Arctic cheilostome bryozoan species of the genus Escharoides

This investigation focuses on the diversity and identity of species of Escharoides found north of the Arctic Circle. Study of type and other material from this region using SEM shows that only two Arctic species can be recognized, Escharoides bidenkapi (Kluge) and E. jacksoni (Waters). The first of these is characterized by the distolateral orientation of the avicularia located beside the orifice, and by the suboral shelf on the distal border of the autozooidal orifice which is crenulated. Escharoides jacksoni differs in having slightly larger avicularia that are directed laterally, and a smooth suboral shelf.


Introduction
The ascophoran cheilostome bryozoan genus Escharoides contains approximately 45 species, fossil and living (Bock 2006). It is one of the longest ranging of all ascophoran genera, with recorded occurrences stretching back to the Late Cretaceous (e.g. Guha and Nathan 1996), although some putative species from the Cretaceous are better assigned to other genera (Taylor and McKinney 2006). Recent species are distributed worldwide across all climatic zones, from the poles to the tropics. There are no obvious diversity hot spots, although species richness does seem to be greatest in temperate seas. To date 15 species have been described from the northern hemisphere (Bock 2006). The present paper focuses on species of Escharoides from the Arctic (i.e. north of the Arctic Circle). Kluge's (1962Kluge's ( , 1975 comprehensive taxonomic study of Arctic bryozoans listed four species and one variety of Escharoides. These are Escharoides coccinea (Abildgaard, 1806), E. bidenkapi (Kluge, 1946), E. jacksoni (Waters, 1900), E. monstruosa (Kluge, 1946), and E. jacksoni var. rostrata Kluge, 1946. However, E. coccinea is Atlantic boreal in distribution and has never been recorded in the Arctic (Kluge 1975;Hayward and Ryland 1999). Furthermore, Escharoides monstruosa lacks the lateral avicularia characteristic of Escharoides (see Figure 1) and is considered to belong elsewhere.
Species of Escharoides possess complex calcified skeletons, which should facilitate determination of species and allow taxonomic resolution within this genus. However, the lack of scanning electron microscopy (SEM) of the genus has hindered progress, and the number of species inhabiting the Arctic has remained uncertain. For example, Bille-Hansen (1962) synonymized E. jacksoni and E. bidenkapi, an opinion followed by Hayward and Ryland (1999). There is also uncertainty whether a variety of E. jacksoni (Waters, 1900), E. jacksoni var. rostrata Kluge, 1946, should be regarded as a distinct species. Here we use SEM to study type and other Arctic material of Escharoides in order to evaluate the species diversity of this genus in the Arctic and to provide up-to-date descriptions and illustrations.

Material and methods
Material studied is lodged in the Natural History Museum, London (NHM); University of Manchester Museum (MM); Canadian Museum of Nature, Ottawa (CMN); and Zoological Institute of the Russian Academy of Sciences, St Petersburg (ZI). Both historical and new collections were employed for this study.
Scanning electron microscopy was undertaken with a low-vacuum instrument (LEO 1455-VP) capable of imaging uncoated specimens using back-scattered electrons.

Diagnosis
Frontal shield with marginal areolae, lacking pseudopores; umbonuloid, with ring scar on underside. Oral spines present on distal border of orifice; secondary orifice generally peristomate and/or with denticles. Avicularia well developed, single or paired, lateral to orifice, pointed. Ovicell prominent, hyperstomial.

Remarks
Although Escharoides coccinea has never been recorded from the Arctic (Kluge 1975), it is the type species of Escharoides and we therefore present SEM images of this species to illustrate the key characteristics of the genus (Figure 1). Hayward and Ryland (1999) provided a detailed description of this species. The frontal shield is more coarsely tuberculate in E. coccinea than in either of the two Arctic species of Escharoides; there are six rather than four oral spines; and the paired avicularia are often of different sizes ( Figure 1C), a feature not seen in either E. bidenkapi or E. jacksoni.

Type material examined
Lectotype: ZI 30/2945, Kara Sea, ''Sadko'' Stn 58/98, 12 September 1935, det. Kluge from Gorbunov material, Kluge Collection. This specimen from the Kluge Collection is here chosen as the lectotype based on the match between the locality information and that given in the original description (Kluge 1946

Description
Colony forming a thick unilaminar crust ( Figure 2A). Ancestrula ( Figure 2D) tatiform, oval, with narrow cryptocyst, broad proximal gymnocyst, and 14 spines. Autozooids large, irregular in shape, separated by deep grooves, 0.61-1.03 mm long (mean 0.84 mm, n520) by 0.50-0.76 mm wide (mean 0.62 mm, n520). Frontal shield usually granular with polygonal surface patterning, bordered by a single or double row of round areolae. Orifice suborbicular; distal border with a broad, crenulated suboral shelf ( Figure 2C); proximal edge developed as a thick, projecting peristome with usually three (one median and paired lateral) thickened denticles around proximal inner margin, and with a median notch on the rim. Denticles and notch sometimes missing. Denticles when present striated. Oral spines usually numbering four, short, thick, the outer two fused with the peristome. Ovicellate zooids have only two visible oral spines. Avicularia typically paired at distolateral corners of autozooids, sometimes single, very rarely lacking, large, 0.17-0.28 mm long (mean 0.23 mm, n520) by 0.09-0.13 mm wide (mean 0.11 mm, n520), directed distolaterally, rostrum narrowly triangular, hooked at tip, avicularian chamber often with pores at the base and rarely on the chamber itself; mandible elongatetriangular, crossbar calcified.

Distribution
This Arctic and deep-water temperate species has been most frequently recorded from the Atlantic part of the Arctic. There are some records from the East Siberian Sea but none so far from the Canadian Arctic, which means that E. bidenkapi is probably not circumpolar in distribution. The species has been recorded as far south as the Bay of Biscay, at depths of 1390-1582 m in the temperate Atlantic (Hayward and Ryland 1978).

Distribution
An Arctic, circumpolar species recorded from the Greenland, Barents, Kara, Laptev, East Siberian, and Chukchi Seas; and the Canadian Arctic (Kluge 1975;current account). -Hansen (1962) and Hayward and Ryland (1999) synonymized Escharoides bidenkapi (Kluge, 1946) with E. jacksoni (Waters, 1900). However, their analyses were based on small sample sizes, and the synonymy is not supported by a more detailed comparison. Our broader investigation using SEM permits us to distinguish E. bidenkapi (Figure 2) and E. jacksoni (Figures 3, 4) as separate species. Both species have a similar peristome shape, but there is large variation both among colonies and within colonies of Escharoides in this character. However, a few skeletal morphological characters do allow us to distinguish these two species with confidence. In general, the peristome of E. bidnekapi is much more complex than that of E. jacksoni. In E. jacksoni the peristome is never produced into three prominent denticles (cf. Figure 2C). On average, autozooids of E. bidenkapi are smaller than those of E. jacksoni, as are the avicularia. Also, in the majority of cases, avicularia of E. bidenkapi are directed distolaterally, whereas those of E. jacksoni are typically directed laterally. The frontal shield texture of E. bidenkapi is polygonal, whereas that of E. jacksoni is finely granulated, although in early astogeny E. jacksoni also has frontal shields with a polygonal texture (see Figures 2D, 3D). A very stable character of skeletal morphology among the specimens studied is the structure of the distal edge of the suboral shelf. In E. bidenkapi this is crenulated, whereas in E. jacksoni it is always smooth. Escharoides jacksoni has more bulbous avicularian chambers, which are better demarcated from the autozooidal frontal shield than in E. bidenkapi.

Bille
Escharoides bidenkapi and E. jacksoni overlap in geographical distribution but whereas E. jacksoni is circumpolar in distribution, E. bidenkapi does not occur in some parts of the Arctic (e.g. Canadian Arctic, Chukchi Sea). In our study material, we found one instance of the two species growing together on the same substratum ( Figure 5). The adjacent colonies show the distinctive characters mentioned above for the two species, which cannot be ecophenotypic as the colonies are juxtaposed. This specimen therefore supports the assertion that E. bidenkapi and E. jacksoni are two separate species.

Discussion
The complexity of the skeleton found in Escharoides makes recognition of the genus relatively straightforward. However, despite possessing numerous skeletal characters, species determination is challenging, as reflected by errors in the taxonomic literature. Small samples may be misleading in not allowing within species variability to be taken into account when identifying species of Escharoides. Kluge (1962Kluge ( , 1975 believed the Arctic biodiversity of Escharoides to comprise four species and one variety (see Introduction). Comparative scanning electron microscopy of type and other material has confirmed the distinctiveness of two species, E. bidenkapi (Kluge) and E. jacksoni (Waters), which have in the past been incorrectly synonymized under the name E. jacksoni (e.g. Bille-Hansen 1962; Hayward and Ryland 1999). The third species (E. coccinea) listed by Kluge (1962Kluge ( , 1975 seems not to occur in the Arctic, and the fourth species (E. monstruosa) does not belong to Escharoides. As with the majority of bryozoans, genetic studies of Escharoides are needed to test species distinctions made using skeletal morphology.