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Myoanatomy of the Lophophore in Adult Phoronids and the Evolution of the Phoronid Lophophore.

Introduction

Adult phoronids are benthic animals that inhabit soft or hard substrata. The main, elongated part of the phoronid body is embedded in the substratum, whereas the anterior part protrudes from the substratum and bears a lophophore with tentacles. The protruding lophophore has many functions, including food capture, respiration, perception of stimuli, and brooding (Emig, 1976, 1982; Temereva and Malakhov, 2010). Among phoronids, there are several main types of lophophore morphology and several transitional states (Emig, 1979; Temereva and Malakhov, 2009). These lophophore types differ in shape and number of tentacles. In terms of general morphology, the oval lophophore is the simplest and bears about 24-30 tentacles, whereas horseshoe-shaped and spiral lophophores are more complex and bear 100-1500 tentacles. The most complicated lophophore is the helicoidal type.

Some researchers inferred that lophophore type depends on body size (Pixell, 1912; Emig, 1976, 1982; see Fig. 1). The smallest phoronid, Phoronis ovalis, has an oval lophophore, and the largest, Phoronopsis californica, has a helicoidal lophophore. The phoronid lophophore is thought to have evolved from the simplest type, that is, the oval lophophore, to the horseshoe and spiral types, and then to the helicoidal type (Emig, 1976). This opinion is supported by phoronid ontogeny: in all phoronids, newly formed juveniles have an oval lophophore. Moreover, tiny Phoronis ovalis is traditionally regarded as the basal species in the Phoronida (Santagata and Cohen, 2009); its oval lophophore therefore seems to be a plesiomorphic feature for all phoronids. This view has been presented in several previous papers (Emig, 1979, 1982) and is supported by Kuzmina and Temereva (2019).

That lophophore type depends on body size, however, has not been supported by other recent studies. Temereva (2017c), for example, reported that lophophore morphology is simpler in large phoronids than in small phoronids. Moreover, the recently discovered species Phoronis embryolabi is smaller than P. ovalis, but it has a horseshoe-shaped lophophore (Temereva and Chichvarkhin, 2017). These results clearly demonstrate that the type of lophophore does not necessarily depend on body size.

The Lophophorata (which includes phoronids, bryozoans, and brachiopods) have been traditionally thought to be closely related because they all have lophophores and are generally similar in morphology (Emig, 1976). This view has been supported by several recent reports. A study of the myoanatomy of the lophophore in P. ovalis, for example, revealed some homologous elements in phoronids and bryozoans (Temereva, 2019). Similarities were also discovered in the neuroanatomy of the lophophore of P. ovalis and bryozoans (Temereva, 2017a). Although other recent morphological studies also support the monophyly of the lophophorates (Temereva and Tsitrin, 2015; Temereva and Kosevich, 2016, 2018a; Temereva, 2017b). similarities in morphology may result from similarities in life style in the absence of close genetic relationships.

The results of some molecular studies have been consistent with the traditional view that the lophophorates are a monophyletic group consisting of three phyla: Phoronida, Brachiopoda, and Bryozoa (Jang and Hwang, 2009; Nesnidal et al., 2013; Laumer et al., 2015; Marletaz et al., 2018; Fig. 2A). The results of other molecular studies, however, have been inconsistent with such monophyly and have indicated that phoronids and brachiopods are united in a group called the Brachiozoa, whereas bryozoans form a separate clade that is very distant from the Brachiozoa (Dunn et al., 2008; Hejnol et al., 2009; Kocot et al., 2017). Despite incongruence of bryozoan phylogenetic positions in some molecular phylogenies, monophyly of Lophophorata has been supported by a recent genomic study using only high-quality transcriptomes and genomes (Luo et al., 2018). The position of bryozoans is affected by the sampling quality and the evolutionary rates of selected genes; slowly evolving genes support bryozoans as a sister group to phoronids. Zverkov and coauthors (2019) have shown that the monophyly of Lophophorata depends on the tree searching algorithm and substitution model used, and they generally support the sister relation of Phoronida and Bryozoa.

Phoronid phylogeny is still poorly resolved and requires additional morphological and molecular data from both larvae and adults (Hirose et al., 2014; Temereva et al., 2016; Temereva and Neklyudov, 2018). According to the current view of phoronid taxonomy, P. ovalis is always regarded as a sister group to the rest of the phoronids; the genus Phoronis is paraphyletic and includes clades of burrowing phoronids and phoronids that live in soft substrata; and the genus Phoronopsis is monophyletic (Fig. 2B).

The current study had the following three objectives: (1) to describe and compare the lophophore myoanatomy of three phoronids that differ in lophophore morphology (Phoronis ijimai, Phoronis australis, and Phoronopsis harmeri); (2) to compare the lophophore myoanatomy of the three phoronids with that of Phoronis ovalis (the only other phoronid for which lophophore myoanatomy has been previously described in detail); and (3) to consider how this new information increases our understanding of phoronid evolution and relates to the problem of the monophyly versus the polyphyly of the lophophorates.

Materials and Methods

Animals

About 50 adult specimens of Phoronis ijimai Oka, 1897 were collected in May 2016 in Olga Bay, Sea of Japan. The animals were embedded in the shells of Crassostrea gigas, which were found at three- to four-meter depth. These specimens were fixed and used for histological and other studies as described below. Adults of the same species were collected on the shore of Bering Island in August of 2014; these live adults were embedded in pieces of mollusc shells and were photographed by Sergey Gorin (Moscow State University), who used a Nikon D7000 camera with a Tamron (Commack, NY) 60-mm f/2.0 lens (exposure 1/200 s; diaphragm F 11, ISO 100).

Adults and juveniles of Phoronis australis Haswell, 1883 were collected in May 2013 from the tubes of species of Cerianthus in Nha-Trang Bay, South China Sea, Vietnam. Live animals were photographed with a Panasonic DMC-TZ10 digital camera on an Olympus CX22 light microscope. Because the lophophore of P. australis is very large, it is difficult to study in whole by confocal laser scanning microscopy. We therefore studied by confocal laser scanning microscopy the juvenile lophophore, which is changing into the spiral type. About 20 juveniles were extracted from tubes and then fixed and used for histological and other studies as described in the following two subsections.

Adults of Phoronopsis harmeri Pixell, 1912 were collected in July 2015 in Vostok Bay, Sea of Japan. About 60 specimens were fixed and used for histological and other studies as described below. A dense population of P. harmeri was discovered in Amursky Bay, Sea of Japan, in April 2015 by Anton Chichvarkhin (Institute of Marine Biology), who photographed the live animals with a Nikon D810 camera and a Nikkor 110/2.8 lens.

Histology and scanning electron microscopy (SEM)

For histology, lophophores of adult Phoronis ijimai, P. australis, and Phoronopsis harmeri were cut from the body and fixed in a 4% paraformaldehyde solution in filtered seawater for 48 hours at 4 [degrees]C; the fixed specimens were then washed in distilled water for 8 hours and dehydrated in solutions with increasing ethanol concentrations (up to 95%) and then in xylol. The specimens were then embedded in paraplast and cut serially to yield 5-[micro]m-thick sections. The sections were placed on glass microscope slides, stained with hematoxylin, embedded in Canada balsam, and covered with coverslips. The sections were observed with a Zeiss (Oberkochen, Germany) Axioplan2 microscope and photographed with an AxioCam HRm camera.

For SEM, lophophores of adult Phoronis ijimai, P. australis, and Phoronopsis harmeri were fixed as described above, dehydrated in ethanol followed by an acetone series, and critical-point dried. Dried lophophores were mounted on stabs, sputter-coated with platinum-palladium alloy, and examined with a Camscan S2 Scan scanning electron microscope (Camscan Electron Optics, London).

Cytochemistry and confocal laser scanning microscopy (CLSM)

Lophophores of Phoronis ijimai adults, P. australis juveniles, and Phoronopsis harmeri adults were fixed in a 4% paraformaldehyde solution in phosphate buffer (pH 7.4) (Fisher Scientific, Pittsburgh, PA) for 8 hours at 4 [degrees]C and then washed 3 times (30 minutes each time) in phosphate buffer with Triton X-100 (1%; PBT; Fisher Scientific). For F-actin staining, specimens were placed in a 1:30 dilution of AlexaFluor 488 phalloidin (Molecular Probes, Eugene, OR) in PBT for 4 hours at room temperature. The specimens were then washed three times in phosphate buffer, washed for several minutes in isopropanol of increasing concentrations, and embedded in Murray Clear (a mixture of benzyl benzoate and benzyl alcohol). Specimens were observed with a Nikon Eclipse Ti confocal microscope (ThermoFisher Scientific, Waltham, MA).

Image processing

Z-projections were prepared using ImageJ software (Schneider et al., 2012). Volume renderings were prepared with Amira version 5.2.2 software (Thermo Fisher Scientific, Waltham, MA). Images were processed in Adobe Photoshop CS3 (San Jose, CA); images were edited with crop, level, copy, and paste tools.

Results

Morphology of the lophophore

The lophophore is the apical part of the phoronid body. The lophophore of Phoronis ijimai protrudes only slightly from the hard substratum (Fig. 3A), whereas the lophophore and a long portion of the trunk of Phoronopsis harmed protrude from the hard substratum (Fig. 3C). The phoronid lophophore is separated from the trunk by the diaphragm, which is visible in live animals (Fig. 3B). The phoronid lophophore has a base that bears the tentacles. The base of the phoronid lophophore can be divided into two parts: the proximal (the base proper) and the distal (the tentacular lamina) (Fig. 3E, F). The base proper contains two lophophoral blood vessels, which are evident in live animals (Fig. 3D-F). In the tentacular lamina, the bases of all tentacles are fused to each other (Fig. 4A-C). In all studied species, a narrow furrow separates the distal and proximal parts of the lophophore base (Fig. 4A, B). In P. harmeri, the base proper is partly covered by the collar, which is an epidermal fold that extends around the lophophore (Fig. 4A). In all phoronids, tentacles surround the mouth and are arranged in one row that bends inward on the anal side, where the row of tentacles forms a coil in P. harmeri or several coils in Phoronis australis adults. Because the mouth and anus are located near each other in all phoronids, the lophophore of all phoronids has an oral side and an anal side. Thus, there are inner (or anal) and outer (or oral) tentacles. In all phoronids, the row of tentacles is interrupted on the anal side where the young tentacles arise (Fig. 5A-C). The lophophore is bilaterally symmetrical: two arms of tentacles are located on the left and right sides of the anus (Figs. 4A, 5). The epistome is an epidermal fold that covers the mouth from the anal side (Figs. 3E, 5A-C).

Several ciliated zones extend along each tentacle in all three species (Fig. 4D). The frontal zone faces the mouth and is covered by many cilia. Cilia density is maximal in the two lateral zones. The abfrontal zone is opposite the frontal zone and is covered by only a few cilia (Fig. 4D).

The lophophore is bilaterally symmetrical and consists of two halves (left and right arms) (Fig. 5). The lophophore is horseshoe shaped in P. ijimai adults (Fig. 5A), is changing to the spiral type in P. australis juveniles and forms a spiral with three coils in P. australis adults (Fig. 5B), and forms a spiral with one coil in Phoronopsis harmeri adults (Fig. 5C).

Myoanatomy of the lophophore of Phoronis ijimai

The musculature of the P. ijimai lophophore has four main groups: muscles of the base proper, of the tentacular lamina, of the tentacles, and of the epistome.

The circular muscle (cm; circular muscle of the lophophore base) is the main muscle of the lophophore base (Fig. 6A). The circular muscle extends around the lophophore base and repeats the shape of the lophophore: it bends inward on the anal side and extends along left and right arms of the lophophore (Fig. 6B). On the oral side of the lophophore, the circular muscle is connected to the truncal musculature via groups of longitudinal muscles (lib, longitudinal muscles of the lophophore base), each of which consists of three to five thick muscles that branch into many thin bundles. On the anal side of the lophophore, numerous short longitudinal muscles (lib) connect the lophophore base and the circular muscle of the lophophore (cm), forming two arms (left and right) on the anal side (Fig. 7A, B). Above the circular muscle (cm), many groups of short muscles extend in different directions (Fig. 6F).

The tentacular lamina has several groups of muscles that are associated with the bases of the tentacles. The first group consists of thick longitudinal muscles of the tentacular lamina (ltl). These muscles start from the circular muscle and extend along the base of each tentacle (Fig. 6D, E). Each longitudinal muscle starts as many thin muscle projections, which then fuse and form a thick muscular bundle (Fig. 6C, H). The second group of muscles of the tentacular lamina is formed by paired feather-like muscles that are associated with the longitudinal muscular bundles and are located at the distal end of the tentacular lamina; these are groups of paired distal muscles of the tentacular lamina (pdm) (Fig. 5G). Groups of paired distal muscles of the tentacular lamina (pdm) are located on the left and right sides of each longitudinal muscle of the tentacular lamina, and they extend parallel to the longitudinal muscle of the tentacular lamina. At the distal end of the tentacular lamina, the longitudinal muscle of the tentacular lamina and groups of paired distal muscles of the tentacular lamina of one tentacle fuse and give rise to the frontal muscle (fm) of the tentacle (Fig. 7D). The abfrontal muscle (afm) of the tentacle appears as several muscular fibers at the base of the tentacle. Each tentacle has abfrontal muscles, which are represented by five to seven muscular cells, and a frontal muscle, which looks like a single, thick muscular bundle (Fig. 7C).

The epistomal musculature is composed of external circular and internal longitudinal muscular fibers (Fig. 6H). Two nephridioducts and the anus are located on the anal side of the lophophore (Fig. 7A, B). The musculature of the anal hill is mostly circular (Fig. 7B). Each nephridioduct has two layers of circular muscles: inner and outer (Fig. 7A).

Myoanatomy of the lophophore of Phoronis australis

The musculature of the lophophore in P. australis consists of the same groups as in P. ijimai, but the muscles differ in morphology (Fig. 8A). The circular muscle of the lophophore base (cm) extends along the lophophore base and is connected to the truncal musculature via separated short longitudinal muscles of the lophophore base (lib) (Fig. 8B). The lophophore is underlain by the circular portion of the trunk, which also has the circle muscle (Fig. 8C).

Longitudinal muscles of the tentacular lamina (ltl) start as thin numerous projections that group together and form a bipartite bundle in the base of each tentacle (Fig. 8B). The groups of paired distal muscles (pdm) of the tentacular lamina are associated with longitudinal muscles of the tentacular lamina (ltl): together they form a complex muscular construction that occupies the whole abfrontal side of the tentacle base (Fig. 8B). Groups of paired distal muscles (pdm) of the tentacular lamina give rise to the abfrontal muscle (afm) of the tentacle (Fig. 8A). The frontal muscles (fin) of the tentacle start from the base proper, extend along the tentacular lamina, and then continue to the tentacle (Fig. 8D). Each tentacle contains thick frontal muscle and several (three to four) thin abfrontal muscles (Fig. 8F). Intertentacular muscles (itm) consist of six muscle fibers and pass between tentacles along the frontal side of the distal end of the tentacular lamina (Fig. 8D). The epistomal musculature is mostly formed by numerous circular muscles (Fig. 8E).

Myoanatomy of the lophophore of Phoronopsis harmeri

In P. harmeri, the lophophore base is surrounded by a collar, which has its own circular muscle (trc, trunk circular muscle) that extends along the anal and lateral sides of the body (Fig. 9A). The lophophore base contains the circular muscle (cm), which is wave-like (Fig. 9A, B). The circular muscle of the lophophore base is connected to the truncal musculature via thin, separated longitudinal muscles (lib) of the lophophore base (Fig. 9B). A complex net of muscles that form the musculature of the lophophore base is located above the circular muscle. This net includes longitudinal muscles of the tentacular lamina (ltl) and paired diagonal muscles (dm) that extend from the longitudinal muscles of the tentacular lamina to the body wall (Fig. 9B). The lophophore base contains a thin, inner circular muscle (icm) that extends above the lophophoral blood vessels (Fig. 9C).

The musculature of the tentacular lamina includes longitudinal muscles (ltl) and groups of paired distal muscular bundles (pdm) (Fig. 9A, C, D). The longitudinal muscles of the tentacular lamina begin as two parallel muscular bundles that extend from the "wave crest" of the circular muscle of the lophophore base (Fig. 9A). These bundles are connected to the inner circular muscle via thin arch-like projections (Fig. 9C, arrowheads). Above the arch-like projections, the longitudinal muscle consists of numerous thin muscles that distally fuse and form a single, thick muscular bundle. This bundle is associated with groups of paired distal muscular bundles. Each tentacle contains two bundles of these muscles, located at the tentacle base (Fig. 9D, E). Each bundle of paired muscles consists of 15 to 20 thick fibers that extend along the frontal surface of the tentacle base (Fig. 9E). At the distal end of the tentacular lamina, groups of abfrontal transversal muscles are located between tentacles (itm) (Fig. 9F). In the distal portion of the tentacular lamina, the abfrontal tentacular muscles (afm) start as a bundle of numerous (8-10) thick muscular fibers (Fig. 9F). In the tentacular lamina, the frontal tentacular muscle (fm) is very thin and is associated with the blood vessel, but it is not evidently connected to the longitudinal muscle of the tentacular lamina (Fig. 9E). Each tentacle contains a very thick, compact frontal muscle and three to four thin abfrontal muscles (Fig. 9H). In the tentacles, the circular muscles of the wall of the blood vessel are well developed (Fig. 9H).

Discussion

Lophophore myoanatomy of the phoronids

The organization of lophophore muscles is generally similar in the three phoronid species of the current study (Fig. 10). In all three species, the main muscle of the lophophore is the circular muscle, which is connected to the truncal muscles via short longitudinal muscles. The circular muscle contacts the longitudinal muscles of the tentacular lamina, and these longitudinal muscles are associated with groups of paired distal muscles. The tentacles contain frontal and abfrontal muscles. Thus, in all three phoronids in the current study, the musculature of the lophophore has four main elements: a circular muscle, longitudinal muscles of the tentacular lamina, groups of paired distal muscles of the tentacular lamina, and frontal and abfrontal muscles of the tentacles.

The most important differences concern complexity. In Phoronis ijimai, the musculature of the horseshoe-shaped lophophore lacks the additional muscles of the tentacular lamina, which are present in Phoronis australis and Phoronopsis harmeri. Thus, among studied phoronids, Phoronis australis has the strongest tentacular muscles; the frontal and abfrontal tentacular muscles arise from the lophophore base and extend along the whole tentacular lamina. Such strong tentacular musculature probably helps stabilize the tentacles, which is important because P. australis adults have a huge lophophore with many tentacles. The lophophore musculature is most complex in Phoronopsis harmeri, in that the musculature includes an inner circular muscle and arch-like muscles.

The myoanatomy of the lophophore of the three phoronid species in the current study differs from that of Phoronis ovalis in several ways. In P. ovalis, the circular muscle extends around the pharynx and is connected to the radial dilators of the pharynx (Temereva, 2019; Fig. 10). In P. ijimai, P. australis, and Phoronopsis harmeri, in contrast, the circular muscle extends around the lophophore base and is connected to the longitudinal muscles of the tentacular lamina, which probably cannot function as dilators of the pharynx. This difference in the location of the circular muscle may be explained by the pharynx, which occupies the entire volume of the lophophore base in Phoronis ovalis but not in the other three species; thus, the circular muscle of the lophophore base abuts the pharynx in P. ovalis (Fig. 10).

In P. ovalis, moreover, the lophophore base is very long and bears longitudinal, radial, and circular muscles that contribute to the movements of the lophophore and to the transportation of food in the pharynx (Temereva, 2019). In the other phoronid species, the lophophore base lacks radial muscles, and the longitudinal muscles are short. Because they are short, the longitudinal muscles in the other three species probably have a limited ability to contribute to lophophore movement.

Although there are differences in the musculature of the lophophore in adults of Phoronis ijimai, P. australis, Phoronopsis harmeri, and Phoronis ovalis, there are important similarities; that is, the musculature of the lophophore in adults of all four species includes the following main elements: (i) a circular muscle, (ii) longitudinal muscles of the tentacular lamina, (iii) groups of paired distal muscles of the tentacular lamina, and (iv) frontal and abfrontal muscles of the tentacles.

The musculature of the horseshoe-shaped lophophore in P. ijimai has four parts but lacks the additional muscles of the lophophore base (which are present in P. ovalis) and of the tentacular lamina (which are present in P. australis and Phoronopsis harmeri). It follows that among the four phoronid species, the lophophoral musculature seems to be the least specialized in Phoronis ijimai.

Myoanatomy of the lophophore in the Lophophorata

By definition, the lophophore is a special part of the body that bears tentacles that surround the mouth but that never surround the anus (Emig, 1976). Three groups of invertebrates have lophophores and are traditionally regarded as belonging to the Lophophorata: the Phoronida, Brachiopoda, and Bryozoa.

Because the lophophore is the main synapomorphy of all lophophorates, the study of its organization may be useful for determining whether the lophophorates are monophyletic, which has not been supported by many molecular studies (Dunn et al., 2008; Hejnol et al., 2009; Kocot et al., 2017). On the other hand, recent molecular data support the monophyly of lophophorates (Laumer et al., 2015; Marletaz et al., 2018; Zverkov et al., 2019). These recent molecular results are consistent with many morphological studies of the lophophore, which have revealed great similarities in the organization of the nervous system of the lophophore in phoronids, brachiopods, and bryozoans (Temereva and Tsitrin, 2015; Temereva and Kosevich, 2016, 2018a, b; Temereva, 2017a, b). A recent report documented the presence of homologous structures in the organization of musculature of the lophophore in Phoronis ovalis and in bryozoans (Temereva, 2019).

The myoanatomy of the lophophore has been well studied in bryozoans by modern methods (Schwaha et al., 2011; Schwaha and Wanninger, 2012, 2018; Grischenko and Chernyshev, 2015; Gawin et al., 2017; Schwaha et al., 2018; Worsaae et al., 2018), but it has been less well studied in phoronids (Temereva, 2019) and in brachiopods (Temereva, 2017d; Kuzmina et al., 2018). A previous report found that the musculature of the lophophore of P. ovalis adults and bryozoans has a four-part pattern (Temereva, 2019). The current study demonstrated that this pattern also occurs in the adults of three other phoronids. In brachiopods, whose lophophoral musculature has never been reconstructed three-dimensionally, a different pattern is evident. In adult brachiopods, transverse and longitudinal muscles extend into the lophophore base (the small canal of the lophophore), and frontal and abfrontal muscles extend into the tentacles (Temereva, 2017d; Kuzmina et al., 2018). Brachiopods lack longitudinal muscles of the tentacular lamina and groups of paired distal muscles of the tentacular lamina. Thus, the lophophoral musculature in brachiopods has two rather than four parts. The reduction of muscles of the tentacular lamina correlates with the absence of a tentacular lamina in brachiopods.

The morphological similarity of the myoanatomy of the lophophore in all phoronids and all bryozoans is consistent with the monophyly of the lophophorates.

Conclusion

Because the four-part ground plan of the lophophoral musculature was evident in all studied phoronids, this ground plan may be regarded as ancestral for all phoronids. Diversifications of the lophophoral musculature, found in Phoronis australis, Phoronopsis harmeri, and Phoronis ovalis, may correlate with subsequent changes in lophophore morphology. Two possible evolutionary scenarios may be suggested for transformation of lophophore morphology. According to the first scenario, the morphology of the ancestral horseshoe-shaped lophophore transformed either by (i) becoming increasingly complex, in the case of most phoronids, or by (ii) becoming increasingly simplified, in the case of P. ovalis and bryozoans. In the second scenario, the morphology of the ancestral oval-shaped lophophore gradually evolved (i) to a horseshoe shape and then (ii) to a spiral shape.

The four-part ground plan of the lophophoral musculature in phoronids completely corresponds to that of bryozoans. Although the similarity in the myoanatomy of the lophophore in phoronids and bryozoans supports the monophyly of the lophophorates, this possibility should be tested by the examination of additional species of lophophorates by both morphological and molecular methods.

Acknowledgments

This research was supported in part by the Russian Foundation of Basic Research (grant 17-04-00586; histology and light microscopy) and the Russian Science Foundation (grant 18-14-00082; confocal laser scanning microscopy studies). The work was performed at the User Facilities Center of M.V. Lomonosov Moscow State University, with financial support of the Ministry of Education and Science of the Russian Federation.

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ELENA N. TEMEREVA

Department of Invertebrate Zoology, Biological Faculty, Moscow State University, Moscow, Russia, and National Research University Higher School of Economics, Moscow, Russia

Received 1 March 2019; Accepted 8 July 2019; Published online 6 December 2019.

Email: temereva@mail.ru.

DOI: 10.1086/705424
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Author:Temereva, Elena N.
Publication:The Biological Bulletin
Article Type:Technical report
Geographic Code:4EXRU
Date:Dec 1, 2019
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