Contributions to Zoology, 86 (2) – 2017Nikolai Y. Neretin; Anna E. Zhadan; Alexander B. Tzetlin: Aspects of mast building and the fine structure of “amphipod silk” glands in Dyopedos bispinis (Amphipoda, Dulichiidae)

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Introduction

Many amphipods are able to construct dwellings and make various burrows, tubes and masts (Atkinson and Eastman, 2015; Moore and Eastman, 2015). Masts, which are also known as whips and rods, are thin, flexible vertical structures that are attached to the substrate at one end, and they improve filter-feeding efficiency by elevating the amphipod above the seabed to heights more than 10 times their body length (Mattson and Cedhagen, 1989). It has also been suggested that mast building provides protection from predation (Mattson and Cedhagen, 1989, Thiel, 1999). Furthermore, amphipods exhibit complex territorial behaviour and obligate extended parental care, which is unusual for most tube-building amphipods (Mattson and Cedhagen, 1989; Thiel, 1997, 1998a, 1998b, 1999). Additionally, masts can be used by amphipods to cultivate diatoms (McCloskey, 1970).

Amphipods build masts on different substrates in various biotopes. Dulichia rhabdoplastis, McCloskey, 1970 build masts on the spines of sea urchins; Dyopedos monacantha (Metzger, 1875) prefer soft bottoms; whereas Dyopedos porrectus Bate, 1857 typically live on hard bottoms and associate with hydroids (McCloskey, 1970; Moore and Earll, 1985; Mattson and Cedhagen, 1989; Thiel, 1998b). In certain biotopes, mast-building amphipods are abundant; the density of Dyopedos monacantha reaches more than 3000 individuals per square metre (Thiel, 1998b) while that of Dyopedos bispinis masts in the White Sea can exceed 2000 per square metre (Zhadan et al., 2007). However, little is known regarding the influence of mast-building on benthic communities.

The social structures of masts were studied in Dyopedos monacantha in aquaria and under natural conditions (Mattson and Cedhagen, 1989; Thiel, 1997, 1998a, 1998b, 1999). Each mast belongs to a juvenile amphipod or one adult female and is the territory of that individual. Juveniles remain on their mother’s mast, and members of two consecutive clutches can be present, but it is unknown whether they participate in mast building. Adult males do not build their own masts but participate in the maintenance of the masts of females. While the social structure of other mast-building amphipods has rarely been studied (McCloskey, 1970; Moore and Earll, 1985; Mattson and Cedhagen, 1989), it can differ from that of Dyopedos monacantha; for example, adult male Dyopedos porrectus build their own masts.

In contrast, with epibenthic amphipod tubes, which are relatively short, i.e., rarely greater than 3-4 amphipod body lengths (Shillaker and Moore, 1978; Dixon and Moore, 1997), masts are large-scale structures. Masts built by the amphipod Dyopedos bispinis Gurjanova, 1930 in the White Sea can reach 10 and occasionally even 20 cm, 20 and 40 times longer than the length of an adult female, respectively (our unpublished data). Mattson and Cedhagen (1989) observed mast building in Dyopedos monacantha and Dyopedos porrectus in aquariums and found that amphipods fasten detritus together using mucus threads produced by the gnathopods and mouthparts, and the detritus is subsequently covered with silk threads from the pereopods. Detritus collection methods (from the water column and from the bottom) vary in different species and in different conditions (Mattson and Cedhagen, 1989). Scanning electron microscopy (SEM) was used to characterize the silk network on the surface of the Dyopedos porrectus mast (Moore and Earll, 1985), but the internal structure of masts has not been studied in detail. Therefore, the proportions of mouthpart secretion, pereopodal secretion and detritus in the mast remain unclear.

To build masts and tubes, amphipods use special secretions that are typically called “amphipod silk” (Smith, 1874; Goodhart, 1939; Dixon and Moore, 1997; Cerda et al., 2010, Kronenberger et al., 2012a,b). In some cases, this secretion is a mucus cement (Goodhart, 1939), but in most amphipod species, it is produced in the form of threads (Skutch, 1926; Shillaker and Moore, 1978; Moore and Earll, 1985; Barnard et al., 1988; Mattson and Cedhagen, 1989; Cerda et al., 2010; Zorn et al., 2010; Kronenberger et al., 2012a). Generally, silks are defined as protein polymers produced and spun into fibres by various arthropods (Altman et al., 2003; Sutherland et al., 2010). Insect and spider silks are well known and are currently subject to intense biochemical studies (Kovoor, 1987; Foelix, 2010; Sutherland et al., 2010; Kundu et al., 2014). Certain crustaceans (belonging to Amphipoda, Tanaidacea, Ostracoda and Decapoda) also produce silk-like materials (Wouters and De Grave, 1992; Dworschak, 1998; Kronenberger et al., 2012a; Kakui and Hiruta, 2014), but their chemical structure and the morphology of the silk glands are poorly known. Currently, only one crustacean silk from the amphipod Crassicorophium bonellii (Milne Edwards, 1830) has been chemically investigated (Kronenberger et al. 2012a).

Amphipod silk is secreted from a special large glandular complex located in pereopods 3-4, and the presence of such complexes has been described in most corophiid families and in the family Ampeliscidae (Myers and Lowry, 2003; Cadien, 2015). Nebeski (1880) described the structure of the glandular complex in pereopods 3-4 of Jassa falcata (Montagu, 1808) and certain other tube-building corophiid species. The findings showed that each pereopod contains two gland groups (proximal and distal) that stain differently as well as a common reservoir and a single opening in the dactylus tip. The glands, which belong to the proximal group, have an elongated form and are multicellular, comprising secretory cells that lie along ducts. The ductules from each secretory cell communicate with these ducts individually and in sequence. The glands of another distal group can be unicellular or similar to the proximal glands. Kronenberger et al. (2012b) investigated silk glands in Crassicorophium bonellii and Lembos websteri Bate, 1857 and found that the proximal gland group presents rosette glands, while the distal group presents lobed glands. Thus, the structure of amphipod silk glands varies in different species but has never been studied in mast-building amphipods.

The vast majority of builder amphipods construct tubes and burrows, whereas mast building has only been described in four species of the corophiid family Dulichiidae and has not been observed in other crustaceans (McCloskey, 1970; Moore and Earll, 1985; Mattson and Cedhagen, 1989; Zhadan et al., 2007; Moore and Eastman, 2015). Dyopedos bispinis is a polar amphipod that has been detected in several arctic seas, both Eurasian and American, and in the eastern Pacific (Laubitz, 1977). Abundant Dyopedos bispinis masts were recently detected in the Velikaya Salma Strait (White Sea) (Zhadan et al, 2007), but nothing is known regarding the biology and mast-building activity of this species.