Tolerance and sequestration of macroalgal chemical defenses by an Antarctic amphipod: a ‘cheater’ among mutualists

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 cartilagineum 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 species which utilize it as a host in nature. Paradexamine fissicauda maintained on a diet of Plocamium cartilagineum for 2 mo were much less likely to be eaten by fish than Paradexamine fissicauda maintained on a red alga which does not elaborate chemical defenses, or than a different but morphologically similar sympatric amphipod species. Halogenated secondary metabolites produced 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. fissicauda is sequestering the potent chemical defenses of Plocamium cartilagineum for its own use.

Seawater acidification more than warming presents a challenge for two Antarctic macroalgal‑associated amphipods

“…Four pH−temperature treatment combinations were included: current mean ambient (pH 8.0, 1.5°C), reduced pH (pH 7.6, 1.5°C), elevated temperature (pH 8.0, 3.5°C), and combined reduced pH−elevated temperature (pH 7.6, 3.5°C). Based on previous studies of feeding preferences in Antarctic amphi pods (Amsler et al 2005, Amsler et al 2013, both species used in the present study were fed P. decipiens and its associated epiphytic diatoms. Amphipods in each replicate were provisioned with an ad libitum diet of 5 mm dia meter disks of fresh P. decipiens thallus tissue cut with a cork borer.…”

“…To collect the amphi pod Gondogeneia antarctica we targeted collections of the brown macroalga Desmarestia menziesii (Huang et al 2007). To collect the amphipod Paradexamine fissicauda, we targeted collections of Plocamium cartilagineum (Amsler et al 2013). Macro algae and their associated mesograzers were transported to Palmer Station submerged in 19 l buckets of seawater and transferred to 3800 l flowthrough seawater tables.…”

“…Another endemic gammarid amphi pod, Paradexamine fissicauda, also oc curs commonly along the WAP (Crame 2014). Subsequent analyses have found that P. fissicauda consumed its macro algal host and sequestered the alga's deterrent metabolites in its own tissues in order to deter fish predation (Amsler et al 2013). In contrast to G. antarctica, this species is larger, less active (authors' pers.…”

“…obs. ), and exhibits both habitat and feeding specialization, living in association with the chemically defended red macroalga Plocamium cartilagineum (Amsler et al 2013).…”

Hidden Diversity in an Antarctic Algal Forest: Metabolomic Profiling Linked to Patterns of Genetic Diversification in the Antarctic Red Alga Plocamium sp.

“…WAP Plocamium sp. is chemically defended from a variety of herbivores [14,30,33,41,42] but is preyed upon by at least one sympatric herbivore [14,42]. In closely related species of terrestrial plants, it is thought that neighboring plants with differing chemical defensive compounds are less vulnerable to common herbivores, and thus, that possessing rare defense phenotypes increases fitness [43][44][45].…”