalen 2008). were less susceptible to predation from the domi- Herbivore specialization on chemically defended nant, omnivorous fish than were amphipods associ- prey necessitates a mechanism for tolerating the ated with a non-defended macrophyte. host’s defensive secondary metabolites. Terrestrial Although these Antarctic amphipods do not appear herbivores are able to tolerate plant secondary meta- to consume most host macroalgae, they consume bolite defenses via a range of behavioral and meta- large quantities of epiphytic diatoms (Aumack 2010, bolic processes (Després et al. 2007). There are far Aumack et al. 2011b) which almost certainly benefits fewer studies of tolerance in marine herbivores, but their hosts. Many studies throughout the world have the mechanisms of metabolic tolerance are similar shown that amphipods and other mesograzers can (Sotka & Whalen 2008). In both terrestrial and marine benefit their host macrophytes in this manner by herbivores, metabolic tolerance of lipophilic meta - limiting the growth of epiphytic microalgae and/or bolites is commonly mediated by all or part of a filamentous algae, which can compete with the 3-phase pathway involving cytochrome P450s, glu- macrophytes for light and nutrients (e.g. Brawley & tathione S-transferases, and ATP binding cassette Adey 1981, Shacklock & Doyle 1983, D’Antonio 1985, transporters, in which the metabolites are made more Brawley & Fei 1987, Duffy 1990, Jernakoff et al. hydrophilic and then isolated into vesicles or ex cre - 1996). Although less studied, mesograzers can also ted (reviewed by Karban & Agrawal 2002, Sorensen influence filamentous algae growing endophyticly. et al. 2006, Després et al. 2007, Sotka & Whalen 2008). Parker & Chapman (1994) reported that when meso- In addition to tolerating prey chemical defenses, grazers were excluded from tide pools dominated by some terrestrial arthropods (insects, particularly in the brown alga Fucus distichus, fatal, pathogenic the Coleoptera and Lepidoptera) and vertebrates effects of otherwise unapparent filamentous algal (primarily amphibians, reptiles, and birds) are able endophytes drastically reduced the macroalgal sequester chemical defenses from prey organisms canopy. within their tissues for use as defenses against their Free-living filamentous algae, epiphytic or other- own predators (Blum 1983, Nishida 2002, Opitz & wise, are very uncommon in subtidal communities Muller 2009, Savitzky et al. 2012). Many species of along the western Antarctic Peninsula (Peters 2003) marine opisthobranch molluscs similarly not only tol- even though they are commonly present in adjoining erate chemical defenses of their prey but are able to intertidal areas (e.g. Delépine et al. 1966, Hedgpeth sequester them for their own use (Cimino & Ghiselin 1969, Chung et al. 1994, Kim 2001). However, fila- 2009). However, we are not aware of reports of this mentous algal endophytes growing within the larger, occurring in any taxon of marine grazers other than chemically defended macroalgae are unusually com- opisthobranchs. The metabolic mechanisms res pons - mon (Peters 2003, Amsler et al. 2009b). Peters (2003) ible for sequestration are less studied than for toler- hypothesized that the high densities of macroalgal- ance, but include selective transport and storage of associated amphipods in these Antarctic communi- the defensive metabolites (Després et al. 2007). ties were preventing the growth of free-living fila- As with amphipods from lower latitudes, Antarctic ments while selecting for an endophytic growth form, amphipods appear to benefit from associating with and this has been supported by experimental field, their chemically defended macroalga hosts because laboratory, and mesocosm studies (Amsler et al. Amsler et al.: Sequestration of chemical defenses 81 2009b, 2012, Aumack et al. 2011b). Consequently, The first goal of the present study was to test the the dense assemblage of chemically defended Ant - hypothesis that the amphipod Paradexamine fissi- arctic macroalgae benefits from the dense assem- cauda is unique among common amphipods in the blage of amphipods associated with it because the community in being able to consume chemically amphipods limit the growth of both unicellular and defended macroalgae, particularly Plocamium carti- filamentous epibionts on the macroalgae. lagineum. After discovering that this is indeed the Since both the chemically defended macroalgae
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