Contemporary climate change hinders hybrid performance of ecologically dominant marine invertebrates.

Human activities alter patterns of biodiversity, particularly through species extinctions and range shifts. Two of these activities are human mediated transfer of species and contemporary climate change, and both allow previously isolated genotypes to come into contact and hybridize, potentially altering speciation rates. Hybrids have been shown to survive environmental conditions not tolerated by either parent, suggesting that, under some circumstances, hybrids may be able to expand their ranges and perform well under rapidly changing conditions. However, studies assessing how hybridization influences contemporary range shifts are scarce. We performed crosses on Pyura herdmani and Pyura stolonifera (Chordata, Tunicata), two closely related marine invertebrate species that are ecologically dominant and can hybridize. These sister species live in sympatry along the coasts of southern Africa, but one has a disjunct distribution that includes northern hemisphere sites. We experimentally assessed the performance of hybrid and parental crosses using different temperature regimes, including temperatures predicted under future climate change scenarios. We found that hybrids showed lower performance than parental crosses at the experimental temperatures, suggesting that hybrids are unlikely to expand their ranges to new environments. In turn, we found that the more widespread species performed better at a wide array of temperatures, indicating that this parental species may cope better with future conditions. This study illustrates how offspring fitness may provide key insights to predict range expansions and how contemporary climate change may mediate both the ability of hybrids to expand their ranges and the occurrence of speciation as a result of hybridization.

Keystone predation and molecules of keystone significance.

Keystone species structure ecological communities and are major determinants of biodiversity. A synthesis of research on keystone species is nonetheless missing a critical component - the sensory mechanisms for behavioral interactions that determine population- and community-wide attributes. Here, we establish the chemosensory basis for keystone predation by sea stars (Pisaster ochraceus) on mussels. This consumer-resource interaction is prototypic of top-down driven trophic cascades. Each mussel species (Mytilus californianus and M. galloprovincialis) secretes a glycoprotein orthologue (29.6 and 28.1 kDa, respectively) that acts, singularly, to evoke the sea star predatory response. The orthologues (named "KEYSTONEin") are localized in the epidermis, extrapallial fluid, and organic shell coating (periostracum) of live, intact mussels. Thus, KEYSTONEin contacts chemosensory receptors on tube feet as sea stars crawl over rocky surfaces in search of prey. The complete nucleotide sequences reveal that KEYSTONEin shares 87% (M. californianus) or 98% (M. galloprovincialis) homology with a calcium-binding protein in the shell matrix of a closely related congener, M. edulis. All three molecules cluster tightly within the Complement Component 1 Domain Containing (C1qDC) protein family; each exhibits a large globular domain, low complexity region(s), coiled coil, and at least four of five histidine-aspartic acid tandem motifs. Collective results support the hypothesis that KEYSTONEin evolved ancestrally in immunological, and later, in biomineralization roles. More recently, the substance has become exploited by sea stars as a contact cue for prey recognition. As the first identified compound to evoke keystone predation, KEYSTONEin provides valuable sensory information, promotes biodiversity, and shapes community structure and function. Without this molecule, there would be no predation by sea stars on mussels.

Multispecies genetic objectives in spatial conservation planning.

Growing threats to biodiversity and global alteration of habitats and species distributions make it increasingly necessary to consider evolutionary patterns in conservation decision making. Yet, there is no clear-cut guidance on how genetic features can be incorporated into conservation-planning processes, despite multiple molecular markers and several genetic metrics for each marker type to choose from. Genetic patterns differ between species, but the potential tradeoffs among genetic objectives for multiple species in conservation planning are currently understudied. We compared spatial conservation prioritizations derived from 2 metrics of genetic diversity (nucleotide and haplotype diversity) and 2 metrics of genetic isolation (private haplotypes and local genetic differentiation) in mitochondrial DNA of 5 marine species. We compared outcomes of conservation plans based only on habitat representation with plans based on genetic data and habitat representation. Fewer priority areas were selected for conservation plans based solely on habitat representation than on plans that included habitat and genetic data. All 4 genetic metrics selected approximately similar conservation-priority areas, which is likely a result of prioritizing genetic patterns across a genetically diverse array of species. Largely, our results suggest that multispecies genetic conservation objectives are vital to creating protected-area networks that appropriately preserve community-level evolutionary patterns.

Consistency in a marine algal-grazer interaction over multiple scales.

Coralline algae are conspicuous members of many marine assemblages, especially those characterized by intense grazing pressure. We explored whether articulated species, especially Corallina vancouveriensis, depend on grazing invertebrates to both establish and flourish in an exposed rocky intertidal setting, and whether this plant-grazer relationship varied over more than three orders of magnitude (≈100->300,000 µm). Three experimental manipulations, supplemented by observations on recruitment, demonstrated that (i) C. vancouveriensis failed to recover rapidly from disturbed areas when grazers were experimentally excluded; (ii) recruitment occurred in the presence of grazers; (iii) increasing surface texture of molded surfaces enhanced coralline recruitment more when grazers were present; and (iv) settlement occurred predominately in microtopographical low areas of a molded surface, whereas a competitively superior fleshy red alga tended to recruit to high areas. These results confirm that coralline algal establishment and persistence are enhanced by grazers and reveal that this relationship is consistent over a range of biologically relevant scales.

Indefatigable: an erect coralline alga is highly resistant to fatigue.

Intertidal organisms are subjected to intense hydrodynamic forces as waves break on the shore. These repeated insults can cause a plant or animal's structural materials to fatigue and fail, even though no single force would be sufficient to break the organism. Indeed, the survivorship and maximum size of at least one species of seaweed is set by the accumulated effects of small forces rather than the catastrophic imposition of a single lethal force. One might suppose that fatigue would be especially potent in articulated coralline algae, in which the strain of the entire structure is concentrated in localized joints, the genicula. However, previous studies of joint morphology suggest an alternative hypothesis. Each geniculum is composed of a single tier of cells, which are attached at their ends to the calcified segments of the plant (the intergenicula) but have minimal connection to each other along their lengths. This lack of neighborly attachment potentially allows the weak interfaces between cells to act as 'crack stoppers', inhibiting the growth of fatigue cracks. We tested this possibility by repeatedly loading fronds of Calliarthron cheilosporioides, a coralline alga common on wave-washed shores in California. When repeatedly loaded to 50-80% of its breaking strength, C. cheilosporioides commonly survives more than a million stress cycles, with a record of 51 million. We show how this extraordinary fatigue resistance interacts with the distribution of wave-induced water velocities to set the limits to size in this species.

Assessing the contribution of mangrove carbon and of other basal sources to intertidal flats adjacent to one of the largest West African mangrove forests.

Mangrove forests are productive habitats and major potential exporters of organic matter and nutrients to adjacent habitats. Here we examine the extent to which mangrove carbon is transferred to adjacent intertidal food webs in the second largest mangrove-covered area in Africa, in Guinea-Bissau. Applying stable isotope analysis and mixing models, we made comparisons at two spatial scales: (1) a large scale, comparing intertidal flats with (mangrove sites) and without (control sites) adjacent mangrove forests regarding the carbon isotopic signature of macrozoobenthos and sediment organic matter (SOM), and the relative importance of potential primary food sources in sustaining macrozoobenthos, and (2) a fine scale, performing stable carbon isotope measurements along 200 m transects from the coastline out to open intertidal flats, to trace mangrove carbon in macrozoobenthos and in the SOM. We found no evidence that mangrove carbon sustains intertidal food webs, despite SOM being significantly more depleted in 13C in mangrove sites. Mangrove leaves had the lowest relative contribution to the diet of macrozoobenthos, while macroalgae, benthic microalgae and POM showed variable but overall relevant contributions. Yet, at a smaller scale, mangrove carbon was detectable in SOM and in most macrozoobenthos, being strongest within 50 m of the mangrove edge and quickly fading with increasing distance. Our results suggest that there is only a marginal input of mangrove carbon into the food webs of unvegetated intertidal flats. Still, this leaves open the possibility of mangrove forests acting as sources of dissolved inorganic carbon and processed nitrogen, which can be assimilated by the algae and subsequently fuel adjacent food webs.

Limpet disturbance effects on barnacle recruitment are related to recruitment intensity but not recruit size.

Intertidal limpets are important grazers along rocky coastlines worldwide that not only control algae but also influence invertebrates such as common barnacles. For instance, grazing limpets ingest settling barnacle cyprid larvae (hereafter cyprids) and push cyprids and barnacle recruits off the substrate. Such limpet disturbance effects (LDEs) can limit barnacle recruitment, a key demographic variable affecting barnacle population establishment and persistence. In this study, we examined limpet (Lottia cassis) disturbance to barnacle (Chthamalus dalli, Balanus glandula) recruitment on the Pacific coast of Hokkaido, Japan, as information on limpet-barnacle interactions from this region is missing. We investigated, for the first time, whether barnacle size and recruitment intensity influence LDEs on barnacle recruitment. Small barnacles may be less susceptible to LDEs than larger barnacles, because small size may reduce the propbability of limpet disturbance. Moreover, recruitment intensity can influence LDEs, as high recruitment can compensate for LDEs on barnacle recruitment density. In Hokkaido, C. dalli cyprids are smaller than B. glandula cyprids, and C. dalli recruitment is higher than B. glandula recruitment. Thus, we hypothesized that LDEs on C. dalli recruitment would be weaker than those on B. glandula recruitment. To test our hypothesis, we conducted a field experiment during which we manipulated limpet presence/absence on the interior surfaces of ring-shaped cages. After four weeks, we measured barnacle recruitment and recruit size on the interior surfaces of the cages and found negative LDEs on C. dalli and B. glandula recruitment and recruit size. As hypothesized, the LDEs on C. dalli recruitment were weaker than the LDEs on B. glandula recruitment. Additionally, C. dalli recruits were smaller than B. glandula recruits. However, the LDEs on C. dalli recruit size were as strong as the LDEs on B. glandula recruit size, indicating that the smaller C. dalli recruits are not less susceptible to LDEs than B. glandula recruits. Since C. dalli recruitment was higher than B. glandula recruitment, we propose that the higher C. dalli recruitment compensated for the LDEs on C. dalli recruitment. Our findings indicate that the detected differences in LDEs on barnacle recruitment are related to barnacle recruitment intensity but not recruit size.

Distinct Size and Distribution Patterns of the Sand-sifting Sea Star, Archaster typicus, in an Urbanised Marine Environment.

Yong Kit Samuel Chan, Tai Chong Toh, and Danwei Huang (2018) Archaster typicus is a microphagous sea star ubiquitous throughout sandy shoals of the Indo-Pacific. Along highly urbanised coasts, loss of sandy habitats through land reclamation and degradation of adjacent mangrove forests and seagrass meadows, which serve as nurseries for A. typicus, could lead to local extinction of this species. To determine the population status of A. typicus in Singapore, we performed belt-transect surveys at three modified shores, then compared size structure, clustering patterns and ontogenetic shifts within the Central Indo-Pacific region. We found that A. typicus individuals were, among other things, larger in Singapore (79.2 ± 14.2 mm) than the rest of the Central Indo-Pacific region with further differences amongst Singapore's sites. Sea stars of this species were also greatly clustered in smaller areas within the transects, with most transects presenting small Nearest Neighbour Index values of < 1. While ontogenetic shifts were noted in previous studies, no juveniles have been recorded in the nursery habitats of mangroves and seagrasses, with limited size and mating seasonalities. Although A. typicus appears to have grown in size considerably on reclaimed beaches in Singapore, the lack of any apparent ontogenetic connectivity here may threaten the sea star populations in the near future, particularly in the context of growing coastal development in Southeast Asia.

Unusually low genetic divergence at COI barcode locus between two species of intertidal Thalassaphorura (Collembola: Onychiuridae).

Species classification is challenging when taxa display limited morphological differences. In this paper, we combined morphology and DNA barcode data to investigate the complicated taxonomy of two Onychiurid Collembolan species. Thalassaphorura thalassophila and Thalassaphorura debilis are among the most common arthropod species in intertidal ecosystems and are often considered to be synonymous. Based on morphological and barcode analyses of fresh material collected in their type localities, we redescribed and compared the two species. However, their morphological distinctiveness was supported by a molecular divergence much smaller than previously reported at the interspecific level among Collembola. This divergence was even smaller than inter-population divergences recognized in the related edaphic species T. zschokkei, as well as those known between MOTUs within many Collembolan species. Our results may indicate a link between low genetic interspecific divergence and intertidal habitat, as the only biological peculiarity of the two species of interest compared to other Collembolan species analyzed to date is their strict intertidal life.

Upwelling-derived oceanographic conditions impact growth performance and growth-related gene expression in intertidal fish.

Growth is one of the main biological processes in aquatic organisms that is affected by environmental fluctuations such as upwelling (characterized by food-rich waters). In fish, growth is directly related with skeletal muscle increase; which represents the largest tissue of body mass. However, the effects of upwelling on growth, at the physiological and molecular level, are unknown. This study used Girella laevifrons (one of the most abundant intertidal fish in Eastern South Pacific) as a biological model, considering animals from upwelling (U) and non-upwelling (NU) areas. Here, we evaluated the effect of nutritional composition and food availability on growth performance and expression of key growth-related genes (insulin-kike growth factor 1 (igf1) and myosin heavy-chain (myhc)) and atrophy-related genes (muscle ring-finger 1 (murf1), F-box only protein 32 (atrogin-1) and BCL2/adenovirus E1B 19kDa-interacting protein 3 (bnip3)). We reported that, among zones, U fish displayed higher growth performance in response to nutritional composition, specifically between protein- and fiber-rich diets (~1g). We also found in NU fish that atrophy-related genes were upregulated with fiber-rich diet and during fasting (~2-fold at minimum respect U). In conclusion, our results suggest that the growth potential of upwelling fish may be a consequence of differential muscle gene expression. Our data provide a preliminary approach contributing on how upwelling influence fish growth at the physiological and molecular levels. Future studies are required to gain further knowledge about molecular differences between U and NU animals, as well as the possible applications of this knowledge in the aquaculture industry.

Site fidelity, size, and morphology may differ by tidal position for an intertidal fish, Bathygobius cocosensis (Perciformes-Gobiidae), in Eastern Australia.

The intertidal zone is a transitional environment that undergoes daily environmental fluctuations as tides rise and fall. Relatively few fish species are adapted to endure the physiological pressures of this environment. This study focused on Bathygobius cocosensis (Gobiidae), a common intertidal fish in New South Wales, Australia. We investigated whether shore height impacted site fidelity, survival probability, fish size, and morphological traits with respect to tidal height. Mark-recapture methods were used over a five month period to determine if individuals in high shore pools had greater site fidelity; fish in high tide pools were more than twice as likely to be recaptured in their original pool than fish from low tide pools. High pool individuals were, on average, smaller with larger eyes and longer snouts relative to their size as compared to low pool individuals. We discuss several mechanisms that could cause the observed pattern in morphological variation. Ultimately, this study suggests that within species behaviour and morphology differ by tidal position for an intertidal fish.

Sublethal stress in the intertidal zone: tidal emersion inhibits photosynthesis and retards development in embryos of the brown alga Pelvetia fastigiata.

The effect of tidal emersion on survivorship, photosynthesis and embryonic development was studied in 8 h old zygotes and 7 d old embryos of the intertidal brown alga Pelvetia fastigiata (J. Ag.) DeToni. Zygotes and embryos were outplanted for single low tides in the intertidal zone on the central coast of California (U.S.A.) during June, 1990. Both zygotes and embryos exhibited close to 100% survival when outplanted beneath the canopy of adult P. fastigiata. Embryos (7 d old) also exhibited high survival when outplanted in a red algal turf, the microhabitat where most successful recruitment occurs. However, zygotes (8 h old) experienced high mortality (65-90%) when outplanted in the turf microhabitat. Embryos and zygotes that survived emersion experienced sub-lethal stress that temporarily impaired light-saturated photosynthesis when plants were reimmersed in seawater. The effects of sub-lethal stress were more pronounced in 8 h old zygotes than 7 d embryos, and more severe in the turf microhabitat than beneath the adult Pelvetia canopy. Zygotes outplanted in the red algal turf did not re-establish net photosynthesis until at least 6 h after re-immersion. Photosynthesis was less inhibited in 8 h old zygotes outplanted beneath the adult Pelvetia canopy, and recovered to control (non-emersed) levels within 3 h of re-immersion. Embryos (7 d old) were able to achieve positive net photosynthesis immediately on re-immersion after emersion in the turf or canopy microhabitats. Emersion also retarded the rate of embryonic development in 8 h old zygotes, delaying the formation of primary rhizoids, which help to attach the plant to the substrate. For example, at 19 h post-fertilization, 75% of control (non-emersed) zygotes had developed rhizoids, compared to 3% and 30% for zygotes outplanted in the turf and canopy microhabitats. The different emersion responses of 8 h old zygotes and 7 d old embryos appeared to be related to their ability to tolerate cellular dehydration. Overall, our data suggest that the effects of sub-lethal stresses may have been underestimated in studies of intertidal ecology.

Sex-specific winter distribution in a sexually dimorphic shorebird is explained by resource partitioning.

Sexual size dimorphism (SSD) implies correlated differences in energetic requirements and feeding opportunities, such that sexes will face different trade-offs in habitat selection. In seasonal migrants, this could result in a differential spatial distribution across the wintering range. To identify the ecological causes of sexual spatial segregation, we studied a sexually dimorphic shorebird, the bar-tailed godwit Limosa lapponica, in which females have a larger body and a longer bill than males. With respect to the trade-offs that these migratory shorebirds experience in their choice of wintering area, northern and colder wintering sites have the benefit of being closer to the Arctic breeding grounds. According to Bergmann's rule, the larger females should incur lower energetic costs per unit of body mass over males, helping them to winter in the cold. However, as the sexes have rather different bill lengths, differences in sex-specific wintering sites could also be due to the vertical distribution of their buried prey, that is, resource partitioning. Here, in a comparison between six main intertidal wintering areas across the entire winter range of the lapponica subspecies in northwest Europe, we show that the percentage of females between sites was not correlated with the cost of wintering, but was positively correlated with the biomass in the bottom layer and negatively with the biomass in the top layer. We conclude that resource partitioning, rather than relative expenditure advantages, best explains the differential spatial distribution of male and female bar-tailed godwits across northwest Europe.