Adaptations and plastic phenotypic responses of marine animals to the environmental challenges of the high intertidal zone

The high intertidal zone is home to an incredible variety of marine animals, as it offers an escape from low intertidal/subtidal predation and competition, among other advantages. However, this area of the shore also comes with many tide-driven and emersion-associated environmental stressors, such as desiccation, high temperatures and freezing stress, hypoxia, salinity fluctuations, nitrogenous waste accumulation, ultraviolet (UV) radiation, wave and ice disturbance, and hydrogen sulphide (H2S) toxicity. This review explores the diversity of evolutionary adaptations and plastic phenotypic responses that high intertidal animals use to cope with these challenges. Examples are provided of behavioural, morphological, physiological and biochemical adaptations/responses, along with some of the underlying molecular mechanisms that have been elucidated to date. Adaptations of many different worms, anemones, molluscs, crustaceans and fishes are highlighted. Many adaptations and mechanisms of plasticity are universal among animal phyla, and some are multifunctional (serve more than one function) or provide tolerance to multiple stressors (i.e., ‘cross-tolerance’). High intertidal animals have received considerable attention by scientists, given their accessibility and that they can provide valuable insights in the transition from a marine to a terrestrial lifestyle. Nevertheless, further research is needed to understand the adaptations/responses of these animals more thoroughly, and the future holds great promise for accomplishing this with recent advances in epigenetics, transcriptomics, protein biochemistry and other molecular tools.

The Subhabitat Dependence of Biogeographic Pattern

We introduce and test the subhabitat dependence hypothesis (SDH) in biogeography. This hypothesis posits that biogeographic pattern within a region differs when determined with species abundance data from different subhabitat types. It stems from the notion that the main abiotic factors that drive species distribution in different subhabitat types across a biogeographic region often vary differently across space. To test the SDH, we measured the abundance of algae and sessile invertebrates in two different subhabitats (high intertidal zone and mid-intertidal zone) at eight locations along the Atlantic Canadian coast. We conducted multivariate analyses of the species abundance data to compare alongshore biogeographic pattern between both zones. For both subhabitat types, location groupings based on community similarity not always responded to geographic proximity, leading to biogeographic patchiness to some extent. Nonetheless, both biogeographic patterns were statistically unrelated, thus supporting the SDH. This lack of concordance was most evident for southern locations, which clustered together based on high-intertidal data but showed considerable alongshore patchiness based on mid-intertidal data. We also found that the ordination pattern of these eight locations based on sea surface temperature data was significantly related to biogeographic pattern for the mid-intertidal zone but not for the high intertidal zone. This finding supports the rationale behind the SDH due to the longer periods of submergence experienced by the mid-intertidal zone. Overall, we conclude that biogeographic pattern within a region can depend on the surveyed subhabitat type. Thus, biological surveys restricted to specific subhabitats may not properly reveal biogeographic pattern for a biota as a whole or even just for other subhabitats. As many studies generate biogeographic information with data only for specific subhabitats, we recommend testing the SDH in other systems to determine its domain of application.

Responses of the mussel Brachidontes rodriguezii to aerial exposure: implications on growth and physiological condition

The length of aerial exposure (i.e., environmental conditions) of an organism, due to daily tides, induces physiological responses. A mark–recapture field experiment was conducted in two intertidal zones (low tide and high tide) using the stain calcein AM to determine growth, as measured by shell length, of the mussel Brachidontes rodriguezii (d’Orbigny, 1842) along its vertical distribution off the north Argentinean coast. In the high intertidal zone, B. rodriguezii exhibited slower growth in shell length because of the physiological stress resulting from aerial exposure during low tides. In the low intertidal zone and during spring, B. rodriguezii exhibited faster growth in shell length. It is suggested that growth of B. rodriguezii relies on several environmental factors (temperature, photoperiod, and aerial exposure) that fluctuate according to tidal height.

Quantitative analyses of decapod crustaceans at a rocky intertidal shore in the Gulf of Oman, Iran: diversity, zonation and monsoonal fluctuations

This paper provides data on diversity, zonation and seasonal fluctuations of decapod crustaceans at the northern Gulf of Oman coast, based on quantitative and qualitative samplings. A total of 75 species belonging to four infraorders, 27 families and 48 genera were identified. These species include 20 new records for the entire Gulf of Oman and 13 new records for its Iranian coast. The mid-intertidal zone showed a higher mean diversity and abundance than high- and low-intertidal zones. The mean diversity and abundance in the high-intertidal zone showed significant differences with the mid- and low-intertidal zones. The indices of species richness (Margalef), diversity (Shannon) and evenness (Pielou) showed significant differences among the intertidal zones. Most of the identified species (>60%) that had high values in their frequency of occurrence and relative abundance showed an overlapping vertical distribution, and were present in all three or just in two of the three defined zones. Other species were found only in one of the three zones (non-overlapping vertical distribution). The decapod community in the mid-intertidal zone showed a higher dissimilarity with the high-intertidal zone than with the low-intertidal. Both abundance and diversity were found to be lowest and highest during south-west and north-east monsoons, respectively. During south-west monsoon, the abundance of decapods declined dramatically, but species diversity and ecological indices did not show any statistically significant difference among the sampling periods.

Cyanobacteria isolated from the high-intertidal zone: a model for studying the physiological prerequisites for survival in low Earth orbit

Cyanobacteria are capable of surviving the adverse conditions of low Earth orbit (LEO). We have previously demonstrated thatGloeocapsastrain OU_20,Chroococcidiopsisand akinetes ofAnabaena cylindricawere able to survive 548 days of exposure to LEO. Motivated by an interest to understand how cyanobacteria can survive in LEO, we studied the strategies thatGloeocapsastrain OU_20 employs to survive in its natural environment, the upper region of the intertidal zone. Here, cyanobacteria are exposed to fluctuations in temperature, UV radiation, desiccation and salinity. We demonstrated that an increase in salinity from 6.5‰ (BG-11 medium) to 35.7‰ (similar to that of seawater), resulted in increased resistance to UV radiation (254 nm), vacuum (0.7×10−3±0.01 kPa) and cold temperatures (–20 °C). Concomitantly, biochemical analyses demonstrated that the amount of fatty acids and mycosporine-like amino acids (a UV absorbing pigment) were higher in the stressed cells. Morphological analysis demonstrated that the electron density and thickness of the mucilaginous sheath were also greater than in the control cells. Yet, the control and stressed cells both formed aggregates. As a result of studying the physiological adaptation ofGloeocapsastrain OU_20 in response to salinity, we postulate that survival in the high-intertidal zone and LEO involves a dense extracellular mucilaginous sheath and the formation of aggregates. We conclude that studying the physiological adaptation of cyanobacteria in the intertidal zone provides insight into understanding survival in LEO.

A combined field and modeling study of groundwater flow in a tidal marsh

Bald mud beaches were found among the mangrove marshes in Dongzhaigang National Nature Reserve, Hainan, China. To investigate the possible reasons for this phenomenon, the intertidal zones of a mangrove transect and a bald beach transect with similar topography and same tidal actions were selected for comparison study. Along both transects, observed water table variations were significant in the high and low intertidal zones and negligible in the middle intertidal zones. Field investigations and observations invite two speculations: (1) existence of a high-permeability zone on each transect which underlies the low-permeability surface mud sediments and outcrops in the high intertidal zone, and (2) considerable inland freshwater recharge along the mangrove transect but negligible freshwater recharge along the bald beach transect. Two-dimensional numerical simulations based on these speculations gave results in line with the observed water table. The bald beach is most probably due to the lack of enough freshwater for generating a brackish beach soil condition essential to mangrove growth. It is also indicated that seawater infiltrated the high-permeability zone through its outcrop near the high intertidal zone, and discharged from the tidal river bank in the vicinity of the low tide line, thereby forming a tide-induced seawater-groundwater circulation which may provide considerable contribution to the total submarine groundwater discharge.

Variation in mussel and barnacle recruitment parallels a shift in intertidal community structure in the Cook Strait region of New Zealand

Recruitment influences populations and communities of marine organisms to varying degrees and across a range of spatial scales. We hypothesised that recruitment plays a role in maintaining different intertidal invertebrate assemblages between two nearby locations in New Zealand (Wellington Harbour and the south coast), long reported to have dramatically different communities (with greater cover of sessile invertebrates in the Harbour). Sites in Wellington Harbour were hypothesised to have higher monthly recruitment rates of mussels and barnacles and greater barnacle colonisation after 1 year. Surveys were conducted to quantify community differences. In Wellington Harbour, the mid-intertidal zone was dominated by the mussel Mytilus galloprovincialis and the barnacle Chamaesipho columna and the high intertidal zone by C. columna. In contrast, on the south coast mussels were almost completely absent from both tidal heights and barnacles (predominantly Chamaesipho brunnea) were sparse. In the high zone, monthly recruitment and long term colonisation (over 1 year) of barnacles was much greater in the Harbour; in the mid-intertidal zone, mussel recruitment was up to two orders of magnitude greater in the Harbour than the south coast. Species-specific recruitment patterns differed between the locations, however and were consistent with those of adult abundance.

A new genus and species of polyclad flatworm found in the mantle cavities of gastropod molluscs in the high-intertidal zone of the Pacific coast of Central America

A commensal relationship is described between the polyclad flatworm Paraprostatum echinolittorinae Faubel & Sluys gen. et sp. nov. and gastropod molluscs living on the Pacific coast of central America. Although the worms are relatively large in comparison with their hosts, the latter sustained no apparent damage. Considering the fact that the molluscs live in the upper eulittoral zone and littoral fringe of the shore, it is unlikely that the polyclads could survive for long outside the hosts. Diagnostic characters for the new genus and species are a long penial stylet joined to the proximal vesicle and absence of Lang's vesicle. It is pointed out that Aprostatum clippertoni Bock, 1913 and A. longipenis (Kato, 1943) have been incorrectly transferred to the genus Euplana Girard, 1893 and that Discoplana malagensis Doignon, Artois & Deheyn, 2003 should be transferred to the genus Ilyella Faubel, 1983.

Littoral Stratification in Growth form and Fecundity of the Rock Barnacle, Semibalanus Balanoides

The population dynamics of rock barnacles, Semibalanus balanoides (L.), residing in low and high intertidal zones are affected by conspicuously different factors. The barnacle population in the high intertidal zone tends to show longterm stability due to a low incidence of both predation and interspecific competition. Wave exposure, desiccation and intraspecific competition are more important factors affecting abundance and size distribution in this zone (Menge, 1976). In the low intertidal zone, barnacle predation by the dogwhelk, Nucella lapillus (L.) is intense (Menge, 1976) and both the adults and larvae are smaller than in the high intertidal zone (Barnes, 1953). The growth form of S. balanoides is density dependent with taller, more columnar individuals predominating at high densities and short conical barnacles at low densities. Lower fecundity of conical individuals may be due to lower internal shell volume compared with columnar forms (Wethey, 1984). Fecundity increases both with increasing age and base length (Arnold, 1977) and is positively density dependent (Wethey, 1984).