Ambiguous role of phlorotannins as chemical defenses in the brown alga Fucus vesiculosus

Abstract

Brown seaweeds (Fucales) produce phlorotannins that are often considered chemical defenses against herbivores. The many correlative and fewer direct tests conducted have shown effects of phlorotannins on herbivore feeding behavior to be variable. In an attempt to clarify the roles of phlorotannins versus other metabolites in defending brown algae, we conducted bioassay-guided fractionation of herbivore-deterrent extracts from the commonly studied brown alga Fucus vesiculosus. Feeding by the amphipods Ampithoe valida and A. longimana and the sea urchin Arbacia punctulata was suppressed by crude and water-soluble extracts of F. vesiculosus, but this deterrence was lost following storage or fractionation of the active, water-soluble extract. Phlorotannins in these extracts did not decompose in parallel with the loss of feeding deterrence. F. vesiculosus phlorotannins were fed to herbivores at 3 to 12 × the isolated yield (or 4.2 to 16.8% of plant dry mass). No herbivore was deterred from feeding by concentrations of 3 or 6 ×, but A. valida (the only test herbivore that readily consumes F. vesiculosus in the field) was deterred at 12 × isolated yield. When juvenile A. valida were raised on an artificial diet containing F. vesiculosus phlorotannins at 3 × isolated yield, the phlorotannin-rich diet significantly enhanced, rather than reduced, amphipod survivorship and growth relative to an equivalent diet without phlorotannins. Females ovulated only on the phlorotannin-rich diet. Compounds other than phlorotannins appear to defend the F. vesiculosus populations we investigated, but we were unable to identify these unstable compounds.

Testing for the induction of anti-herbivory defences in four Portuguese macroalgae by direct and water-borne cues of grazing amphipods

“…Algal palatability after induction of phlorotannins stimulated (Pavia et al 1997), decreased, or did not affect seaweed consumption by the mesograzers Littorina obtusata or Idotea granulosa. Also, even at elevated concentrations, phlorotannins lack repulsive effects against at least some mesograzers, including amphipod species (Kubanek et al 2004). The rigorous bioassay guided study of Deal et al (2003) revealed that F. vesiculosus compounds, which were repulsive to urchins, were neither within the phlorotannin-nor the DCM-soluble fraction.…”

Seasonal variation in kelp phlorotannins in relation to grazer abundance and environmental variables in the Alaskan sublittoral zone

“…Briefly, phlorotannin standards were made by grinding (Power Gen 500 homogenizer; Fisher Scientific, Hampton, NH, USA) and extracting frozen kelp tissee Arnold 1998, Amsler andFairhead 2006). The function and effectiveness of phlorotannins as feeding deterrents may differ by algal and herbivore species, with some studies demonstrating grazing reduction or inhibition (Geiselman andMcConnell 1981, Pavia andToth 2000a) and others showing negligible responses or even increased herbivory (Steinberg and van Altena 1992, Deal et al 2003, Kubanek et al 2004.…”

“…Briefly, phlorotannin standards were made by grinding (Power Gen 500 homogenizer; Fisher Scientific, Hampton, NH, USA) and extracting frozen kelp tissee Arnold 1998, Amsler andFairhead 2006). The function and effectiveness of phlorotannins as feeding deterrents may differ by algal and herbivore species, with some studies demonstrating grazing reduction or inhibition (Geiselman and McConnell 1981, Pavia andToth 2000a) and others showing negligible responses or even increased herbivory (Steinberg and van Altena 1992, Deal et al 2003, Kubanek et al 2004.Phlorotannin content in brown algae can be regulated by a variety of abiotic and biotic variables, with large species-specific variability in responses to these factors (reviewed by Amsler and Fairhead 2006), which may act synergistically to affect distribution of phlorotannins within species and within thalli (e.g., Hay 1996, Targett and Arnold 1998). Phlorotannin content may be influenced by temporal variability in physical factors such as irradiance Toth 2000b, Cruces et al 2012), salinity (reviewed by Ragan and Glombitza 1986), nutrients (Yates and Peckol 1993, Cronin and Hay 1996, Svensson et al 2007, and water movement (Dayton 1985).…”

Geographic variation in seaweed induced responses to herbivory

“…These responses are likely to have a major impact on the population biology and life history of the inducing consumer because they suppress both herbivore feeding and egg hatching rates (Toth et al 2005). The underlying mechanism of induction observed in these studies may involve chemical defenses of A. nodosum because (1) artificial foods made from induced seaweeds lacking morphological defenses also suppressed snail grazing and (2) snail grazing increased the concentration of phlorotannins , Toth et al 2005, which are widely thought to serve as defensive compounds in brown algae (but see Kubanek et al 2004 for an exception). Recent evidence suggests that a southern England A. nodosum population also exhibits inducible defenses that suppress herbivore feeding and alter habitat preference (Borell et al 2004).…”