Photoautotrophic Euendoliths and their complex ecological effects in marine bioengineered ecosystems

Photoautotrophic euendolithic microorganisms are ubiquitous where there are calcium carbonate substrates to bore into and sufficient light to sustain photosynthesis. The most diverse and abundant modern euendolithic communities can be found in the marine environment. Euendoliths, as microorganisms infesting inanimate substrates, were first thought to be ecologically irrelevant. Over the past three decades, numerous studies have subsequently shown that euendoliths can colonize living marine calcifying organisms, such as coral skeletons and bivalve shells, causing both sub-lethal and lethal damage. Moreover, under suitable environmental conditions, their presence can have surprising benefits for the host. Thus, infestation by photoautotrophic euendoliths has significant consequences for calcifying organisms that are of particular importance in the case of ecosystems underpinned by calcifying ecosystem engineers. In this review, we address the nature and diversity of marine euendoliths, as revealed recently through genetic techniques, their bioerosive mechanisms, how environmental conditions influence their incidence in marine ecosystems and their potential as bioindicators, how they affect live calcifiers, and the potential future of euendolithic infestation in the context of global climate change and ocean acidificationinfo:eu-repo/semantics/publishedVersio

Euendolithic infestation of Mussel Shells indirectly improves the thermal buffering offered by Mussel Beds to associated Molluscs, but one size does not fit all

Mussel beds form important intertidal matrices that provide thermal buffering to associated invertebrate communities, especially under stressful environmental conditions. Mussel shells are often colonized by photoautotrophic euendoliths, which have indirect conditional beneficial thermoregulatory effects on both solitary and aggregated mussels by increasing the albedo of the shell. We investigated whether euendolithic infestation of artificial mussel beds (Perna perna) influences the body temperatures of four associated mollusc species during simulated periods of emersion, using shell temperature obtained via non-invasive infrared thermography as a proxy. Shell temperatures of the limpet Scutellastra granularis and the chiton Acanthochitona garnoti were higher in non-infested than infested mussel beds during simulated low tides under high solar irradiance and low wind speeds. However, this was not the case for the limpet Helcion pectunculus or the top shell Oxystele antoni. Morphological differences in mollusc shape and colour could, in part, explain this contrast between species. Our results indicated that endolith-induced improvements in humidity and temperature in mussel beds could benefit associated molluscs. The beneficial thermal buffering offered by euendolithic infestation of the mussel beds was effective only if the organism was under heat stress. With global climate change, the indirect beneficial effect of euendolithic infestation for invertebrate communities associated with mussel beds may mitigate intertidal local extinction events triggered by marine heatwaves.National Research Foundation - South Africa 64801; French National Research Agency (ANR) SAN22202;info:eu-repo/semantics/publishedVersio

Microplastics in commercial bivalves harvested from intertidal seagrasses and sandbanks in the Ria Formosa lagoon, Portugal

Through seafood consumption, microplastic (MP) pollution is potentially threatening human health. Commercial bivalves in particular are a cause of major concern because their filter-feeding activity directly exposes them to MP in the water column and they are then ingested by humans. Here, we provide a quantitative and qualitative baseline data on MP content in the soft tissues of three commercially important bivalves (Ruditapes decussatus, Cerastoderma spp. and Polititapes spp.) collected in Ria Formosa lagoon, southern Portugal. The abundance of MPs (items per soft tissue weight) did not significantly differ among species. On average, R. decussatus exhibited the highest MP abundance (on average, 18.4 +/- 21.9 MP items g(-1) WW), followed by Cerastoderma spp. (11.9 +/- 5.5 MP items g(-1) WW) and Polititapes spp. (10.4 +/- 10.4 MP items g(-1) WW). Overall, 88% of the MPs found were synthetic fibres, the majority of which were blue (52%). Size categories >0.1-1 mm and >1-5 mm were the most common (60% and 34% respectively). The most represented polymers were polyethylene (PE) and polystyrene (PS). The unexpectedly high number of MPs recorded in the three commercially exploited species suggests that this semi-closed lagoon system is experiencing a higher anthropogenic pressure than are open coastal systems.Portuguese Foundation for Science and Technology: PTDC/MAR-EST/3223/2014 IF/01413/2014/CP1217/CT0004 UIDB/04326/2020 SFRH/BPD/119344/2016info: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

Congruence between fine-scale genetic breaks and dispersal potential in an estuarine seaweed across multiple transition zones

Genetic structure in biogeographical transition zones can be shaped by several factors including limited dispersal across barriers, admixture following secondary contact, differential selection, and mating incompatibility. A striking example is found in Northwest France and Northwest Spain, where the estuarine seaweed Fucus ceranoides L. exhibits sharp, regional genetic clustering. This pattern has been related to historical population fragmentation and divergence into distinct glacial refugia, followed by post-glacial expansion and secondary contact. The contemporary persistence of sharp ancient genetic breaks between nearby estuaries has been attributed to prior colonization effects (density barriers) but the effect of oceanographic barriers has not been tested. Here, through a combination of mesoscale sampling (15 consecutive populations) and population genetic data (mtIGS) in NW France, we define regional genetic disjunctions similar to those described in NW Iberia. Most importantly, using high resolution dispersal simulations for Brittany and Iberian populations, we provide evidence for a central role of contemporary hydrodynamics in maintaining genetic breaks across these two major biogeographic transition zones. Our findings further show the importance of a comprehensive understanding of oceanographic regimes in hydrodynamically complex coastal regions to explain the maintenance of sharp genetic breaks along continuously populated coastlines.Foundation for Science and Technology (FCT-MEC, Portugal) [DL57/2016/CP1361/CT0035]National Research Foundation of South AfricaNational Research Foundation - South Africa [64801]FCTPortuguese Foundation for Science and TechnologyEuropean Commission [SFRH/BPD/88935/2012, SFRH/BPD/111003/2015]Pew Marine Fellowship (USA) [SFRH/BPD/111003/2015][BIODIVERSA/004/2015][IF/01413/2014/CP1217/CT0004][UID/Multi/04326/2019]info:eu-repo/semantics/publishedVersio

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

Comparative mitogenomic analyses and gene rearrangements reject the alleged polyphyly of a bivalve genus

Background: The order and orientation of genes encoded by animal mitogenomes are typically conserved, although there is increasing evidence of multiple rearrangements among mollusks. The mitogenome from a Brazilian brown mussel (hereafter named B1) classified as Perna perna Linnaeus, 1758 and assembled from Illumina short-length reads revealed an unusual gene order very different from other congeneric species. Previous mitogenomic analyses based on the Brazilian specimen and other Mytilidae suggested the polyphyly of the genus Perna. Methods: To confirm the proposed gene rearrangements, we sequenced a second Brazilian P. perna specimen using the "primer-walking" method and performed the assembly using as reference Perna canaliculus. This time-consuming sequencing method is highly effective when assessing gene order because it relies on sequentially-determined, overlapping fragments. We also sequenced the mitogenomes of eastern and southwestern South African P. perna lineages to analyze the existence of putative intraspecific gene order changes as the two lineages show overlapping distributions but do not exhibit a sister relationship. Results: The three P. perna mitogenomes sequenced in this study exhibit the same gene order as the reference. CREx, a software that heuristically determines rearrangement scenarios, identified numerous gene order changes between B1 and our P. perna mitogenomes, rejecting the previously proposed gene order for the species. Our results validate the monophyly of the genus Perna and indicate a misidentification of B1.info:eu-repo/semantics/publishedVersio