Fronts, jumps and secondary introductions suggested as different invasion patterns in marine species, with an increase in spread rates over time

Not all introduced (invasive) species in a region will spread from a single point of introduction. Long-distance dispersal or further introductions can obscure the pattern of spread, but the regional importance of such processes is difficult to gauge. These difficulties are further compounded when information on the multiple scale process of invasive species range expansion is reduced to one-dimensional estimates of spread (e. g. km yr(-1)). We therefore compared the results of two different metrics of range expansion: maximum linear rate of spread and accumulation of occupied grid squares (50 x 50 km) over time. An analysis of records for 54 species of introduced marine macrophytes in the Mediterranean and northeast Atlantic revealed cases where the invasion process was probably missed (e. g. Atlantic Bonnemaisonia hamifera) and suggested cases of secondary introductions or erratic jump dispersal (Dasysiphonia sp. and Womersleyella setacea). A majority of species analysed showed evidence for an accumulation of invaded sites without a clear invasion front. Estimates of spread rate are increasing for more recent introductions. The increase is greater than can be accounted for by temporally varying search effort and implies a historical increase in vector efficiency and/or a decreased resistance of native communities to invasion.

The effects of past, present and future climate change on range-wide genetic diversity in northern North Atlantic marine species

It is now accepted that changes in the Earth’s climate are having a profound effect on the distributions of a wide variety of species. One aspect of these changes that has only recently received any attention, however, is their potential effect on levels of within-species genetic diversity. Theoretical, empirical and modelling studies suggest that the impact of trailing-edge population extirpation on range-wide intraspecific diversity will be most pronounced in species that harbour the majority of their genetic variation at low latitudes as a result of changes during the Quaternary glaciations. In the present review, I describe the historical factors that have determined current patterns of genetic variation across the ranges of Northern North Atlantic species, highlight the fact that the majority of these species do indeed harbour a disproportionate level of genetic diversity in rear-edge populations, and outline how combined species distribution modelling and genetic analyses can provide insights into the potential effects of climate change on their overall genetic diversity.

Systematics of the marine microfilamentous green algae Uronema curvatum and Urospora microscopica (Chlorophyta)

The microfilamentous green alga Uronema curvatum is widely distributed along the western and eastern coasts of the north Atlantic Ocean where it typically grows on crustose red algae and on haptera of kelps in subtidal habitats. The placement of this marine species in a genus of freshwater Chlorophyceae had been questioned. Molecular phylogenetic analysis of nuclear-encoded small and large subunit rDNA sequences reveal that U. curvatum is closely related to the ulvophycean order Cladophorales, with which it shares a number of morphological features, including a siphonocladous level of organization and zoidangial development. The divergent phylogenetic position of U. curvatum, sister to the rest of the Cladophorales, along with a combination of distinctive morphological features, such as the absence of pyrenoids, the diminutive size of the unbranched filaments and the discoid holdfast, warrants the recognition of a separate genus, Okellya, within a new family of Cladophorales, Okellyaceae. The epiphytic Urospora microscopica from Norway, which has been allied with U. curvatum, is revealed as a member of the cladophoralean genus Chaetomorpha and is herein transferred to that genus as C. norvegica nom. nov.

Evaluating signatures of glacial refugia for North Atlantic benthic marine taxa

A goal of phylogeography is to relate patterns of genetic differentiation to potential historical geographic isolating events. Quaternary glaciations, particularly the one culminating in the Last Glacial Maximum ~21 ka (thousands of years ago), greatly affected the distributions and population sizes of temperate marine species as their ranges retreated southward to escape ice sheets. Traditional genetic models of glacial refugia and routes of recolonization include these predictions: low genetic diversity in formerly glaciated areas, with a small number of alleles/haplotypes dominating disproportionately large areas, and high diversity including "private" alleles in glacial refugia. In the Northern Hemisphere, low diversity in the north and high diversity in the south are expected. This simple model does not account for the possibility of populations surviving in relatively small northern periglacial refugia. If these periglacial populations experienced extreme bottlenecks, they could have the low genetic diversity expected in recolonized areas with no refugia, but should have more endemic diversity (private alleles) than recently recolonized areas. This review examines evidence of putative glacial refugia for eight benthic marine taxa in the temperate North Atlantic. All data sets were reanalyzed to allow direct comparisons between geographic patterns of genetic diversity and distribution of particular clades and haplotypes including private alleles. We contend that for marine organisms the genetic signatures of northern periglacial and southern refugia can be distinguished from one another. There is evidence for several periglacial refugia in northern latitudes, giving credence to recent climatic reconstructions with less extensive glaciation.

Idiosyncratic species effects confound size-based predictions of responses to climate change

Understanding and predicting the consequences of warming for complex ecosystems and indeed individual species remains a major ecological challenge. Here, we investigated the effect of increased seawater temperatures on the metabolic and consumption rates of five distinct marine species. The experimental species reflected different trophic positions within a typical benthic East Atlantic food web, and included a herbivorous gastropod, a scavenging decapod, a predatory echinoderm, a decapod and a benthic-feeding fish. We examined the metabolism-body mass and consumption-body mass scaling for each species, and assessed changes in their consumption efficiencies. Our results indicate that body mass and temperature effects on metabolism were inconsistent across species and that some species were unable to meet metabolic demand at higher temperatures, thus highlighting the vulnerability of individual species to warming. While body size explains a large proportion of the variation in species' physiological responses to warming, it is clear that idiosyncratic species responses, irrespective of body size, complicate predictions of population and ecosystem level response to future scenarios of climate change. © 2012 The Royal Society.

Between-taxon matching of common and rare species richness patterns

Aim: Our primary aim is to understand how assemblages of rare (restricted range) and common (widespread) species are correlated with each other among different taxa. We tested the proposition that marine species richness patterns of rare and common species differ, both within a taxon in their contribution to the richness pattern of the full assemblage and among taxa in the strength of their correlations with each other. Location The UK intertidal zone. Methods: We used high-resolution marine datasets for UK intertidal macroalgae, molluscs and crustaceans each with more than 400 species. We estimated the relative contribution of rare and common species, treating rarity and commonness as a continuous spectrum, to spatial patterns in richness using spatial crosscorrelations. Correlation strength and significance was estimated both within and between taxa. Results: Common species drove richness patterns within taxa, but rare species contributed more when species were placed on an equal footing via scaling by binomial variance. Between taxa, relatively small sub-assemblages (fewer than 60 species) of common species produced the maximum correlation with each other, regardless of taxon pairing. Cross-correlations between rare species were generally weak, with maximum correlation occurring between small sub-assemblages in only one case. Cross-correlations between common and rare species of different taxa were consistently weak or absent. Main conclusions: Common species in the three marine assemblages were congruent in their richness patterns, but rare species were generally not. The contrast between the stronger correlations among common species and the weak or absent correlations among rare species indicates a decoupling of the processes driving common and rare species richness patterns. The internal structure of richness patterns of these marine taxa is similar to that observed for terrestrial taxa.

rbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi.

In Europe, the last 20 years have seen a spectacular increase in accidental introductions of marine species, but it has recently been suggested that both the actual number of invaders and their impacts have been seriously underestimated because of the prevalence of sibling species in marine habitats. The red alga Polysiphoniaharveyi is regarded as an alien in the British Isles and Atlantic Europe, having appeared in various locations there during the past 170 years. Similar or conspecific populations are known from Atlantic North America and Japan. To choose between three competing hypotheses concerning the origin of P. harveyi in Europe, we employed rbcL sequence analysis in conjunction with karyological and interbreeding data for samples and isolates of P. harveyi and various congeners from the Pacific and North Atlantic Oceans. All cultured isolates of P. harveyi were completely interfertile, and there was no evidence of polyploidy or aneuploidy. Thus, this biological species is both morphologically and genetically variable: intraspecific rbcL divergences of up to 2.1% are high even for red algae. Seven rbcL haplotypes were identified. The four most divergent haplotypes were observed in Japanese samples from Hokkaido and south-central Honshu, which are linked by hypothetical 'missing' haplotypes that may be located in northern Honshu. These data are consistent with Japan being the centre of diversity and origin for P. harveyi. Two non-Japanese lineages were linked to Hokkaido and Honshu, respectively. A single haplotype was found in all North Atlantic and Mediterranean accessions, except for North Carolina, where the haplotype found was the same as that invading in New Zealand and California. The introduction of P. harveyi into New Zealand has gone unnoticed because P. strictissima is a morphologically indistinguishable native sibling species. The sequence divergence between them is 4–5%, greater than between some morphologically distinct red algal species. Two different types of cryptic invasions of P. harveyi have therefore occurred. In addition to its introduction as a cryptic sibling species in New Zealand, P. harveyi has been introduced at least twice into the North Atlantic from presumed different source populations. These two introductions are genetically and probably also physiologically divergent but completely interfertile.

Molecular approaches to the study of invasive seaweeds

A wide range of vectors is currently introducing a plethora of alien marine species into indigenous marine species assemblages. Over the past two decades, molecular studies of non-native seaweeds, including cryptic invaders, have successfully identified the species involved and their sources; we briefly review these studies. As yet, however, little research has been directed towards examining the genetic consequences of seaweed invasions. Here we provide an overview of seaweed invasions from a genetic perspective, focusing on invader species for which the greatest amount of information is available. We review invasion processes, and rationalize evolutionary and genetic consequences for the indigenous and invader species into two main groups: (1) changes in gene-pool composition, in population structure and allele frequencies; and (2) changes in genome organization at the species level through hybridization, and in individual gene expression profiles at the levels of expressed messenger RNA and the proteome (i.e., all proteins synthesized) and thus the phenotype. We draw on studies of better-known aquatic and terrestrial organisms to point the way forward in revealing the genetic consequences of seaweed invasions. We also highlight potential applications of more recent methodological and statistical approaches, such as microarray technology, assignment tests and mixed stock analysis.

Pleistocene glaciation events shape genetic structure across the range of the American lobster, Homarus americanus

A north/south discontinuity along the northeastern coast of North America in the genetic structure of the American lobster (Homarus americanus) was detected using a suite of 13 microsatellite loci assessed using spatial analyses. Population genetic data laid over existing data on physiographic changes and sea-surface temperatures were used to reconstruct the Pleistocene distribution of this species. A postglacial northern-edge colonization model best explains the relative genetic homogeneity of the northern region compared to the southern region centred in the Gulf of Maine. Population genetic analyses identified significant structure (range of standardized theta 0-0.02) but no significant evidence for isolation by distance. The novel application of spatial genetic analyses to a marine species allowed us to interpret these results by providing a greater insight into the evolutionary factors responsible for shaping the genetic structure of this species throughout is natural range.

Resource pressure and environmental change on the North African littoral: Epipalaeolithic to Roman gastropods from Cyrenaica, Libya.

This paper discusses the marine and terrestrial shell on Epipalaeolithic to Classical-period sites in the Cyrenaican coastlands, northeast Libya, with particular reference to the Haua Fteah, with parallel studies at a late-Roman farmstead and two small caves. Together they provide evidence for coastal and terrestrial environments and for the continued nutritional importance of gastropods to humans during the Holocene. Land snail evidence is consistent with regional vegetation in coastal Cyrenaica becoming increasingly open through the Holocene, as a result of some combination of climate change and human impact. Marine species suggest that the coastline near the Haua had been rocky throughout the Holocene. At Hagfet al-Gama, changing faunas provide evidence for sand encroachment onto a previously rocky shoreline in Hellenistic times. A biometric study of Osilinus turbinatus shows that in the archaeological sites these shells are systematically smaller than modern specimens, providing evidence for long-term dietary stress in the human populations around the Haua Fteah, with particularly severe stress in parts of the Epipalaeolithic. A biometric study of Patella spp. provided evidence for size selection, but also seems to show evidence for resource pressure. It is unlikely that variations in resource pressure seen in the mollusc biometrics are the result of climatic stress or natural ecological factors and explanations must be sought in society-environment dynamics.

Ecological and societal benefits of jellyfish blooms

Jellyfish are often considered as stressors on marine ecosystems or as indicators of highly perturbed systems. Far less attention is given to the potential of such species to provide beneficial ecosystem services in their own right. In an attempt to redress this imbalance we take the liberty of portraying jellyfish in a positive light and suggest that the story is not entirely one of doom and gloom. More specifically, we outline how gelatinous marine species contribute to the four categories of ecosystem services (regulating, supporting, provisioning and cultural) defined by the Millennium Ecosystem Assessment. This discussion ranges from the role of jellyfish in carbon capture and advection to the deep ocean through to the creation of micro habitat for developing fishes and the advancement of citizen science programmes. Attention is paid also to incorporation of gelatinous species into fisheries or ecosystem level models and the mechanisms by which we can improve the transfer of information between jellyfish researchers and the wider non-specialist community.

Natural Toxicants: Tetrodotoxin

Tetrodotoxin (tetrodotoxin) is a potent neurotoxin, which shuts down electrical signaling in nerves by blocking the voltage-gated sodium channel proteins in nerve cell membranes. It was originally discovered in puffer fish but is found in a range of animal species and thought to be produced by bacteria. The toxin can be lethal to humans being 10 000 times more potent than cyanide. Human fatalities have been attributed to the ingestion of this toxin through consumption of puffer fish, a delicacy in Japan and other regions, and other marine species. The effects of tetrodotoxin poisoning onset quickly and include shortness of breath, numbness, tingling, light-headedness, paralysis, and irregular heartbeat. Treatment usually consists of respiratory assistance as no antidote has been developed. The accepted method of analysis for tetrodotoxin is the mouse bioassay, although recently more ethical assays have been developed including high performance liquid chromatography, biosensor and enzyme-linked immunosorbant assay.

One size fits all: stability of metabolic scaling under warming and ocean acidification in echinoderms

Responses by marine species to ocean acidification (OA) have recently been shown to be modulated by external factors including temperature, food supply and salinity. However the role of a fundamental biological parameter relevant to all organisms, that of body size, in governing responses to multiple stressors has been almost entirely overlooked. Recent consensus suggests allometric scaling of metabolism with body size differs between species, the commonly cited 'universal' mass scaling exponent (b) of A3/4 representing an average of exponents that naturally vary. One model, the Metabolic-Level Boundaries hypothesis, provides a testable prediction: that b will decrease within species under increasing temperature. However, no previous studies have examined how metabolic scaling may be directly affected by OA. We acclimated a wide body-mass range of three common NE Atlantic echinoderms (the sea star Asterias rubens, the brittlestars Ophiothrix fragilis and Amphiura filiformis) to two levels of pCO(2) and three temperatures, and metabolic rates were determined using closed-chamber respirometry. The results show that contrary to some models these echinoderm species possess a notable degree of stability in metabolic scaling under different abiotic conditions; the mass scaling exponent (b) varied in value between species, but not within species under different conditions. Additionally, we found no effect of OA on metabolic rates in any species. These data suggest responses to abiotic stressors are not modulated by body size in these species, as reflected in the stability of the metabolic scaling relationship. Such equivalence in response across ontogenetic size ranges has important implications for the stability of ecological food webs.

Living to the range limit: consumer isotopic variation increases with environmental stress

Background: Theoretically, each species’ ecological niche is phylogenetically-determined and expressed spatially as the species’ range. However, environmental stress gradients may directly or indirectly decrease individual performance, such that the precise process delimiting a species range may not be revealed simply by studying abundance patterns. In the intertidal habitat the vertical ranges of marine species may be constrained by their abilities to tolerate thermal and desiccation stress, which may act directly or indirectly, the latter by limiting the availability of preferred trophic resources. Therefore, we expected individuals at greater shore heights to show greater variation in diet alongside lower indices of physiological condition.

Methods: We sampled the grazing gastropod Echinolittorina peruviana from the desert coastline of northern Chile at three shore heights, across eighteen regionally-representative shores. Stable isotope values (δ13C and δ15N) were extracted from E. peruviana and its putative food resources to estimate Bayesian ellipse area, carbon and nitrogen ranges and diet. Individual physiological condition was tracked by muscle % C and % N.

Results: There was an increase in isotopic variation at high shore levels, where E. peruviana’s preferred resource, tide-deposited particulate organic matter (POM), appeared to decrease in dietary contribution, and was expected to be less abundant. Both muscle % C and % N of individuals decreased with height on the shore.

Discussion: Individuals at higher stress levels appear to be less discriminating in diet, likely because of abiotic forcing, which decreases both consumer mobility and the availability of a preferred resource. Abiotic stress might be expected to increase trophic variation in other selective dietary generalist species. Where this coincides with a lower physiological condition, this may be a direct factor in setting their range limit.

The comparative effects of habitat complexity on faunal assemblages of northern temperate artificial and natural reefs

Several north temperate marine species were recorded on subtidal hard-substratum reef sites selected to produce a gradient of structural complexity. The study employed an established scuba-based census method, the belt transect. The three types of reef examined, with a measured gradient of increasing structural complexity, were natural rocky reef, artificial reef constructed of solid concrete blocks, and artificial reef made of concrete blocks with voids. Surveys were undertaken monthly over a calendar year using randomly placed fixed rope transects. For a number of conspicuous species of fish and invertebrates, significant differences were found between the levels of habitat complexity and abundance. Overall abundance for many of the species examined was 2-3 times higher on the complex artificial habitats than on simple artificial or natural reef habitats. The enhanced habitat availability produced by the increased structural complexity delivered through specifically designed artificial reefs may have the potential to augment faunal abundance while promoting species diversity.