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Chemical Inhibition of Barnacle Larval Settlement by the Brown Alga Fucus Vesiculosus

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Chemical Inhibition of Barnacle Larval Settlement by the Brown Alga Fucus Vesiculosus MARINE ECOLOGY PROGRESS SERIES Vol. 337: 165–174, 2007 Published May 14 Mar Ecol Prog Ser Chemical inhibition of barnacle larval settlement by the brown alga Fucus vesiculosus Elisabet Brock*, Göran M. Nylund, Henrik Pavia Department of Marine Ecology, Göteborg University, Tjärnö Marine Biological Laboratory, 45296 Strömstad, Sweden ABSTRACT: The possible importance of larval settlement inhibition by Fucus vesiculosus in explain- ing the low abundance of the barnacle Balanus improvisus on algal fronds compared to adjacent rock was investigated by a combination of field and laboratory studies. A field survey showed that the abundance of adult barnacles was significantly lower on F. vesiculosus than on rocks and settlement preference experiments strongly suggested that settlement avoidance for algal fronds during the natural settlement season was chemically mediated. By using a multi-step approach, whereby both exuded and surface associated metabolites were tested on larval settlement, we further investigated the possible existence of chemical antifouling processes in F. vesiculosus. For exuded metabolites, seawater was conditioned for 1 and 3 h with both submerged and desiccated algae. Surface extracts at natural concentrations and seawater conditioned with submerged algae had no significant effect on larval settlement, although there was a tendency for reduced settlement in the 3 h samples. Sea- water conditioned with desiccated algae consistently inhibited settlement and chemical analyses showed that the mean phlorotannin level in the water was 31.5 µg ml–1, which is ca. 30× higher than concentrations previously shown to inhibit barnacle settlement. Seawater conditioned with sub- merged algae had a mean phlorotannin content of 0.85 µg ml–1 and in samples conditioned for 3 h there was a strong and significant negative relationship between phlorotannin concentration and larval settlement, suggesting that the phlorotannin concentration varied around a level inhibitory to barnacle settlement. Altogether, the results from the laboratory experiments strongly suggested that the low larval preference for algae was caused by exudation of waterborne metabolites, primarily phlorotannins. Finally, field measurements showed that phlorotannins exuded from F. vesiculosus can under natural conditions reach concentrations inhibitory to settlement of barnacle larvae. KEY WORDS: Fucus vesiculosus · Phlorotannins · Chemical defence · Fouling · Barnacles · Balanus improvisus · Exudation · Desiccation Resale or republication not permitted without written consent of the publisher INTRODUCTION and associated supplementary Internet files available at: www.int-res.com/journals/meps/supplementary- The limiting factor for recruitment of sessile marine material/#2002). Fouling organisms can affect the organisms on intertidal rocky shores can often be a growth and survival of algal hosts (see review by de free surface to which they may attach (Wahl 1989, Nys & Steinberg 1999) and should therefore select for Richmond & Seed 1991). As a consequence, epibiosis defence strategies that reduce the recruitment of (i.e. organisms colonising the surface of other organ- foulers on the surface of potential hosts. Such strate- isms in a non-mutualistic way) is a widespread phe- gies include mechanical and physical defences, as nomenon in such environments. In many temperate well as the production of chemical substances that areas, dense stands of large, canopy-forming sea- inhibit settlement of fouling organisms (reviewed by weeds provide a major substratum for recruitment of Davis et al. 1989, Wahl 1989, Pawlik 1992, de Nys & marine epibionts (Jennings & Steinberg 1997, Wik- Steinberg 1999, Steinberg et al. 2001). Many studies ström & Kautsky 2004; see also Wahl & Mark 1999 have demonstrated that seaweeds contain metabolites *Email: [email protected] © Inter-Research 2007 · www.int-res.com 166 Mar Ecol Prog Ser 337: 165–174, 2007 that can inhibit the settlement of fouling organisms ing the low abundance of the barnacle Balanus impro- (see literature cited by de Nys & Steinberg 1999, visus on algal fronds, compared to bare rocks. Bare Nylund & Pavia 2005). However, the vast majority of rock and fucoids are commonly the 2 dominating sub- these studies have been conducted outside of an eco- strata available for the settlement of sessile inverte- logical context, i.e. they have not explicitly aimed to brate larvae on many mid-intertidal shores in the explain the natural distribution patterns of fouling North Atlantic, including the Swedish west coast. The organisms, they have not examined settlement behav- natural distribution of B. improvisus on F. vesiculosus iour on algal surfaces compared to other naturally and adjacent rocks was determined in a field study at 3 available substrata, and they have not determined different sites. To test the hypothesis that the observed ecologically relevant concentrations of the inhibiting low abundance of barnacles on F. vesiculosus com- metabolites (but see Schmitt et al. 1995, Steinberg et pared to rocks could be a result of the settlement al. 2001, Wikström & Pavia 2004, Nylund et al. 2005 behaviour of barnacle larvae, we conducted settlement for exceptions). preference experiments, where barnacle larvae were Several species of the order Fucales are dominating, given a choice between rocks and algal fronds. The canopy-forming macroalgae in the intertidal zone of experiments were carried out on 2 occasions, before sheltered and semi-exposed rocky shores of the North and during the natural recruitment season. The results Atlantic. The bladder wrack Fucus vesiculosus forms from these experiments suggested that the observed a conspicuous belt in the middle of many North settlement preference during the natural settlement Atlantic intertidal shores, and it is the host for a range season was chemically mediated and therefore further of epibiotic sessile taxa, such as hydroids (e.g. Clava experiments were carried out in order to determine multicornis), crustaceans (e.g. Balanus improvisus), potential chemical antifouling processes in F. vesiculo- bryozoans (e.g. Electra pilosa and Membranipora sus. This was done through a multi-step approach, membranacea) and macro algal epiphytes (e.g. where possible occurrence of both surface associated Elachista fucicola and Pilayella littoralis, Ceramium and exuded algal metabolites inhibiting larval settle- sp.) (Hansson 1998, Wikström & Kautsky 2004). Foul- ment was investigated in the laboratory. In order to ing organisms colonizing F. vesiculosus have the mimic the effects of natural variation in water levels on potential to significantly decrease the growth of their the exudation of algal metabolites (Carlson & Carlson host, which should therefore select for increased 1984), the inhibitory activity of exudates was tested for resistance to fouling (Honkanen & Jormalainen 2005). previously emerged, as well as submerged, F. vesiculo- However, little is known about natural defence mech- sus plants. Finally, the levels of phlorotannins were anisms against fouling in F. vesiculosus and other measured in seawater samples from natural stands of fucoids. Many fucoid species contain high levels (3 to F. vesiculosus. 15% DW) of polyphenolic metabolites called phloro- tannins, which are known to exude into the water, with a possible role as fouling deterrents (Conover & MATERIALS AND METHODS Sieburth 1966, Ragan & Glombitza 1986, Lau & Qian 2000; but see also Jennings & Steinberg 1994). In a Study organisms. The study was performed at previous study with laboratory assays, it was shown Tjärnö Marine Biological Laboratory, on the Swedish that phlorotannins extracted from F. vesiculosus west coast (58°52’N, 11°09’E), between 2001 and significantly inhibited settlement of larvae from the 2004. In this area, Fucus vesiculosus, a perennial barnacle Balanus improvisus at concentrations of 0.1 brown alga of the family Fucaceae, is common in the to 1 µg ml–1. Furthermore, it was found that settle- narrow intertidal zone of sheltered and semi-exposed ment of B. improvisus larvae was significantly lower rocky shores. The barnacle Balanus improvisus is also on F. vesiculosus fronds in comparison to a less abun- commonly found in this intertidal zone, attached to dant congeneric alga, as well as to plexiglass control rocks, seaweeds and artificial surfaces (Barnes & panels (Wikström & Pavia 2004). These findings sug- Barnes 1962, Foster 1987, Berntsson & Jonsson 2003, gest that F. vesiculosus can reduce its epibiotic load Wikström & Kautsky 2004). On the Swedish west coast through chemical inhibition of larval settlement. How- it reproduces during the summer and, in their final ever, the suggestion remains speculative as long as it morph called cyprids, the planktonic larvae settle from has not be shown that exuded phlorotannins in the late June to October (Berntsson & Jonsson 2003). It water surrounding F. vesiculosus can reach concen- takes 8 to 24 h for cyprids to metamorphose to fully trations sufficient to inhibit larval recruitment onto the functional juveniles (Glenner & Hoeg 1993). The surface of the alga. cyprids used for experiments in this study were reared We investigated the possible importance of larval in a laboratory culture, as described by Berntsson et al. settlement inhibition by Fucus vesiculosus in explain- (2000). Brock et al.: Chemical inhibition of larval settlement 167 Field abundance of Balanus improvisus. A field Based on the effect of extraction time on cell lysis, survey
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