Читать книгу Marine Mussels - Elizabeth Gosling - Страница 16

As already mentioned, one of the most significant developments in bivalve evolution was the emergence of the heteromyarian form, possibly from a putative isomyarian infaunal ancestor (Figures 1.3 and 1.5A). The form – most pronounced in the Mytilidae – when coupled with secure byssal attachment allowed mussels to anchor themselves and live in high population densities in wave‐exposed habitats (Morton 1996). Species of Mytilidae that exhibit varying degrees of heteromyarianism are found in the subfamilies Arcuatulinae, Brachidontinae, Mytilinae, Modiolinae, Musculinae, Septiferinae and Limnoperninae. Infaunal (endobyssate) mytilids inhabit both hard and soft substrates and are less heteromyarian, but more diverse, than epifaunal (epibyssate) rocky shore mytilids. The most significant adaptation in infaunal mytilids is a shell that is long and narrow (modioliform), allowing large numbers of individuals to form dense beds. The following text is heavily reliant on Morton (1992).

The posteriorly elongated shell keeps the inhalant and exhalant orifices in these fixed bivalves above the sediment water interface (Figure 1.5B). Enlargement of the posterior face of the shell and reduction of the anterior has resulted in the development of larger posterior adductor and posterior byssal retractor muscles and reduced anterior adductor and anterior byssal retractor muscles. In Perna, the anterior adductor muscle has been lost entirely, making the genus the only monomyarian one that has retained the heteromyarian form (Morton 1987). In addition, there has been an enlargement of the ligament, which probably acts to keep the two shell valves correctly aligned, particularly since another consequence of heteromyarianism is either a large reduction in hinge plate and teeth or their loss. Another adaptive feature, exemplified by species of Musculista, Modiolus and Arcuatula, is a thin, brittle shell that provides sufficient protection for an attached, infaunal lifestyle. Epibyssate mytilids (e.g. Septifer and Brachidontes) have much thicker sculptured shells that help to withstand the effects of wave action and provide protection against predatory snails, crabs and birds. To enhance stability around the point of byssal attachment, the antero‐ventral region of the shell valves is flattened, both laterally and antero‐posteriorly. Flattening of the shell provides greater stability on wave exposed shores by opposing an overturning force and lowering the centre of gravity, thereby reducing the effects of drag. Such an adaptation is clearly associated with the full expression of heteromyarianism and thus the successful colonisation of hard subtrates (Figure 1.5C). For some mytilids (e.g. Mytilus spp.), however, this adaptation has released them from a colonial life, and some (e.g. Septifer bilocularis) are completely solitary. Ventral flattening also resulted in development of the umbones into ‘beaks’, which, with the progressive assumption of the heteromyarian form, are located in a subterminal position beyond the reduced anterior edge of the shell. There are a few points worth noting. In infaunal habitats, some species (e.g. Brachiodontes erosus) possess a cyclindrical shell, but the shell is more triangular and ventrally flattened when the species is epifaunal (Morton 1991). According to Morton (1970), the essential adaptations necessary in the development of the heteromyarian shell probably commenced in infaunal lineages, as a wide range of extant mytilids still possess features that adapt them for an endobyssate mode of life (e.g. a pallial sinus, an elongated modioliform shell and a smooth and often thin shell).

Figure 1.5 Lateral views (A–C) and transverse sections (A1–C1) of (A) an isomyarian, (B) a modioliform, and (C) a mytiliform bivalve; a = axis through the adductor muscles; d = the mid‐dorso‐ventral axis of the shell; h = the hinge axis; m = the mid‐dorsal and foot (byssus) axis; and w = the position of greatest shell width.

Source: From Morton (1992). Reproduced with permission from Elsevier.

The evolution of hard calcareous coral reefs in the Mesozoic (252–66 mya) was an event that foresaw important phases of molluscan adaptive radiation (Morton 1990). In the family Mytilidae, borers of coral skeletons, rock and even wood constitute an excellent example of such a radiation. The evolution of gastropod predators is regarded as the driving force for coral–bivalve associations (Morton 1990). Exploitation of living coral as a habitat was facilitated by the evolution of larval adaptations, enabling them to penetrate living coral tissue and thereby develop mechanisms to overcome coral defences (Morton 1990). The boring life habit developed independently in both epifaunal and infaunal ancestors and also in at least five other families of clams: Gastrochaenidae, Petricolidae, Pholadidae, Clavagellidae and Tridacnidae (references in Ockelmann & Dinesen 2009). In the Mytilidae there are about 78 species of borers in six genera: Adula (7 species), Botula (6), Fungiacava (1), Gregariella (17), Leiosolenus (36) and Lithophaga (11). The majority of species use chemical means to bore into calcareous rocks or corals, while Adula and Botula, for example, are mechanical borers in softer clay and chalk (Kleemann 1990). The boring habit was made possible by the elongated shell as seen in Adula, Botula and Lithophaga, which probably evolved from a heteromyarian ancestor like Modiolus (Kleemann 1990). The exceptionally long shell ligament in the Mytilidae, with its consequent powerful opening thrust, represents another preconditioning factor that made boring possible. Coevolution between some borers and certain living corals has been suggested (Mokady et al. 1994).

In the chemical borer Lithophaga, the dorsal extension of the mantle edges was accompanied by increased mucus secretion to aid in cleansing. Protrusion of these tissues, and direct application by them of the mucous, provided the means of chemical boring (Kleemann 1990). Initially, the mucous was believed to be acidic, but histochemical tests have since shown that the secretion is a neutral mucoprotein with calcium‐binding ability. This finding indicates that in Lithophaga the complexing of calcium by the secretion of the pallial glands is the mechanism of chemical boring into calcareous rock (Jaccarini et al. 1968). The boring glands in the Lithophaga may be derived from the cocoon‐forming cells of a nest‐building bivalve like Arcuatula (Morton 1982). According to Yonge (1955), all boring in the Mytilidae was initially mechanical. In mechanical borers such as Botula and Adula, firm attachment is made by byssal threads arranged in a large anterior and a small posterior group. These threads are much more numerous but less localised than in chemical borers. Noncalcareous rock is abraded by the dorsal surfaces of the valves, which are deeply eroded. The posterior byssal retractors and the exceptionally long ligament provide the force needed for boring. The former deepens the boring by forcing the anterior end of the shell against the rock, while the latter widens it by forcing apart the shell valves.

The result of boring activity is referred to as bioerosion (Warme 1975), which includes both bioabrasion and biocorrosion. Species of Lithophaga bore into dead and live coral and are most abundant subtidally, with some attacking reef corals to their lower depth limits. The siphonal openings of Lithophaga typically have a keyhole‐like appearance on coral surfaces and the circular holes penetrate vertically into the coral skeleton, from 1 to 10 cm deep depending upon the species. Population densities in productive equatorial eastern Pacific waters range from 500 to 10 000 individuals/m² (Scott et al. 1988), which can lead to rapid reef erosion. Bioerosion also renders coral more susceptible to physical erosion (see review by Glynn & Manzello 2015).

An unusual example of adaptive radiation in the Mytilidae is one in which mussels have colonised chemosynthetic habitats such as hydrothermal and cold‐seep vents in deep oceanic waters (Figure 1.6). These are places where chemical‐rich fluids exude from the seafloor, often providing the energy to sustain rich communities in very harsh environments. The habitats differ from one another in the underlying conditions that form and drive them. While mussels dominate many vents and cold seeps worldwide, they are also common in other sulphide‐rich habitats such as whale carcasses and sunken wood (Duperron 2010) – habitats that are regarded as stepping stones to deep‐sea vents (Distel et al. 2000). Mussels thrive in such habitats because of the symbiotic bacteria housed in their gills. Some of these symbionts harness energy by oxidising methane to carbon dioxide, while others do so by oxidising hydrogen sulphide to sulphate (Orphan & Hoehler 2011). The sulphide‐oxidising bacteria can also use hydrogen as an energy source, oxidising it to water (Petersen et al. 2011 and references therein). Mussels absorb nutrients synthesised by the bacteria, while they also filter‐feed from surrounding waters. Genera such as Bathymodiolus and Tamu are dominant at hydrothermal vents and cold seeps, while small‐sized mussels in the genera Idas, Adipicola and Benthomodiolus inhabit sunken wood, vegetal debris and bones on the ocean floor. This decomposing organic matter produces sulphide, which is used by mussels through symbionts similar to those of vent and seep mussels (Duperron et al. 2009). Another genus, Giganticus, inhabits warm water seeps near active volcanoes in the Southern Hemisphere. In addition to a diversity of habitats, many mussels live in a dual symbiosis with both sulphur‐ and methane‐oxidising bacteria. Indeed, as many as six distinct symbionts have been recorded in the gills of a single species of Idas, thereby allowing greater flexibility to the host in the use of substrates (Duperron et al. 2008). Mussels from chemosynthesis‐based ecosystems have several features in common, including a modioliform shell, reduced labial palps and digestive system, greatly enlarged gills and planktotrophic larvae with large dispersal abilities (see Duperron 2010 for details).

Figure 1.6 Vent mussels and associated fauna are bathed in hydrothermal fluids at the Wideawake vent field on the Mid‐Atlantic Ridge. Photo taken by the remotely operated, deep‐sea submersible MARUM‐QUEST.

Source: From Orphan & Hoehler (2011). Reproduced with permission from Nature Publishing Group.

Although these mussels were initially regarded as archaic, molecular age estimates and fossil records suggest that most of the modern vent and seep animals appeared during a short time interval between the Late Mesozoic and the Early Cenozoic, less than 100 mya (Van Dover et al. 2002). The evolutionary history of deep‐sea symbiotic mussels has been investigated over the past two decades using a range of mitochondrial and nuclear DNA markers. Distel et al. (2000) were the first to propose the stepping stone hypothesis (i.e. that vent and seep mussels derived from ancestors associated with wood and whale fall ecosystems). Results from subsequent phylogenetic studies have strongly supported this proposal (Samadi et al. 2007; Miyazaki et al. 2010; Lorion et al. 2013; Thubaut et al. 2013). Rather than a single step toward colonisation of vents and seeps, there were multiple habitat shifts from organic substrates to vents and cold seeps, always in the one direction (Thubaut et al. 2013). Cold seeps seem to be an intermediate habitat for the colonisation of deep vents (Thubaut et al. 2013). Ancestors of Bathymodiolus mussels were shallow species that acquired the ability to associate with bacteria, most likely sulphur oxidisers (Duperron 2010). For mussels, the acquisition of such symbionts is seen as a prerequisite for their adaptation to, and successful radiation within, chemosynthetic environments (Lorion et al. 2013). Subsequent acquisition of methanotrophic symbionts allowed the colonisation of new niches within the vent and seep habitats, resulting in a second wave of diversification (Lorion et al. 2013). To date, there is no general consensus on the phylogenetic relationships of deep‐sea Bathymodiolus mussels and their mytilid relatives (see Jones et al. 2006; Fujita et al. 2009; Miyazaki et al. 2010; Thubaut et al. 2013; Oliver 2015).