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.

Origin of British and Irish mammals: disparate post-glacial colonisation and species introductions

Global climate changes during the Quaternary reveal much about broader evolutionary effects of environmental change. Detailed regional studies reveal how evolutionary lineages and novel communities and ecosystems, emerge through glacial bottlenecks or from refugia. There have been significant advances in benthic imaging and dating, particularly with respect to the movements of the British (Scottish) and Irish ice sheets and associated changes in sea level during and after the Last Glacial Maximum (LGM). Ireland has been isolated as an island for approximately twice as long as Britain with no evidence of any substantial, enduring land bridge between these islands after ca 15 kya. Recent biogeographical studies show that Britain's mammal community is akin to those of southern parts of Scandinavia, The Netherlands and Belgium, but the much lower mammal species richness of Ireland is unique and needs explanation. Here, we consider physiographic, archaeological, phylogeographical i.e. molecular genetic, and biological evidence comprising ecological, behavioural and morphological data, to review how mammal species recolonized western Europe after the LGM with emphasis on Britain and, in particular, Ireland. We focus on why these close neighbours had such different mammal fauna in the early Holocene, the stability of ecosystems after LGM subject to climate change and later species introductions.

There is general concordance of archaeological and molecular genetic evidence where data allow some insight into history after the LGM. Phylogeography reveals the process of recolonization, e.g. with respect to source of colonizers and anthropogenic influence, whilst archaeological data reveal timing more precisely through carbon dating and stratigraphy. More representative samples and improved calibration of the ‘molecular clock’ will lead to further insights with regards to the influence of successive glaciations. Species showing greatest morphological, behavioural and ecological divergence in Ireland in comparison to Britain and continental Europe, were also those which arrived in Ireland very early in the Holocene either with or without the assistance of people. Cold tolerant mammal species recolonized quickly after LGM but disappeared, potentially as a result of a short period of rapid warming. Other early arrivals were less cold tolerant and succumbed to the colder conditions during the Younger Dryas or shortly after the start of the Holocene (11.5 kya), or the area of suitable habitat was insufficient to sustain a viable population especially in larger species. Late Pleistocene mammals in Ireland were restricted to those able to colonize up to ca 15 kya, probably originating from adjacent areas of unglaciated Britain and land now below sea level, to the south and west (of Ireland). These few, early colonizers retain genetic diversity which dates from before the LGM. Late Pleistocene Ireland, therefore, had a much depleted complement of mammal species in comparison to Britain.

Mammal species, colonising predominantly from southeast and east Europe occupied west Europe only as far as Britain between ca 15 and 8 kya, were excluded from Ireland by the Irish and Celtic Seas. Smaller species in particular failed to colonise Ireland. Britain being isolated as an island from ca. 8 kya has similar species richness and composition to adjacent lowland areas of northwest continental Europe and its mammals almost all show strongest genetic affinity to populations in neighbouring continental Europe with a few retaining genotypes associated with earlier, western lineages.

The role of people in the deliberate introduction of mammal species and distinct genotypes is much more significant with regards to Ireland than Britain reflecting the larger species richness of the latter and its more enduring land link with continental Europe. The prime motivation of early people in moving mammals was likely to be resource driven but also potentially cultural; as elsewhere, people exploring uninhabited places introduced species for food and the materials they required to survive. It is possible that the process of introduction of mammals to Ireland commenced during the Mesolithic and accelerated with Neolithic people. Irish populations of these long established, introduced species show some unique genetic variation whilst retaining traces of their origins principally from Britain but in some cases, Scandinavia and Iberia. It is of particular interest that they may retain genetic forms now absent from their source populations. Further species introductions, during the Bronze and late Iron Ages, and Viking and Norman invasions, follow the same pattern but lack the time for genetic divergence from their source populations. Accidental introductions of commensal species show considerable genetic diversity based on numerous translocations along the eastern Atlantic coastline. More recent accidental and deliberate introductions are characterised by a lack of genetic diversity other than that explicable by more than one introduction.

The substantial advances in understanding the postglacial origins and genetic diversity of British and Irish mammals, the role of early people in species translocations, and determination of species that are more recently introduced, should inform policy decisions with regards to species and genetic conservation. Conservation should prioritise early, naturally recolonizing species and those brought in by early people reflecting their long association with these islands. These early arrivals in Britain and Ireland and associated islands show genetic diversity that may be of value in mitigating anthropogenic climate change across Europe. In contrast, more recent introductions are likely to disturb ecosystems greatly, lead to loss of diversity and should be controlled. This challenge is more severe in Ireland where the number and proportion of invasive species from the 19th century to the present has been greater than in Britain.

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.

Hull fouling on commercial ships as a vector of macroalgal introduction

Hull fouling is thought to have been the vector of introduction for many algal species. We studied ships arriving at a Mediterranean harbour to clarify the present role of commercial cargo shipping in algal introductions. A total of 31 macroalgal taxa were identified from 22 sampled hulls. The majority of records (58%) were of species with a known cosmopolitan geographical distribution. Due to a prevalence of cosmopolitan species and a high turnover of fouling communities, species composition of assemblages did not appear to be influenced by the area of origin, length of ship or age of coating. In the light of the present results, hull fouling on standard trading commercial vessels does not seem to pose a significant risk for new macroalgal species introductions. However, a high proportion of non-cosmopolitan species found on a ship with non-toxic coating may modify this assessment, especially in the light of the increasing use of such coatings and the potential future changes in shipping routes.

Role of behaviour in biological invasions and species distributions; lessons from interactions between the invasive Gammarus pulex and the native G-duebeni (Crustacea : Amphipoda)

In attempting to understand the distributions of both introduced species and the native species on which they impact, there is a growing trend to integrate studies of behaviour with more traditional life history/ecological approaches. The question of what mechanisms drive the displacement of the freshwater amphipod Gammarus duebeni by the often introduced G pulex is presented as a case study Patterns of displacement are well documented throughout Europe, but the speed and direction of displacement between these species can be varied. From early studies proposing interspecific competition as causal in these patterns, I review research progress to date. I show there has been no evidence for interspecific competition operating, other than the field patterns themselves, a somewhat tautological argument. Rather, the increased recognition of behavioural attributes with respect to the cannibalistic and predatory nature of these species gave rise to a series of studies unravelling the processes driving field patterns. Both species engage in 'intraguild predation' (IGP), with moulting females particularly vulnerable to predation by congeneric males. G pulex is more able both to engage in and avoid this interaction with G duebeni. However, several factors mediate the strength and asymmetry of this IGP, some biotic (e.g. parasitism) and others abiotic (e.g. water chemistry). Further, a number of alternative hypotheses that may account for the displacement (hybridization; parasite transmission) have been tested and rejected. While interspecific competition has been modelled mathematically and found to be a weak interaction relative to IGP, mechanisms of competition between these Gammarus species remain largely untested empirically. Since IGP may be finely balanced in some circumstances, I conclude that the challenge to detect interspecific competition remains and we require assessment of its role, if any, in the interaction between these species. Appreciation of behavioural attributes and their mediation should allow us to more fully understand, and perhaps predict, species introductions and resultant distributions.

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.

Species introduction promotes hybridization and introgression in Coregonus: is there sign of selection against hybrids?

Species introductions are considered one of the major drivers of biodiversity loss via ecological interactions and genetic admixture with local fauna. We examined two well-recognized fish species, native whitefish (Coregonus lavaretus) and introduced vendace (Coregonus albula), as well as their morphological hybrids in a single lake to test for selection against hybrids and backcrosses in the wild. A representative random subsample of 693 individuals (27.8%) was taken from the total catch of coregonids. This subsample was examined with the aim to select c. 50 individuals of pure whitefish (n = 52), pure vendace (n = 55) and putative hybrid (n = 19) for genetic analyses. The subsequent microsatellites and mitochondrial (mt) DNA analyses provided compelling evidence of hybridization and introgression. Of the 126 fish examined, four were found to be F-1, 14 backcrosses to whitefish and seven backcrosses to vendace. The estimates of historical gene flow suggested higher rates from introduced vendace into native whitefish than vice versa, whereas estimates of contemporary gene flow were equal. Mitochondrial introgression was skewed, with 18 backcrosses having vendace mtDNA and only three with whitefish mtDNA. Hybrids and backcrosses had intermediate morphology and niche utilization compared with parental species. No evidence of selection against hybrids or backcrosses was apparent, as both hybrid and backcross growth rates and fecundities were high. Hybrids (F-1) were only detected in 2 year-classes, suggesting temporal variability in mating between vendace and whitefish. However, our data show that hybrids reached sexual maturity and reproduced actively, with backcrosses recorded from six consecutive year-classes, whereas no F-2 individuals were found. The results indicate widespread introgression, as 10.8% of coregonids were estimated to be backcrosses.

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.

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.