Social behaviour and mast-building in Dyopedos bispinisnext section
Social structure on masts
Dyopedos bispinis masts are typically inhabited by no more than one adult female and no more than one adult male, indicating that the territorial behaviour of Dyopedos bispinis is similar to that of other Dyopedos species (Mattson and Cedhagen, 1989; Thiel, 1997). Each large mast of Dyopedos monacantha or Dyopedos porrectus is a territory belonging to a single adult female. Only one male can enter, and female descendants can remain for some time on the maternal mast.
Adult male Dyopedos bispinis are occasionally observed on individual masts, but it is unknown whether these males, such as those of Dyopedos porrectus (Mattson and Cedhagen, 1989), can construct their own masts or whether, similar to male Dyopedos monacantha, they use abandoned masts, which are numerous in sea bottom landscapes.
Extended maternal care has been reported in some dulichiid species (McCloskey, 1970; Mattson and Cedhagen, 1989; Thiel 1997). Apparently, Dyopedos bispinis is no exception as numerous juveniles have been observed together with adult females on large masts.
In addition to the masts of Dyopedos bispinis being typical of species from the genus Dyopedos, in that they are usually inhabited by a single female, masts with two and more adult, and sometimes even ovigerous, females were observed. Mattson and Cedhagen (1989) reported Dyopedos monacantha masts with one large male and two smaller females (although not two large females), and McCloskey (1970) also observed masts with three nonbreeding adult Dulichia rhabdoplastis. However, among other building corophiids, the coexistence of several adult females in one dwelling is unknown (Thiel, 2007; Moore and Eastman, 2015). However, some leucothoid amphipods (Thiel, 2000) and other symbiotic malacostraca (Duffy 2002, 2007) have been described inhabiting the inner canals of sponges. The corophiid tube has only one or two openings for outside feeding and only a single place for intratubular filtration (Dixon and Moore, 1997). In contrast, if the mast is long enough, then multiple individuals could probably feed without hindering each other because Dyopedos spp. utilize the water current perpendicular to the mast axis for feeding (Mattson and Cedhagen, 1989). However, it is not clear why collective Dyopedos masts are not widespread. Some possible explanations include mechanical factors (current, waves, substrate quality) or fish-predation pressure, as reported for Dyopedos monacantha, (Mattson and Cedhagen, 1989) which could, in theory, increase with mast elongation.
It is also unknown whether the adult amphipods inhabiting one mast are relatives (is it a parent-offspring or conspecific association? See Thiel, 2011) and whether these crustaceans defend the mast from interspecific competitors. Most likely, these congested masts reflect the development of extended parental care, which has been described in Dyopedos spp. (Mattson and Cedhagen, 1989; Thiel, 1997). However, increasing levels of interspecific aggression typically force juveniles to leave the maternal mast (Mattson and Cedhagen, 1989), and the number of juveniles on the mast rapidly declines with growth (Thiel, 1997). It is possible that a certain aggression suppression mechanism could be involved that would allow the brood to remain on the mast. It is also unknown whether the mother of the brood remains on the mast and, consequently, whether adult amphipods from different generations can coexist on the mast. Parent-offspring groups, iteroparity and the coexistence of several offspring cohorts were observed in many percarids (Thiel, 2007), but overlapping generations (offspring that begin to reproduce in the presence of reproductive parents) and coexisting reproducing adult offspring in the maternal dwelling has not been reported (Thiel, 2007; Thiel, 2011). Although much remains to be discovered, Dyopedos bispinis exhibits the movement from a typical corophiid small parent-offspring group to more complex groups with different social structures.
Cooperative mast building
“Collective” masts are typically much longer than individual masts, likely reflecting cooperative mast maintenance. Indeed, all adults have pereopod glands, so it is difficult to identify a single builder. However, “individual” masts might also be considered a product of cooperative building; for example, Dyopedos monacantha males share the maintenance of female masts, using pereopods 3-4 (Mattson and Cedhagen, 1989). Dyopedos bispinis males have developed pereopod glands, and it is quite likely that they also use these structures. Moreover, these glands are developed in the youngest Dyopedos bispinis juveniles. Silk threads of different diameters are found on the mast surface, which could also be viewed as a result of cooperative building (for more detail, see Discussion section 4.1. on “nonpereopodal secretions”). Juveniles of Dyopedos monacantha leave the maternal mast to build their own masts at different ages (Thiel, 1997), suggesting that there is a time period in which young amphipods are capable of building but inhabit the maternal mast. Thus, although we do not have direct evidence that juveniles participate in maternal mast maintenance, we suggest that, in some cases, juveniles begin to strengthen (build up) and elongate the maternal mast instead of leaving it, leading to the appearance of collective masts.
Ecological aspects of mast-building in Dyopedos bispinis
Habitats of Dyopedos bispinis
Dyopedos bispinis is abundant in conditions with strong currents; their masts are rarely observed on mud but are often on hydroids. Thus, Dyopedos bispinis habitats are more similar to those of Dyopedos porrectus than Dyopedos monacanthus (Moore and Earll, 1985; Mattson and Cedhagen, 1989). Although Dyopedos porrectus was also detected in Velikaya Salma Strait, it was absent in the biotopes studied in this paper; thus, further investigations are required.
Mast-building and foreign organisms
The masts of different dulichiids were observed on hydroids (Dyopedos porrectus, Moore and Earll, 1985), sea urchin spines (Dulichia rhabdoplastis, McCloskey, 1970), shells, polychaete tubes (Dyopedos monacantha, Mattson and Cedhagen, 1989), and amphipod tubes (Dulichia falcata (Bate, 1857), Kanneworff and Nicolaisen, 1972). Dyopedos porrectus has also been associated with bryozoans (Lincoln, 1979, cit. ex. Moore and Earll, 1985). Dyopedos bispinis, although not observed on sea urchins, uses a wide range of organisms as substrata including hydroids, bryozoans, sponges, molluscs, brachiopods and Crassicorophium tubes. Importantly, mast building on hydroids can be easily underestimated because the hydroid can be fully disguised as a part of the mast. Hydroids and bryozoans often occur immured, and it is likely that the building activity of Dyopedos bispinis negatively affects substratum organisms. Because Dyopedos bispinis is a dominant species in the Velikaya Salma Strait (Zhadan et al., 2007), the influence of masts on the benthic ecosystem might be significant.
McCloskey (1970) reported that numerous diatoms cover the surfaces of the masts of Dulichia rhaboplastis, but diatoms are usually only sparsely present on masts of other Dulichiidae (Moore and Earll, 1985; Mattson and Cedhagen, 1989). Additionally, Dyopedos bispinis masts do not have abundant diatom epiflora. Nevertheless, diatoms are abundant in the detritus used to form masts (Fig. 3D-G), and some of pelagic forms likely remain alive for some time because they have mucous pads (arrowheads, Fig. 3E). It is not known whether this is a frequent occurrence or how long these forms survive, but these “former pelagic” algae likely require further attention in the descriptions of community structure.
Mast building by Dyopedos bispinis on hydroids occasionally leads to the appearance of branching masts (Fig. 2D), and this phenomenon is unknown in other dulichiids. Dyopedos bispinis are apparently territorial, and it remains unknown how these organisms share areas of conflict on the branching masts. Masts with several supports (Fig. 2A-B) have also not been previously described, and whether each individual builds additional masts or utilizes abandoned masts remains unknown.
Internal structure and growth of the masts
The mast of Dyopedos bispinis comprises a homogeneous central cylinder and a laminated cortex (Fig. 1A-D and Fig. 3A-B), and the mast surface is covered with a silk sheath (Fig. 1F and Fig. 4), confirming the observation of Mattson and Cedhagen (1989), who reported that mast construction begins with the formation of the detrital central region and continues through the production of silk layers. However, in addition to silk, the laminated cortex includes a large amount of detritus (Fig. 1C-D and Fig. 3A-B), and it is likely that detritus layers alternate with silk layers (Fig. 1F). Moreover, the thickness of the cortex is occasionally comparable to the radius of the central cylinder (Fig. 1C-D).
Thus, we propose that there are different methods for developing the mast for different purposes: (A) mast reinforcement with only silk threads (described by Mattson and Cedhagen (1989)) and (B) mast thickening with detritus and silk. It remains unknown whether thickening is realized by active amphipod activities or by passive detritus settlement and gluing.
Detritus for mast building and maintenance can likely be collected from both the water column and from the bottom because both planktonic and benthic diatoms are present in the mast (bda, pda, Tn in Fig. 3E-G). Both methods were described for Dyopedos monacantha (Mattson and Cedhagen, 1989).
Mast thickening is likely necessary as mast size increases with amphipod growth. The design of the mast facilitates growth without structural disturbance. In contrast, tube-building amphipods, according to the observed data, occasionally (a) leave old dwellings and build new, more spacious tubes, (b) stretch existing tubes, and (c) break old tubes into pieces and build new tubes utilizing these pieces during body growth (Goodhart, 1939; Barnard et al., 1988). Thus, gradual build up is at least occasionally not an option for tube-building amphipods, unlike mast builders.
The surface of a Dyopedos bispinis mast is covered with silk threads that are oriented in various directions and in many layers (Fig. 3E, and Fig. 4A-D). For Dyopedos monacantha, it was observed that under conditions with strong currents, the silk threads are placed at different angles to increase mechanical strength. We collected Dyopedos bispinis masts from straits with strong tidal currents, and there was no prevailing silk direction in these conditions.
When covering the mast with silk, each Dyopedos monacantha pereopod 3-4 tip moves back and forth “along an ample half of the circumference of the mast” (Mattson and Cedhagen, 1989), and this spinning procedure gradually proceeds along the mast (Mattson and Cedhagen, 1989). In Dyopedos bispinis, regular parallel thread deposition was sometimes observed, and remarkably, a nearly rectangular, meshy structure was occasionally observed (Fig. 4B-C). A similar structure was identified by Moore and Earll (1985) in SEM photos of Dyopedos porrectus masts, and according to these authors, “the resultant meshwork is reminiscent of geodetic construction of aircraft fuselages and would confer relative strength together with flexibility”. Similar silk structures were also observed in tube-building species, such as Crassicorophium bonellii and Peramphithoe femorata (Cerda et al., 2010; Kronenberger et al., 2012a).
Silk and mucus production in tube- and mast-building species
The amphipod silk produced by pereopods 3-4 is a very important component of tubes and masts. However, in some cases, additional secretions produced by other appendages are exploited for mast or tube building (Mattson and Cedhagen, 1989; Goodhart, 1939), and these secretions are likely presented as glues. Their importance may be underestimated, especially as mouthparts and gnathopods are very often involved in material collection (Skutch, 1926; Meadows and Reid, 1966; Dixon and Moore, 1997). However, at least in Crassicorophium bonellii and Lembos websteri, the pereopodal silk also includes a mucopolysaccharide adhesive component (Kronenberger et al, 2012a,b). It remains unclear how widespread is the use of additional secretions among tube- and mast-building corophiids.
The tip of one of the examined masts was covered with threads (Fig. 4A) that were thinner than those in the remaining mast surface (Fig. 4B-C). They could be considered mucus threads, but according Mattson and Cedhagen, 1989, the mucus threads of Dyopedos monacantha are more than 10 times thicker than silk threads, and the mouthpart origin of the thin threads is doubtful. Because pereopods 3 and 4 are practically identical and likely to produce threads with similar diameters, we can offer two hypothesizes: threads of different diameters reflect (A) changes in thread diameter (for example, depending on the tension) or (B) shared building activity between several amphipods of different size. We did not detect threads with changing diameters, which supports the second hypothesis.
The mast SEM photos (Fig. 3E-G, and Fig. 4A-D) showed various detritus and silk threads, but we did not observe anything that could be accurately interpreted as cement or glue (amorphous mucus). We proposed that the mucus quantity is not great or that it is washed out during experimental fixation and treatment procedures. However, the fixed masts maintained such characteristics as form and flexibility. Therefore, one possibility is that mucus is important during the first stages of mast building, but silk threads subsequently provide the strength.
Pereopod glandular complex composition
Compositions of the pereopod 3-4 glandular complex are similar in Dyopedos bispinis and tube-building species. All studied corophiid species have two gland groups, proximal and distal, a common cuticular chamber and a single excretory opening (Nebeski, 1880; Kronenberger et al; 2012b; Neretin, 2016, and Fig. 5A). Dyopedos bispinis proximal glands (D1) are multicellular and have a strongly elongated form (i.e., “pseudotubular” glands, see discussion below in sections 5.4-5.6 and Fig. 9D-H), as has been observed in most other corophiid species (Nebeski, 1880; Neretin, 2016), likely with the exception of Crassicorophium bonellii and Lembos websteri (Kronenberger et al., 2012b). It is not clear whether the distal glands (D2) or Dyopedos bispinis are multicellular like the proximal glands (D1) or whether each D2 secretory cell has an individual duct. Both variants have been identified in other amphipods: multicellular distal glands in Ampithoe spp. (Nebeski, 1880; Neretin, 2016) and glands including a single secretory cell in J. falcata (Nebeski, 1880).
According to Kronenberger et al. (2012b), the Crassicorophium bonellii and Lembos websteri glandular complexes comprise both rosette (as in Fig. 9C) and lobed glands. According to our findings, Dyopedos bispinis and Ampithoe rubricata glands are not typical rosette or lobed but have some common features with both these gland types (facultative binuclearity, presence of deep cell membrane invaginations and cellular composition, see discussion section 5 and Fig. 9). Considering that another species of Crassicorophium (Crassicorophium crassicorne) has elongated glands typical of other amphipods (Nebeski, 1880), these differences most likely reflect differences in terminology. On the other hand, the schematics by Kronenberger et al., (2012b) show typical rosette glands. Thus, it remains in question whether the structure of the pereopodal glands of Crassicorophium bonellii and Lembos websteri is unique among other corophiids.
Fig. 9. Comparative schematic drawings of Dyopedos bispinis proximal glands (D1) and other crustacean tegumental glands. A, B and C – several types of crustacean tegumental glands modified from Talbot and Demers, 1993 and Rieder, 1977: A – bicellular glands, B – tricellular glands, C – rosette glands; D, E and F – pseudotubular silk glands of Amphipoda: D – A. rubricata (after Neretin, 2016), E – J. falcata (modified from Nebeski, 1880), F – Dyopedos bispinis; G and H – tube-building glands of the tanaid H. oerstedii (Kroyer 1842) (after Blanc, 1884), also likely pseudotubular; I – cirripedian cement glands (modified from Lacombe and Liguori, 1969). Abbreviations: as – accumulation site; c – cuticle; CC – central cell; DC – duct cell; hyp – hypoderm; IC – intermediary cell; LD – lateral duct; MD – main duct; nu, nu1 and nu2 – nucleuses of secretory cells; SC – secretory cell; ySC – young secretory cells.
Volume of pereopodal glandular complex
Although the Dyopedos bispinis masts are large structures compared with the length of the amphipod body, we have not observed Dyopedos bispinis glands to be strongly enlarged compared with tube-building species. The number of secretory cells (approximately 70 in each Dyopedos bispinis pereopod, Fig. 5B, 8A) is lower than in other species (about 130 in Crassicorophium bonellii, based on figures in Kronenberger et al., 2012b, and more than 400 in Ampithoe rubricata, N. Neretin, unpublished data), and the cell size is also minimal in Dyopedos bispinis. These facts might reflect small body size of the White Sea Dyopedos bispinis compared with other studied amphipods.
The secretory granule ultrastructure is similar in the studied species (Dyopedos bispinis, Ampithoe rubricata, and Crassicorophium bonellii, Kronenberger et al., 2012b; Neretin, 2016); granules of proximal gland groups are electron dense and have a normal, round shape (Fig. 6D, H, and Fig. 7C-D), unlike distal group granules (Fig. 8B-E).
The distal glands of Dyopedos bispinis may produce several different substances because D2 secretory cells contain different types of granules (Fig. 8D). Two morphologically different types of granules are presented in Ampithoe rubricata distal glands (Neretin, 2016), and only uniform granules are found in Crassicorophium bonellii distal glands (Kronenberger et al., 2012b).
Secretion for tube and mast building summary
In general, we did not detect any crucial differences in the glandular complex structure and forms of secretions in tube-building species and the mast-builder Dyopedos bispinis. The variability in the dwellings most likely reflects behavioural adaptations.
Morphology of amphipod silk glands compared with other crustacean glands
Secretory cell nucleus quantity
Dyopedos bispinis D1 and D2 secretory cells are uninucleate (Fig. 6A), as are the silk glands of the majority of other amphipod species (Jassa falcata, Jassa ocia (Bate, 1862), Crassicorophium crassicorne (Bruzelius, 1859), Ericthonius punctatus (Bate, 1857), and Ampithoe ramondi Audouin, 1826) (Nebeski, 1880)). However, in Ampithoe rubricata glands, binuclear secretory cells have also been observed together with uninucleate cells (Neretin, 2016). The basis glands in the pereopods of Crassicorophium bonellii are also binuclear according to the drawing by Kronenberger et al. (2012b).
Binuclearity is typically regarded as a prominent feature of lobed glands (Talbot and Demers, 1993) and is occasionally used as a diagnostic character (Kakui and Hiruta, 2014). However, the secretory cells in lobed glands contain one or two nucleuses, apparently independent of cell size (Gorvett, 1951). Furthermore, it was recently shown that binuclear cells, together with uninuclear cells, occur in isopod rosette glands (Vittori et al., 2012). Thus, variations in nuclear number are present in different types of crustacean tegumental glands but are currently only described within Percarida (Isopoda, Tanaidacea, Amphipoda) and not in Decapoda. It is likely that similar variations also occur in Mystacocarida (Elofsson and Hessler, 2005).
In Dyopedos bispinis, the proximal silk glands (D1) are covered with a lining layer (Fig. 6C, E and Fig. 7). We cannot unambiguously determine whether the lining is a part of the duct cell or an independent structure. Thus, we can only hypothesize as to its origin.
The presence of nuclei favours the independence of the lining cell from other gland cells (duct and secretory). The cellular layer covering the glands, which is classified as connective tissue, has been described in many crustaceans: decapod (Yong, 1932; Pugh, 1962) and isopod (Ide, 1891; Gorvett, 1946) rosette glands, cirripedian cement glands (Lacombe and Liguory, 1969), amphipod Ampithoe rubricata silk glands (Neretin, 2016) and isopod lobed glands (Ide, 1891; Gorvett, 1951), but the fallacy of this interpretation for lobed glands was observed in a study by Weirich and Ziegler (1997).
The lining could also represent a system of branching extensions of the duct (or intermediate) cell, and such systems have been described for intermediate cells in lobed (tricellular, Weirich and Ziegler, 1997) and rosette (Vittori et al., 2012) glands of isopods. In Dyopedos bispinis, this hypothesis is supported by the fact that, in some places, the lining comprises numerous cytoplasmic extensions (arrowheads, Fig. 7E) that deeply penetrate secretory cell invaginations (i, Fig. 7A-D), as in lobed glands. However, branches of intermediate cells in the isopod glands serve to collect secretions on the basal surface of secretory cells (Weirich and Ziegler, 1997). In contrast, the D1 gland cell secretion is excreted through the apical cell membrane, as evidenced by the presence of a definitely visible accumulation site (as, Fig. 6).
The lining might be considered an enlarged sheath cell, thus sharing a common origin with the duct cell. Sheath cells are typically observed in arthropod sensilla and at some stages of insect dermal gland development (Quennedey, 1998; Merritt, 2006).
The lining might also be a complex structure; for example, nervous terminations are likely located in this region as previously assumed for isopod lobed glands (Wägele, 1992). To understand the nature of the lining, more detailed electron microscopy investigations are required.
The observation of an axon-like structure (Fig. 6F) in contact with the secretory cell likely indicates the presence of nervous control of amphipod silk glands. Gland innervation has been demonstrated in the branchial rosette glands of the decapod Palaemonetes pugio Holthuis, 1949 (Doughtie and Rao, 1982), in the labrum glands of the cladoceran Daphnia obtusa Kurz, 1874 emend Scourfield, 1942 (Zeni and Zaffagnini, 1988), in cirripedian cypris larva glands (Okano et al., 1996), and in mystacocarid tegumental glands (Elofsson and Hessler, 2005). However, crustacean tegumental glands are not typically innervated (Talbot and Demers, 1993). For amphipod silk glands, innervation was shown for the first time in the present study.
Cellular composition of Dyopedos bispinis proximal amphipod silk glands
Each proximal gland (D1) contains some (up to 17) secretory cells and one duct cell with an intracellular duct. Insect glands contain duct cells with an intercellular duct, which are referred to as class 3 glands (Noirot and Quennedey, 1974) or dermal glands, in contrast with unicellular and tubular glands (Merritt, 2006). In contrast to typical insect class 3 glands (Noirot and Quennedey, 1974; Quennedy, 1998), the secretory cells of the D1 glands do not have microvilli in the ductule lumen. D1 duct cells also do not have a mesaxon, which is the cross connection between the inner and outer duct cell membranes and has been described in many insect and crustacean dermal glands (Lai-Fook, 1970; Martens, 1979; Lawrence and Staddon, 1975; Doughtie and Rao, 1982; Elofsson and Hessler, 1998; Lombardo et al., 2006; Vittori et al., 2012).
Dermal glands are common in Arthropoda and contain one to two consecutive duct cells and one or several secretory cells (Quennedy, 1998; Coons and Alberti, 1999; Hilken et al., 2005; Pekár and Šobotník, 2007, Müller et al., 2014). The dermal glands of the Crustacea contain one to two secretory cells, which are referred to as bicellular (Fig. 9A) or tricellular (Fig. 9B) depending on the quantity of duct cells (Talbot and Demers, 1993, Elofsson and Hessler, 1998; Zeni and Stagni, 2000). In Malacostraca, rosette dermal glands (Fig. 9C) are also widely distributed, and each are composed of two duct cells (in the narrow sense, duct and intermediate) and multiple (up to 40-50) secretory cells (Talbot and Demers, 1993).
The proximal silk glands (D1) of Dyopedos bispinis (Fig. 6 and Fig. 9F) contain some secretory cells and appear similar to rosette glands, but D1 glands, at least at first glance, have two significant differences. First, we have observed only one (not two) duct cell in each gland. Glands comprising single duct cells and several secretory cells have been described in Crustacea (Claus, 1879; Ide, 1891; Gorvett, 1946; Pugh, 1962), but there are no electron microscopy studies confirming this “bicellular” scheme. Thus, we propose that the boundary between the duct and intermedium cell might be difficult to detect on semi-thin sections and might not be captured on ultrathin sections due to the significant length of the duct (up to 2 mm).
Second, D1 glands markedly differ in shape from typical rosette glands. Rosette glands are typically globular; ductules from secretory cells coalesce at approximately one point (Johnson and Talbot, 1987; Alexander, 1989; Talbot and Demers, 1993, Fig. 9C). In contrast, D1 glands are strongly elongated, and ducts from secretory cells fall individually and sequentially into the main duct. However, occasionally, rosette glands might also be slightly elongated (Ide, 1891; Pugh, 1962) or even have practically tubular forms (recently described terrestrial hermit crab Coenobita spp. antennal glands, Tuchina et al., 2014). Dyopedos bispinis D1 glands even have more elongated, almost cord-like forms (Fig. 5B, 9F), and such gland morphology has not been incorporated into the Talbot and Demers (1993) classification of crustacean tegument glands. If typical rosette glands are similar to the typical acinar glands of metazoans (Ide, 1891), then Dyopedos bispinis D1 glands resemble rather tubular glands. We propose that such glands can be called pseudotubular.
Comparison with other arthropod silk glands
Glands similar in shape to D1 have been described within silk-producing systems in other corophiid amphipod species (Fig. 9D-E) (Nebeski, 1880; Neretin, 2016) and in the tanaid Heterotanais oerstedii (Krøyer, 1842) (Fig. 9G-H) (Blanc, 1884), all of which might be defined as pseudotubular. Building glands in other crustaceans suggest another structure; the amphipods Crassicorophium bonellii and Lembos websteri and the tanaid Phoxokalliapseudes tomiokaensis (Shiino, 1966) have lobed and typical rosette glands (Kronenberger et al., 2012b, Kakui and Hiruta, 2014), while callianassid shrimps (Decapoda) have only typical rosette glands (Dworschak, 1998). Cirripedian cement glands are multicellular but do not possess special duct cells (Lacombe and Liguori, 1969) and might be considered tubular gland variations (class 1 glands, according to the Noirot and Quennedey classification, 1974).
Silkworms and spiders, the most famous silk-producers, have classical tubular glands (Sehnal and Akai, 1990), but there is some evidence of homology between spider ampullate silk glands and sensilla (Hilbrant and Damen, 2015). In insects, dermal glands are homologous to sensilla (Quennedey, 1998; Merritt, 2006), and it can be assumed that spider silk glands passed through the dermal gland stage during evolutionary development. Futhermore, there is an assumption, that insect labial silk glands originate from dermal glands, but it is questionable (Kenchington, 1969; Sutherland et al., 2010).
Dermal (class 3) silk glands are common among insects (Sutherland et al., 2010); these glands are bicellular or tricellular (according to “crustacean” terminology) and typically numerous. However, multicellular dermal silk glands are unknown in insects (although secretory cells can be multinucleated, Nagashima et al., 1991). Thus, the pseudotubular silk glands of amphipods and, likely, tanaids are probably unique among arthropod silk glands as these structures are tubular in shape, although indeed dermal.
Pseudotubular gland origin
We propose that the pseudotubular glands of Dyopedos bispinis could originate from increasing secretion in conjunction with space limitations in narrow appendages. Multicellular gland enlargement could occur at the expense of elongation and growth towards the proximal part of the appendage. In the hermit crab, Coenobita spp., elongated antennal glands also probably appeared as a result of a great increase in secretion production volume (Tuchina et al., 2014).
Coenobita spp. antennal glands likely appear as modified rosette glands (Tuchina et al., 2014). Dyopedos bispinis D1 glands could also have evolved from typical rosette glands, particularly as these glands have been observed in amphipods (Schmitz, 1967, 1992).