Non-consumptive predator effects indirectly influence marine plant biomass and palatability

1. Predators can reduce herbivory and increase plant biomass by consuming herbivores, lowering individual herbivore feeding rates, or both. We tested whether the presence of predators increases plant quality by non-consumptively reducing grazing pressure and thereby weakening the strength of the induced response in plant chemical defences. 2. We performed a 42-day outdoor mesocosm experiment in which the herbivorous amphipod Ampithoe longimana was cultured on the brown seaweed Sargassum filipendula in the presence and absence of olfactory cues of its principal fish predator, the pinfish Lagodon rhomboides. The presence of fish cues reduced per capita rates of amphipod grazing by nearly 50%. Over the span of the mesocosm experiment, this per capita reduction in feeding rate yielded at least a 40% lower growth rate of amphipod populations (i.e. r reduced from 1.01 to 0.61). The lower rates of amphipod grazing (overall or per capita) correlated with higher algal biomass. 3. We pursued a series of laboratory-based feeding choice assays with naive amphipods to determine tissue palatability and the plant traits that mediate feeding choices. Tissue from tanks without grazers was more palatable than tissue from tanks with grazers, a pattern of induced plant defences that has been documented previously. Surprisingly, however, plant tissue from tanks with grazers and fish cues was more palatable than tissue from tanks with grazers but without fish cues. All changes in algal palatability were mediated by polar, but not lipophilic metabolites. These results suggest that the non-consumptive effects of fish predators increases the food quality of Sargassum by weakening the strength of its induced chemical defences. 4. Synthesis. The smell of predators has the potential to regulate herbivore populations and affect the ecological dynamics of plant biomass and chemical defences

Mitochondrial and nuclear markers reveal a lack of genetic structure in the entocommensal nemertean Malacobdella arrokeana in the Patagonian gulfs

Abstract Malacobdella arrokeana is an entocommensal nemertean exclusively found in the bivalve geoduck Panopea abbreviata, and it is the only representative of the genus in the southern hemisphere. To characterize its genetic diversity, population structure and recent demographic history, we conducted the first genetic survey on this species, using sequence data for the cytochrome oxidase I gene (COI), 16S rRNA (16S) and the internal transcribed spacer (ITS2). Only four different ITS2 genotypes were found in the whole sample, and the two main haplotypes identified in the mitochondrial dataset were present among all localities with a diversity ranging from 0.583 to 0.939. Nucleotide diversity was low (p = 0.001?0.002). No significant genetic structure was detected between populations, and mismatch distribution patterns and neutrality tests results are consistent with a population in expansion or under selection. Analysis of molecular variance (AMOVA) revealed that the largest level of variance observed was due to intrapopulation variation (100, 100 and 94.39 % for 16S, COI and ITS2, respectively). Fst values were also non-significant. The observed lack of population structure is likely due to high levels of genetic connectivity in combination with the lack or permeability of biogeographic barriers and episodes of habitat modification.Fil: Fernandez Alfaya, Jose Elias. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Bigatti, Gregorio. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Nacional Patagónico; ArgentinaFil: Machordom, Annie. Consejo Superior de Investigaciones Cientificas. Museo Nacional de Cs. Naturales; Españ

Biochemical warfare on the reef : the role of glutathione transferases in consumer tolerance of dietary prostaglandins

© 2010 The Authors. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in PLoS ONE 5 (2010): e8537, doi:10.1371/journal.pone.0008537.Despite the profound variation among marine consumers in tolerance for allelochemically-rich foods, few studies have examined the biochemical adaptations underlying diet choice. Here we examine the role of glutathione S-transferases (GSTs) in the detoxification of dietary allelochemicals in the digestive gland of the predatory gastropod Cyphoma gibbosum, a generalist consumer of gorgonian corals. Controlled laboratory feeding experiments were used to investigate the influence of gorgonian diet on Cyphoma GST activity and isoform expression. Gorgonian extracts and semi-purified fractions were also screened to identify inhibitors and possible substrates of Cyphoma GSTs. In addition, we investigated the inhibitory properties of prostaglandins (PGs) structurally similar to antipredatory PGs found in high concentrations in the Caribbean gorgonian Plexaura homomalla. Cyphoma GST subunit composition was invariant and activity was constitutively high regardless of gorgonian diet. Bioassay-guided fractionation of gorgonian extracts revealed that moderately hydrophobic fractions from all eight gorgonian species examined contained putative GST substrates/inhibitors. LC-MS and NMR spectral analysis of the most inhibitory fraction from P. homomalla subsequently identified prostaglandin A2 (PGA2) as the dominant component. A similar screening of commercially available prostaglandins in series A, E, and F revealed that those prostaglandins most abundant in gorgonian tissues (e.g., PGA2) were also the most potent inhibitors. In vivo estimates of PGA2 concentration in digestive gland tissues calculated from snail grazing rates revealed that Cyphoma GSTs would be saturated with respect to PGA2 and operating at or near physiological capacity. The high, constitutive activity of Cyphoma GSTs is likely necessitated by the ubiquitous presence of GST substrates and/or inhibitors in this consumer's gorgonian diet. This generalist's GSTs may operate as ‘all-purpose’ detoxification enzymes, capable of conjugating or sequestering a broad range of lipophilic gorgonian compounds, thereby allowing this predator to exploit a range of chemically-defended prey, resulting in a competitive dietary advantage for this species.Financial support for this work was provided by the Ocean Life Institute Tropical Research Initiative Grant (WHOI) to KEW and MEH; the Robert H. Cole Endowed Ocean Ventures Fund (WHOI) to KEW; the National Undersea Research Center - Program Development Proposal (CMRC-03PRMN0103A) to KEW; Walter A. and Hope Noyes Smith, and a National Science Foundation Graduate Research Fellowship to KEW

Genetic Structure Among 50 Species of the Northeastern Pacific Rocky Intertidal Community

Comparing many species' population genetic patterns across the same seascape can identify species with different levels of structure, and suggest hypotheses about the processes that cause such variation for species in the same ecosystem. This comparative approach helps focus on geographic barriers and selective or demographic processes that define genetic connectivity on an ecosystem scale, the understanding of which is particularly important for large-scale management efforts. Moreover, a multispecies dataset has great statistical advantages over single-species studies, lending explanatory power in an effort to uncover the mechanisms driving population structure. Here, we analyze a 50-species dataset of Pacific nearshore invertebrates with the aim of discovering the most influential structuring factors along the Pacific coast of North America. We collected cytochrome c oxidase I (COI) mtDNA data from populations of 34 species of marine invertebrates sampled coarsely at four coastal locations in California, Oregon, and Alaska, and added published data from 16 additional species. All nine species with non-pelagic development have strong genetic structure. For the 41 species with pelagic development, 13 show significant genetic differentiation, nine of which show striking FST levels of 0.1–0.6. Finer scale geographic investigations show unexpected regional patterns of genetic change near Cape Mendocino in northern California for five of the six species tested. The region between Oregon and Alaska is a second focus of intraspecific genetic change, showing differentiation in half the species tested. Across regions, strong genetic subdivision occurs more often than expected in mid-to-high intertidal species, a result that may reflect reduced gene flow due to natural selection along coastal environmental gradients. Finally, the results highlight the importance of making primary research accessible to policymakers, as unexpected barriers to marine dispersal break the coast into separate demographic zones that may require their own management plans

Water-Borne Cues of a Non-Indigenous Seaweed Mediate Grazer-Deterrent Responses in Native Seaweeds, but Not Vice Versa

Plants optimise their resistance to herbivores by regulating deterrent responses on demand. Induction of anti-herbivory defences can occur directly in grazed plants or from emission of risk cues to the environment, which modifies interactions of adjacent plants with, for instance, their consumers. This study confirmed the induction of anti-herbivory responses by water-borne risk cues between adjoining con-specific seaweeds and firstly examined whether plant-plant signalling also exists among adjacent hetero-specific seaweeds. Furthermore, differential abilities and geographic variation in plant-plant signalling by a non-indigenous seaweed as well as native seaweeds were assessed. Twelve-day induction experiments using the non-indigenous seaweed Sargassum muticum were conducted in the laboratory in Portugal and Germany with one local con-familiar (Portugal: Cystoseira humilis, Germany: Halidrys siliquosa) and hetero-familiar native species (Portugal: Fucus spiralis, Germany: F. vesiculosus). All seaweeds were grazed by a local isopod species (Portugal: Stenosoma nadejda, Germany: Idotea baltica) and were positioned upstream of con- and hetero-specific seaweeds. Grazing-induced modification in seaweed traits were tested in three-day feeding assays between cue-exposed and cue-free ( = control) pieces of both fresh and reconstituted seaweeds. Both Fucus species reduced their palatability when positioned downstream of isopod-grazed con-specifics. Yet, the palatability of non-indigenous S. muticum remained constant in the presence of upstream grazed con-specifics and native hetero-specifics. In contrast, both con-familiar (but neither hetero-familiar) native species reduced palatability when located downstream of grazed S. muticum. Similar patterns of grazer-deterrent responses to water-borne cues were observed on both European shores, and were almost identical between assays using fresh and reconstituted seaweeds. Hence, seaweeds may use plant-plant signalling to optimise chemical resistance to consumers, though this ability appeared to be species-specific. Furthermore, this study suggests that native species may benefit more than a non-indigenous species from water-borne cue mediated reduction in consumption as only natives responded to signals emitted by hetero-specifics

Anti‑predatory chemical defences in Antarctic benthic fauna

Antarctic benthic communities are largely structured by predation, which leads to the development of mechanisms of repellence. Among those mechanisms, chemical defences are quite extensive, yet poorly understood. To increase knowledge about the role of chemical defences in the Southern Ocean ecosystems, we assessed the incidence of feeding repellents in sessile and vagile invertebrates from nine phyla: Porifera, Cnidaria, Nemertea, Annelida, Mollusca, Bryozoa, Echinodermata, Hemichordata, and Tunicata (Ascidiacea). Samples were collected at depths of 120–789 m in the eastern Weddell Sea and Bouvet Island, and at depths ranging 0–100 m in the South Shetland Islands. When possible, specimens were dissected to study anatomical allocation of repellents. The common, eurybathic sea star Odontaster validus was chosen to perform feeding repellence bioassays, using diethyl ether (lipophilic) and butanol (hydrophilic) extracts from these samples. Among the 75 species tested, 52 % were studied for the first time for anti-predatory properties. Results provide further evidence of the prevalence of defensive metabolites in Antarctic organisms, with 47 % of the species exhibiting significant repellence within their lipophilic extracts. They also suggest a wider use of nonpolar defensive chemicals. Sessile taxa displayed highest repellence activities, with ascidians, cnidarians, and sponges being the most chemically protected. Overall, the present study indicates that natural products by mediating trophic interactions between prey and their potential predators play an important role in structuring Antarctic benthic ecosystems.Versión del editor2,011

Model-Derived Dispersal Pathways from Multiple Source Populations Explain Variability of Invertebrate Larval Supply

Background: Predicting the spatial and temporal patterns of marine larval dispersal and supply is a challenging task due to the small size of the larvae and the variability of oceanographic processes. Addressing this problem requires the use of novel approaches capable of capturing the inherent variability in the mechanisms involved. Methodology/Principal Findings: In this study we test whether dispersal and connectivity patterns generated from a biophysical model of larval dispersal of the crab Carcinus maenas, along the west coast of the Iberian Peninsula, can predict the highly variable daily pattern of wind-driven larval supply to an estuary observed during the peak reproductive season (March–June) in 2006 and 2007. Cross-correlations between observed and predicted supply were significant (p,0.05) and strong, ranging from 0.34 to 0.81 at time lags of 26 to+5 d. Importantly, the model correctly predicted observed cross-shelf distributions (Pearson r = 0.82, p,0.001, and r = 0.79, p,0.01, in 2006 and 2007) and indicated that all supply events were comprised of larvae that had been retained within the inner shelf; larvae transported to the outer shelf and beyond never recruited. Estimated average dispersal distances ranged from 57 to 198 km and were only marginally affected by mortality. Conclusions/Significance: The high degree of predicted demographic connectivity over relatively large geographic scales is consistent with the lack of genetic structuring in C. maenas along the Iberian Peninsula. These findings indicate that the dynamic nature of larval dispersal can be captured by mechanistic biophysical models, which can be used to provid

Genetic Population Structure in the Antarctic Benthos: Insights from the Widespread Amphipod, Orchomenella franklini

Currently there is very limited understanding of genetic population structure in the Antarctic benthos. We conducted one of the first studies of microsatellite variation in an Antarctic benthic invertebrate, using the ubiquitous amphipod Orchomenella franklini (Walker, 1903). Seven microsatellite loci were used to assess genetic structure on three spatial scales: sites (100 s of metres), locations (1–10 kilometres) and regions (1000 s of kilometres) sampled in East Antarctica at Casey and Davis stations. Considerable genetic diversity was revealed, which varied between the two regions and also between polluted and unpolluted sites. Genetic differentiation among all populations was highly significant (FST = 0.086, RST = 0.139, p<0.001) consistent with the brooding mode of development in O. franklini. Hierarchical AMOVA revealed that the majority of the genetic subdivision occurred across the largest geographical scale, with Nem≈1 suggesting insufficient gene flow to prevent independent evolution of the two regions, i.e., Casey and Davis are effectively isolated. Isolation by distance was detected at smaller scales and indicates that gene flow in O. franklini occurs primarily through stepping-stone dispersal. Three of the microsatellite loci showed signs of selection, providing evidence that localised adaptation may occur within the Antarctic benthos. These results provide insights into processes of speciation in Antarctic brooders, and will help inform the design of spatial management initiatives recently endorsed for the Antarctic benthos

Effects of Trophic Skewing of Species Richness on Ecosystem Functioning in a Diverse Marine Community

Widespread overharvesting of top consumers of the world’s ecosystems has “skewed” food webs, in terms of biomass and species richness, towards a generally greater domination at lower trophic levels. This skewing is exacerbated in locations where exotic species are predominantly low-trophic level consumers such as benthic macrophytes, detritivores, and filter feeders. However, in some systems where numerous exotic predators have been added, sometimes purposefully as in many freshwater systems, food webs are skewed in the opposite direction toward consumer dominance. Little is known about how such modifications to food web topology, e.g., changes in the ratio of predator to prey species richness, affect ecosystem functioning. We experimentally measured the effects of trophic skew on production in an estuarine food web by manipulating ratios of species richness across three trophic levels in experimental mesocosms. After 24 days, increasing macroalgal richness promoted both plant biomass and grazer abundance, although the positive effect on plant biomass disappeared in the presence of grazers. The strongest trophic cascade on the experimentally stocked macroalgae emerged in communities with a greater ratio of prey to predator richness (bottom-rich food webs), while stronger cascades on the accumulation of naturally colonizing algae (primarily microalgae with some early successional macroalgae that recruited and grew in the mesocosms) generally emerged in communities with greater predator to prey richness (the more top-rich food webs). These results suggest that trophic skewing of species richness and overall changes in food web topology can influence marine community structure and food web dynamics in complex ways, emphasizing the need for multitrophic approaches to understand the consequences of marine extinctions and invasions