Markus Molis

The genus Laminaria sensu lato : recent insights and developments

This review about the genus Laminaria sensu lato summarizes the extensive literature that has been published since the overview of the genus given by Kain in 1979. The recent proposal to divide the genus into the two genera Laminaria and Saccharina is acknowledged, but the published data are discussed under a ‘sensu lato’ concept, introduced here. This includes all species which have been considered to be ‘Laminaria’ before the division of the genus. In detail, after an introduction the review covers recent insights into phylogeny and taxonomy, and discusses morphotypes, ecotypes, population genetics and demography. It describes growth and photosynthetic performance of sporophytes with special paragraphs on the regulation of sporogenesis, regulation by endogenous rhythms, nutrient metabolism, storage products, and salinity tolerance. The biology of microstages is discussed separately. The ecology of these kelps is described with a focus on stress defence against abiotic and biotic factors and the role of Laminaria as habitat, its trophic interactions and its competition is discussed. Finally, recent developments in aquaculture are summarized. In conclusion to each section, as a perspective and guide to future research, we draw attention to the remaining gaps in the knowledge about the genus and kelps in general.

Maximum species richness at intermediate frequencies of disturbance : Consistency among levels of productivity

Development of a mechanistic understanding and predictions of patterns of biodiversity is a central theme in ecology. One of the most influential theories, the intermediate disturbance hypothesis (IDH), predicts maximum diversity at intermediate levels of disturbance frequency. The dynamic equilibrium model (DEM), an extension of the IDH, predicts that the level of productivity determines at what frequency of disturbance maximum diversity occurs. To test, and contrast, the predictions of these two models, a field experiment on marine hard-substratum assemblages was conducted with seven levels of disturbance frequency and three levels of nutrient availability. Consistent with the IDH, maximum diversity, measured as species richness, was observed at an intermediate frequency of disturbance. Despite documented effects on productivity, the relationship between disturbance and diversity was not altered by the nutrient treatments. Thus, in this system the DEM did not improve the understanding of patterns of diversity compared to the IDH. Furthermore, it is suggested that careful consideration of measurements and practical definitions of productivity in natural assemblages is necessary for a rigorous test of the DEM.

Re-Structuring of Marine Communities Exposed to Environmental Change: A Global Study on the Interactive Effects of Species and Functional Richness

Species richness is the most commonly used but controversial biodiversity metric in studies on aspects of community stability such as structural composition or productivity. The apparent ambiguity of theoretical and experimental findings may in part be due to experimental shortcomings and/or heterogeneity of scales and methods in earlier studies. This has led to an urgent call for improved and more realistic experiments. In a series of experiments replicated at a global scale we translocated several hundred marine hard bottom communities to new environments simulating a rapid but moderate environmental change. Subsequently, we measured their rate of compositional change (re-structuring) which in the great majority of cases represented a compositional convergence towards local communities. Re-structuring is driven by mortality of community components (original species) and establishment of new species in the changed environmental context. The rate of this re-structuring was then related to various system properties. We show that availability of free substratum relates negatively while taxon richness relates positively to structural persistence (i.e., no or slow re-structuring). Thus, when faced with environmental change, taxon-rich communities retain their original composition longer than taxon-poor communities. The effect of taxon richness, however, interacts with another aspect of diversity, functional richness. Indeed, taxon richness relates positively to persistence in functionally depauperate communities, but not in functionally diverse communities. The interaction between taxonomic and functional diversity with regard to the behaviour of communities exposed to environmental stress may help understand some of the seemingly contrasting findings of past research.

Induction and reduction of Anti-Herbivore defenses in brown and red macroalgae off the Kenyan Coast

Herbivory is particularly intense in tropical benthic communities, suggesting preference of constitutive, rather than inducible, anti‐herbivory defense. The objective of the study was to examine whether anti‐herbivore defenses in the red alga Hypnea pannosa J. Agardh and the brown algae Sargassum asperifolium Hering and G. Martens ex J. Agardh and Cystoseira myrica (S.G. Gmelin) C. Agardh could be induced and subsequently reduced in response to grazing by the amphipod Cymadusa filosa Savigny. During a 14‐day treatment phase, algae were exposed to amphipod grazing or were left ungrazed (control). Subsequently, one subset of algae was used in feeding assays, whereas another was cultivated for additional 14 days without consumers (recovery phase). At the end of each phase, bioassays were conducted to detect defensive traits in terms of differences in consumption rates of grazed and control pieces of live algae and agar‐based food containing nonpolar algal extracts. Consumption of grazed live S. asperifolium and H. pannosa specimens was lower than of control algae. Furthermore, nonpolar extracts of grazed S. asperifolium and C. myrica were less preferred than those from control algae. Defensive responses were exclusively detected after the treatment phase, although strong preference of ungrazed H. pannosa and C. myrica over grazed conspecifics continued throughout the recovery phase. These findings suggest that phenotypic plasticity in anti‐herbivory defense of marine macroalgae 1) might be more common than previously shown, 2) could be switched on and off within 2 weeks, and 3) can be found in nonpolar algal extracts.

Drivers of colonization and succession in polar benthic macro- and microalgal communities

Information on succession in marine benthic primary producers in polar regions is very scarce, particularly with regard to effects of abiotic and biotic drivers of community structure. Primary succession begins with rapid colonizers, such as diatoms and ephemeral macroalgae, whereas slow, highly seasonal recruitment and growth are characteristic of annual or perennial seaweed species. Colonization of intertidal and subtidal assemblages on polar rocky shores is severely affected by physical disturbance and by seasonal changes in abiotic conditions. Biotic factors, such as grazing, can strongly affect colonization patterns and also alter competitive interactions among benthic algae. Ambient UV radiation affects the diversity of macroalgal communities during early and later stages of succession. In contrast, microalgal assemblages have high tolerance to UV stress. Climate warming could alter algal latitudinal distribution and favor invasion of polar regions by cold-temperate species. Reduced sea ice cover and retreating glaciers could expand colonization areas but alter light, salinity, sedimentation and disturbance processes. Although the key role of macroalgae in coastal systems and, to a much reduced extent, the importance of microphytobenthos have been documented for polar regions, information on the successional process is incomplete and will benefit from further ecological studies.

Large-scale variation in combined impacts of canopy loss and disturbance on community structure and ecosystem functioning

Ecosystems are under pressure from multiple human disturbances whose impact may vary depending on environmental context. We experimentally evaluated variation in the separate and combined effects of the loss of a key functional group (canopy algae) and physical disturbance on rocky shore ecosystems at nine locations across Europe. Multivariate community structure was initially affected (during the first three to six months) at six locations but after 18 months, effects were apparent at only three. Loss of canopy caused increases in cover of non-canopy algae in the three locations in southern Europe and decreases in some northern locations. Measures of ecosystem functioning (community respiration, gross primary productivity, net primary productivity) were affected by loss of canopy at five of the six locations for which data were available. Short-term effects on community respiration were widespread, but effects were rare after 18 months. Functional changes corresponded with changes in community structure and/or species richness at most locations and times sampled, but no single aspect of biodiversity was an effective predictor of longer-term functional changes. Most ecosystems studied were able to compensate in functional terms for impacts caused by indiscriminate physical disturbance. The only consistent effect of disturbance was to increase cover of non-canopy species. Loss of canopy algae temporarily reduced community resistance to disturbance at only two locations and at two locations actually increased resistance. Resistance to disturbance-induced changes in gross primary productivity was reduced by loss of canopy algae at four locations. Location-specific variation in the effects of the same stressors argues for flexible frameworks for the management of marine environments. These results also highlight the need to analyse how species loss and other stressors combine and interact in different environmental contexts.

GRAZING IMPACT OF, AND INDIRECT INTERACTIONS BETWEEN MESOGRAZERS ASSOCIATED WITH KELP (LAMINARIA DIGITATA)

Little is known about the indirect effects of nonlethal grazing impacts in mesograzer–seaweed interactions. Using laboratory experiments, the effect of grazing by the seasonally abundant kelp‐associated gastropod Lacuna vincta on subsequent kelp consumption by one kelp‐associated (Idotea granulosa) and one nonassociated species of isopod (I. emarginata) was determined. Measurements of the toughness and elemental composition of different parts of the sporophyte of Laminaria digitata (Huds.) J. V. Lamour., as well as grazer‐induced changes in the palatability of the blade, were conducted to explore possible mechanisms of indirect effects. In situ grazing pressure was the highest between July and September, with the blade being the preferred part of the kelp sporophyte, despite missing differences in the elemental composition among kelp parts. The laboratory experiments supported our hypotheses in that kelp consumption by both species of isopods was lower on intact than on L. vincta–damaged areas of the blade. This pattern was not caused by grazing‐induced changes in blade palatability. Instead, the observed increase in isopod consumption following grazing by L. vincta resulted more likely from the combined effects of a reduction in the toughness of L. vincta–damaged kelp blades and some unknown gastropod cue(s). These results suggest that kelp‐associated and nonassociated mesograzers may benefit from the nonlethal grazing impact of L. vincta due to changes in physical traits of the seaweed. Thus, the nonlethal grazing impact by one species of mesograzer can positively modify the trophic interactions between kelp and other potential competitors, suggesting that the interactions among mesograzers might be more complex than previously assumed.

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

Herbivory is a key factor in regulating plant biomass, thereby driving ecosystem performance. Algae have developed multiple adaptations to cope with grazers, including morphological and chemical defences. In a series of experiments we investigated whether several species of macroalgae possess anti-herbivore defences and whether these could be regulated to demand, i.e. grazing events. The potential of direct grazing on defence induction was assessed for two brown (Dictyopteris membranacea, Fucus vesiculosus) and two red seaweeds (Gelidium sesquipedale, Sphaerococcus coronopifolius) from São Rafael and Ria Formosa, Portugal. Bioassays conducted with live algal pieces and agar-based food containing lipophilic algal extracts were used to detect changes in palatability after exposure to amphipod attacks (=treatment phase). Fucus vesiculosus was the only species significantly reducing palatability in response to direct amphipod-attacks. This pattern was observed in live F. vesiculosus pieces and agar-based food containing a lipophilic extract, suggesting that lipophilic compounds produced during the treatment phase were responsible for the repulsion of grazers. Water-borne cues of grazed F. vesiculosus as well as non-grazing amphipods also reduced palatability of neighbouring conspecifics. However, this effect was only observed in live tissues of F. vesiculosus. This study is the first to show that amphipods, like isopods, are capable to induce anti-herbivory defences in F. vesiculosus and that a seasonally variable effectiveness of chemical defences might serve as a dynamic control in alga–herbivore interactions.

Laboratory experiments examining inducible defense show variable responses of temperate brown and red macroalgae

Macroalgae can defend themselves against generalist and specialist herbivores via morphological and/or chemical traits. Herein we examined the defensive responses (via relative palatability) of two brown (Lessonia nigrescens, Glossophora kunthii) and two red algae (Grateloupia doryphora, Chondracanthus chamissoi) from the northern-central coast of Chile against selected generalist meso-herbivores. Two laboratory experiments were conducted to investigate whether (i) algae can respond generally to grazing pressure of meso-herbivores (amphipods, isopods and juvenile sea urchins) and whether (ii) these algal responses were inducible. In order to examine palatability and thus effectiveness of responses, feeding assays were run after each experiment using fresh algal pieces and artificial agar-based food. Lessonia nigrescens responded to amphipods but not to sea urchins, and G. kunthii showed inducible response against one species of amphipods. Grateloupia doryphora did not respond against any of the tested grazers, whereas C. chamissoi responded against one species of amphipods and the tested isopod. Our results indicate variable responses of macroalgae against selected generalist meso-herbivores and evidence of an inducible defense in the brown alga G. kunthii.

Predator nonconsumptive effects on prey recruitment weaken with recruit density

We investigated the nonconsumptive effects (NCEs) of predatory dogwhelks (Nucella lapillus) on intertidal barnacle (Semibalanus balanoides) recruitment through field experiments on the Gulf of St. Lawrence coast and the Atlantic coast of Nova Scotia, Canada. We studied the recruitment seasons (May-June) of 2011 and 2013. In 2011, the Gulf coast had five times more nearshore phytoplankton (food for barnacle larvae and recruits) during the recruitment season and yielded a 58% higher barnacle recruit density than the Atlantic coast at the end of the recruitment season. In 2013, phytoplankton levels and barnacle recruit density were similar on both coasts and also lower than for the Gulf coast in 2011. Using the comparative-experimental method, the manipulation of dogwhelk presence (without allowing physical contact with prey) revealed that dogwhelk cues limited barnacle recruitment under moderate recruit densities (Atlantic 2011/2013 and Gulf 2013) but had no effect under a high recruit density (Gulf 2011). Barnacle recruits attract settling larvae through chemical cues. Thus, the highest recruit density appears to have neutralized dogwhelk effects. This study suggests that the predation risk perceived by settling larvae may decrease with increasing recruit density and that prey food supply may indirectly influence predator NCEs on prey recruitment.