Effects of coastal topography on physiology, behaviour and genetics of indigenous (Perna perna) and invasive (Mytilus galloprovincialis) mussels

Organisms inhabit environments that have many dimensions, each of which can vary temporally and spatially. The spatial-temporal variations of environmental stressors and disturbances may have major but different effects on indigenous and invasive species, favouring either of them at different times and places. The invasive mussel Mytilus galloprovincialis invaded the South African coast 30 years ago and, on the south coast of South Africa, it now competes and co-exists with the indigenous Perna perna in the lower eulittoral zone (referred to here as the mussel zone) The invasive and indigenous species dominate the upper and the lower mussel zones respectively, while the two co-exist in the mid-zone. My results show that intertidal mussels experience, and respond to, spatial and temporal fluctuations of several biotic and abiotic stressors. The invasive and the indigenous species adopt different strategies when reacting to environmental factors and their physiological and behavioural responses vary in time and in different habitats as different pressures become of overriding importance. Attachment strength of both species decreased in summer and increased in winter, and was higher on the open coast than in bays for both species, showing a strong positive correlation with wave force in time and space. P. perna had significantly higher attachment strength than M. galloprovincialis but, contrary to previous studies, the difference in gonad index between the two species varied according to the habitat. In bay habitats, M. galloprovincialis had a higher maximum reproductive effort than P. perna, however, on the open coast, there was no significant difference between the two species, suggesting that for the invasive species wave action is a limiting factor not only in terms of the attachment strength but also of energy availability for reproductive tissue development. Major spawning events occurred during periods of low wave action while minor spawning coincided with periods of intense hydrodynamic stress. On the open coast, gonad index was negatively correlated with attachment strength for both species while, in bays, there was no correlation between these two factors for either. The two species also showed different behaviour. In the field, M. galloprovincialis moved significantly more than P. perna over a period of six months. The higher mobility of the invasive species was also confirmed in the laboratory where, in general, M. galloprovincialis formed clumps more readily than P. perna. Taken collectively, these results suggest that channelling more energy into attachment strength limits reproductive tissue development and that, while the indigenous species invests more in byssal production, the invasive species adopts a more dynamic strategy looking for aggregation or a safer arrangement. Higher endolithic infestation and a greater expression of heat shock proteins (Hsps) in mussel populations on the open coast than in bays indicate that this habitat is a more stressful environment not only in terms of wave action. Endolith damaged mussels had significantly lower attachment strengths and condition indices than clean mussels, probably due to the need to channel energy into shell repair. The constant shell repair and expression of Hsps typical of open coast populations are energetically demanding processes. These observations suggest that on the open coast, mussels are subjected to more severe energetic constraints than in bay habitats. Wave and sand stress fluctuated seasonally with the former having a greater effect on mussel mortality on the open coast and the latter a higher impact on bay populations. Overall, mussel mortality rates were higher on the open coast than in bays. My results show that populations on the open coast had fewer private haplotypes and less genetic endemism than those inside bays. Gene flow analysis showed the relatively stable bay habitats act as source populations with greater genetic migration rates out of bays than into them. These differences in genetic structure on scales of las of kilometers show that coastal configuration strongly affects selection, larval dispersal and haplotype diversity. Environmental gradients that are key factors in species distribution over large geographical scales can also be responsible for micro-scale distributions. My results show that M. galloprovincialis colonizes the upper mussel zone where temperature is high, but is less tolerant to this stressor and has to maintain a high expression of Hsps. This suggests that temperature is probably a limiting factor in its invasion towards the sub-tropical east coast. There are inter- and intra-specific differences in responses to the environment which highlight the efforts of M. galloprovincialis and P. perna to optimize resource utilization for survival and reproduction. Determining these differences is crucial to understanding patterns of co-existence between competing indigenous and invasive species

Behind the mask: cryptic genetic diversity of Mytilus galloprovincialis along southern European and northern African shores

Morphological uniformity in geographically widespread species may cause genetically distinct entities to pass unnoticed if they can only be detected by molecular approaches. The importance of uncovering such cryptic diversity is prompted by the need to understand the putative adaptive potential of populations along species ranges and to manage biodiversity conservation efforts. In this study, we aim to assess cryptic intraspecific genetic diversity and taxonomic status of the widely distributed intertidal mussel Mytilus galloprovincialis, along Atlantic southwestern (SW) Iberian, Atlantic northwestern (NW) Moroccan and Mediterranean Tunisian shores. By using mitochondrial (16S restriction-fragment length polymorphism) and nuclear (polyphenolic adhesive protein gene, Glu-5') markers, we discovered a more complex taxonomic diversity of M. galloprovincialis than previously known. Both Atlantic and Mediterranean haplogroups of M. galloprovincialis were detected along Atlantic SW Iberian shores along with M. galloprovincialis/edulis hybrids (92.2% Atlantic, 3.9% Mediterranean and 3.9% hybrids). In contrast, NW Moroccan populations consisted solely of Atlantic M. galloprovincialis. The Mediterranean populations did not include M. galloprovincialis/ edulis hybrids, but both Atlantic (58%) and Mediterranean (42%) lineages were detected. Divergent selection between coastlines and/or indirect larval dispersal by human activities may be the drivers of this geographically structured genetic diversity.Fundacao para a Ciencia e Tecnologia (FCT), Portugal; FCT [PTDC/BIA-BEC/103916/2008]; Bilateral Project (Acordo Portugal - Tunisia)info:eu-repo/semantics/publishedVersio

Shift happens: trailing edge contraction associated with recent warming trends threatens a distinct genetic lineage in the marine macroalga Fucus vesiculosus

Significant effects of recent global climate change have already been observed in a variety of ecosystems, with evidence for shifts in species ranges, but rarely have such consequences been related to the changes in the species genetic pool. The stretch of Atlantic coast between North Africa and North Iberia is ideal for studying the relationship between species distribution and climate change as it includes the distributional limits of a considerable number of both cold- and warm-water species. We compared temporal changes in distribution of the canopy-forming alga Fucus vesiculosus with historical sea surface temperature (SST) patterns to draw links between range shifts and contemporary climate change. Moreover, we genetically characterized with microsatellite markers previously sampled extinct and extant populations in order to estimate resulting cryptic genetic erosion. Results Over the past 30 years, a geographic contraction of the southern range edge of this species has occurred, with a northward latitudinal shift of approximately 1,250 km. Additionally, a more restricted distributional decline was recorded in the Bay of Biscay. Coastal SST warming data over the last three decades revealed a significant increase in temperature along most of the studied coastline, averaging 0.214°C/decade. Importantly, the analysis of existing and extinct population samples clearly distinguished two genetically different groups, a northern and a southern clade. Because of the range contraction, the southern group is currently represented by very few extant populations. This southern edge range shift is thus causing the loss of a distinct component of the species genetic background. Conclusions We reveal a climate-correlated diversity loss below the species level, a process that could render the species more vulnerable to future environmental changes and affect its evolutionary potential. This is a remarkable case of genetic uniqueness of a vanishing cryptic genetic clade (southern clade).Peer Reviewe

The role of gaping behaviour in habitat partitioning between coexisting intertidal mussels

Background Environmental heterogeneity plays a major role in invasion and coexistence dynamics. Habitat segregation between introduced species and their native competitors is usually described in terms of different physiological and behavioural abilities. However little attention has been paid to the effects of behaviour in habitat partitioning among invertebrates, partially because their behavioural repertoires, especially marine benthic taxa, are extremely limited. This study investigates the effect of gaping behaviour on habitat segregation of the two dominant mussel species living in South Africa, the invasive Mytilus galloprovincialis and the indigenous Perna perna. These two species show partial habitat segregation on the south coast of South Africa, the lower and upper areas of the mussel zone are dominated by P. perna and M. galloprovincialis respectively, with overlap in the middle zone. During emergence, intertidal mussels will either keep the valves closed, minimizing water loss and undergoing anaerobic metabolism, or will periodically open the valves maintaining a more efficient aerobic metabolism but increasing the risk of desiccation. Results Our results show that, when air exposed, the two species adopt clearly different behaviours. M. galloprovincialis keeps the shell valves closed, while P. perna periodically gapes. Gaping behaviour increased water loss in the indigenous species, and consequently the risk of desiccation. The indigenous species expressed significantly higher levels of stress protein (Hsp70) than M. galloprovincialis under field conditions and suffered significantly higher mortality rates when exposed to air in the laboratory. In general, no intra-specific differences were observed in relation to intertidal height. The absence of gaping minimises water loss but exposes the invasive species to other stresses, probably related to anoxic respiration. Conclusions Gaping affects tolerance to desiccation, thus influencing the vertical zonation of the two species. Valve closure exposes the invasive species to higher stress and associated energy demands, but it minimizes water loss, allowing this species to dominate the upper mussel zone, where the gaping indigenous P. perna cannot survive. Thus even very simple behaviour can influence the outcome of interactions between indigenous and invasive species

Love thy neighbour: group properties of gaping behaviour in mussel aggregations

By associating closely with others to form a group, an animal can benefit from a number of advantages including reduced risk of predation, amelioration of environmental conditions, and increased reproductive success, but at the price of reduced resources. Although made up of individual members, an aggregation often displays novel effects that do not manifest at the level of the individual organism. Here we show that very simple behaviour in intertidal mussels shows new effects in dense aggregations but not in isolated individuals. Perna perna and Mytilus galloprovincialis are gaping (periodic valve movement during emersion) and non-gaping mussels respectively. P. perna gaping behaviour had no effect on body temperatures of isolated individuals, while it led to increased humidity and decreased temperatures in dense groups (beds). Gaping resulted in cooler body temperatures for P. perna than M. galloprovincialis when in aggregations, while solitary individuals exhibited the highest temperatures. Gradients of increasing body temperature were detected from the center to edges of beds, but M. galloprovincialis at the edge had the same temperature as isolated individuals. Furthermore, a field study showed that during periods of severe heat stress, mortality rates of mussels within beds of the gaping P. perna were lower than those of isolated individuals or within beds of M. galloprovincialis, highlighting the determinant role of gaping on fitness and group functioning. We demonstrate that new effects of very simple individual behaviour lead to amelioration of abiotic conditions at the aggregation level and that these effects increase mussel resistance to thermal stress

Intraspecific genetic lineages of a marine mussel show behavioural divergence and spatial segregation over a tropical/subtropical biogeographic transition

Background: Intraspecific variability is seen as a central component of biodiversity. We investigated genetic differentiation, contemporary patterns of demographic connectivity and intraspecific variation of adaptive behavioural traits in two lineages of an intertidal mussel (Perna perna) across a tropical/subtropical biogeographic transition. Results: Microsatellite analyses revealed clear genetic differentiation between western (temperate) and eastern (subtropical/tropical) populations, confirming divergence previously detected with mitochondrial (COI) and nuclear (ITS) markers. Gene flow between regions was predominantly east-to-west and was only moderate, with higher heterozygote deficiency where the two lineages co-occur. This can be explained by differential selection and/or oceanographic dynamics acting as a barrier to larval dispersal. Common garden experiments showed that gaping (periodic closure and opening of the shell) and attachment to the substratum differed significantly between the two lineages. Western individuals gaped more and attached less strongly to the substratum than eastern ones. Conclusions: These behavioural differences are consistent with the geographic and intertidal distributions of each lineage along sharp environmental clines, indicating their strong adaptive significance. We highlight the functional role of diversity below the species level in evolutionary trends and the need to understand this when predicting biodiversity responses to environmental change.Fundação para a Ciência e a Tecnologi

First record of the brown mussel (Perna perna) from the European Atlantic coast

The occurrence of the brown mussel Perna perna is reported for the first time from the European Atlantic coast, on the southern Portuguese coast. Several specimens of this mytilidae species were identified in exposed rocky intertidal habitats in Vilamoura (37804019.7000N 8807019.7100W) and Ilha do Farol (36858029.3800N 7851042.5100W). It is suggested that, under warming climate conditions, this subtropical/tropical species might have extended its geographical distribution from North Africa

Cheating the locals: invasive mussels steal and benefit from the cooling effect of indigenous mussels

The indigenous South African mussel Perna perna gapes during periods of aerial exposure to maintain aerobic respiration. This behaviour has no effect on the body temperatures of isolated individuals, but when surrounded by conspecifics, beneficial cooling effects of gaping emerge. It is uncertain, however, whether the presence of the invasive mussel Mytilus galloprovincialis limits the ability of P. perna for collective thermoregulation. We investigated whether varying densities of P. perna and M. galloprovincialis influences the thermal properties of both natural and artificial mussel beds during periods of emersion. Using infrared thermography, body temperatures of P. perna within mixed artificial beds were shown to increase faster and reach higher temperatures than individuals in conspecific beds, indicating that the presence of M. galloprovincialis limits the group cooling effects of gaping. In contrast, body temperatures of M. galloprovincialis within mixed artificial mussel beds increased slower and exhibited lower temperatures than for individuals in beds comprised entirely of M. galloprovincialis. Interestingly, differences in bed temperatures and heating rates were largely dependent on the size of mussels, with beds comprised of larger individuals experiencing less thermal stress irrespective of species composition. The small-scale patterns of thermal stress detected within manipulated beds were not observed within naturally occurring mixed mussel beds. We propose that small-scale differences in topography, size-structure, mussel bed size and the presence of organisms encrusting the mussel shells mask the effects of gaping behaviour within natural mussel beds. Nevertheless, the results from our manipulative experiment indicate that the invasive species M. galloprovincialis steals thermal properties as well as resources from the indigenous mussel P. perna. This may have significant implications for predicting how the co-existence of these two species may change as global temperatures continue to rise

Characterization of ten highly polymorphic microsatellite loci for the intertidal mussel Perna perna, and cross species amplification within the genus

The brown mussel Perna perna (Linnaeus, 1758) is a dominant constituent of intertidal communities and a strong invader with multiple non-native populations distributed around the world. In a previous study, two polymorphic microsatellite loci were developed and used to determine population-level genetic diversity in invasive and native P. perna populations. However, higher number of microsatellite markers are required for reliable population genetic studies. In this context, in order to understand P. perna origins and history of invasion and to compare population genetic structure in native versus invaded areas, we developed 10 polymorphic microsatellite markers. Findings Described microsatellite markers were developed from an enriched genomic library. Analyses and characterization of loci using 20 individuals from a population in Western Sahara revealed on average 11 alleles per locus (range: 5–27) and mean gene diversity of 0.75 (range: 0.31 - 0.95). One primer pair revealed possible linkage disequilibrium while heterozygote deficiency was significant at four loci. Six of these markers cross-amplified in P. canaliculus (origin: New Zealand). Conclusions Developed markers will be useful in addressing a variety of questions concerning P. perna, including dispersal scales, genetic variation and population structure, in both native and invaded areas.Peer Reviewe