Pleistocene Bryozoans from the Clyde Clay Formation of Scotland, and the Holocene Retreat of Cold-Water Species

: Although bryozoans are a diverse phylum of aquatic invertebrates with a rich fossil record, very little has been written about bryozoan faunas from the latest Pleistocene at a time of rapid global change when temperatures increased dramatically and the sea-level rose. Two species of cyclostome and eight species of cheilostome bryozoans are here described from the late Devensian Clyde Clay Formation of Greenock, Scotland, based on historical material in the collections of the NHM, UK. All are illustrated for the ﬁrst time from this deposit using scanning electron microscopy. Three of the species ( Tubulipora cf. marisalbi , Rhamphostomella radiatula and Schizomavella porifera ) are unknown from the seas around Scotland at the present-day but occur in colder waters to the north. This is consistent with the poleward retreat of cold-water species as seawater temperatures increased at the end of the Pleistocene.


Introduction
Concomitant with global warming and facilitated by human-related dispersal mechanisms, the last few decades have seen the expansion of the ranges of several bryozoan species into higher latitudes. These include warm-water fouling species, notably Bugula neritina, Watersipora subatra and Schizoporella japonica, which have begun to appear in harbours increasingly further north in the Atlantic waters of northwest Europe [1][2][3]. A further expectation is that the ranges of cold-water bryozoan species will have contracted polewards as sea temperatures increased, causing local extinctions. However, it is unclear whether any such range contractions have actually been documented.
Rapid climatic warming marked the end of the so-called Ice Age in the late Pleistocene [4]. Comparing the composition of fossil bryozoan faunas formed at this time with those of the present-day in the same region has the potential for identifying local extinctions of cold-adapted species. Unfortunately, very little has been published on bryozoans from the latest Pleistocene, especially in northern Europe. The presence in the Natural History Museum, London (NHMUK) of some latest Pleistocene bryozoans collected during the late 19th century from temporary exposures near the shore of the Firth of Clyde downstream of Glasgow at Garvel Park, Greenock (Figure 1), allows a glimpse of a bryozoan fauna that lived at a coastal site following deglaciation and sea-level rise. A few lists of bryozoan species from the Garvel Park have been published [5][6][7], but none of the species recorded have been described or figured. The current paper provides the first descriptions and figures of the Garvel Park bryozoans, some of which no longer live in Scottish waters but are present in colder waters further to the north, an example of 'trailing-edge extirpation' [8].  [9], and the location (star) of the latest Pleistocene fossil bryozoan locality at Garvel Park, Greenock.

Materials and Methods
This taxonomic study is based entirely on historical material lodged in the fossil collections of the NHMUK. Some of these specimens were presented to the museum by D. Robertson on 4 November 1883, one is from the collection of J. Young and a few are from the collection of E. Jelly, who is known to have received bryozoans from other collectors and then redistributed them to her colleagues. The specimens donated by Robertson are labelled 'Garvel Park, Greenock'. Other specimens, which were apparently collected at about the same time, probably came from the same locality or very nearby. Colonies are fragmentary but well preserved, allowing identification to species level in most instances.
Robertson [6] gave a detailed account of the Pleistocene geology of Garvel Park, Greenock, where the construction of a dry dock in 1870 and a wet dock in 1881 exposed boulder clay overlain by a sequence of clays and sands containing marine shells. These late glacial marine deposits came to become known as the 'Clyde beds' [10] or 'Garvel Park Beds' [7] but have since been given the formal name Clyde Clay Formation [11,12]. No permanent exposures exist at Greenock but temporary excavations both during the late 19th century and again in 1962 allowed the Clyde Clay Fm. to be seen in six small basins to a thickness of 10 m or more [10]. Unfortunately, the exact stratigraphical level (or levels) from which the bryozoans were collected is unknown. The Clyde Clay Fm. is a glaciomarine deposit considered to have been formed during the late Devensian (= late Weichselian) Marine Isotope Stage 2, about 13-10 ka BP [12,13].
After initial study with an optical microscope, the bryozoans were examined and imaged using a LEO 1455-VP scanning electron microscope. This instrument was operated in low vacuum mode, allowing the uncoated bryozoans to be imaged using a back-scat- Figure 1. Regions of the sea around Scotland, based on work by Rouse and others [9], and the location (star) of the latest Pleistocene fossil bryozoan locality at Garvel Park, Greenock.

Materials and Methods
This taxonomic study is based entirely on historical material lodged in the fossil collections of the NHMUK. Some of these specimens were presented to the museum by D. Robertson on 4 November 1883, one is from the collection of J. Young and a few are from the collection of E. Jelly, who is known to have received bryozoans from other collectors and then redistributed them to her colleagues. The specimens donated by Robertson are labelled 'Garvel Park, Greenock'. Other specimens, which were apparently collected at about the same time, probably came from the same locality or very nearby. Colonies are fragmentary but well preserved, allowing identification to species level in most instances.
Robertson [6] gave a detailed account of the Pleistocene geology of Garvel Park, Greenock, where the construction of a dry dock in 1870 and a wet dock in 1881 exposed boulder clay overlain by a sequence of clays and sands containing marine shells. These late glacial marine deposits came to become known as the 'Clyde beds' [10] or 'Garvel Park Beds' [7] but have since been given the formal name Clyde Clay Formation [11,12]. No permanent exposures exist at Greenock but temporary excavations both during the late 19th century and again in 1962 allowed the Clyde Clay Fm. to be seen in six small basins to a thickness of 10 m or more [10]. Unfortunately, the exact stratigraphical level (or levels) from which the bryozoans were collected is unknown. The Clyde Clay Fm. is a glaciomarine deposit considered to have been formed during the late Devensian (= late Weichselian) Marine Isotope Stage 2, about 13-10 ka BP [12,13].
After initial study with an optical microscope, the bryozoans were examined and imaged using a LEO 1455-VP scanning electron microscope. This instrument was operated in low vacuum mode, allowing the uncoated bryozoans to be imaged using a back-scattered electron detector. Species descriptions are based on the scanning electron micrographs obtained, and measurements were made from these calibrated micrographs. Abbreviated synonymies are given for each species that include the first description, first referral to the currently accepted genus, and a modern description. tered electron detector. Species descriptions are based on the scanning electron micrographs obtained, and measurements were made from these calibrated micrographs. Abbreviated synonymies are given for each species that include the first description, first referral to the currently accepted genus, and a modern description.
Remarks. Seven species of Tubulipora have been recorded from the seas around Scotland [9], three from the Clyde region ( Figure 1): T. flabellaris, T. liliacea and T. lobifera. However, the Clyde Clay Fm. specimen resembles none of these three and instead is closer in overall morphology to a fourth Scottish species [17] (T. aperta) not recorded from western Scotland but which has a funnel-shaped ooeciostome and a larger ooeciopore than the fossil species. A better match is with T. marisalbi Gostilovskaja, 1955 [14], in which the ooeciopore is described as being smaller than an autozooidal apertures and the ooeciostome appears not to be flared [16]. This species is known only from the White Sea where it is very rare (A.N. Ostrovsky, pers. comm. 20/3/2021). Pending a modern revision of the type material of T. marisalbi, the single Clyde Clay Fm. specimen can only be referred with some reservation to this Arctic species.
Genus Idmidronea Canu and Bassler, 1920 Idmidronea atlantica (Forbes in Johnston, 1847) Figure  Material examined. NHMUK B1223a-d. Robertson Collection. Description. Colony erect, comprising narrow, about 0.6-1 mm wide, bifurcating branches of rounded triangular cross-section with zooids opening on the two frontolateral sides and lacking on the abfrontal side; branch abfrontal formed of pseudoporous exterior wall marked by traces of the basal outlines of the zooids; kenozooidal overgrowths often developing on branch reverse apparently originating from enlarged pseudopores. Autozooids arranged in transverse series comprising four or five zooids on each of the two frontolateral branch sides, alternating along the midline with series on the opposite frontolateral side; peristomes basally connate, becoming separated distally, particularly those of the most axial zooid; apertures circular to rounded quadrate, up to 100 µm in diameter; frontal walls slightly convex, irregularly and sparsely pseudoporous, 388-447 µm long (mean 418 µm; SD 18 µm; N = 10) by 82-106 µm wide (mean 85 µm; SD 7 µm; N = 10). Gonozooid elongate, brood chamber 2.6 mm long, located along the branch axis with lobes extending between autozooidal series, continuing into the two daughter branches at bifurcation; frontal wall densely covered with elliptical or teardrop-shaped pseudopores, sutured along the midlines of the main axis and lobes; ooeciostome about midway along length of brood chamber, attached to the distal side of an autozooidal peristome, oriented distolaterally, gently dilated distally, straight and tubular, distal end probably broken off; ooeciopore about the same diameter as an autozooidal aperture. Kenozooids developing on branch abfrontal side as patches or a more extensive proximally directed overgrowth; frontal walls lacking, apertures oblique, irregular in size and shape.
Remarks. Idmidronea atlantica is represented in the Clyde Clay Fm. by broken branches from what would originally have been erect colonies in the form of two-dimensional fans. Vine (1885, p. 214) [7] described this species as the 'most important' in the Garvel Park bryozoan fauna, possibly meaning that it is the most abundant or conspicuous. Idmidronea atlantica is a widely distributed species in the Atlantic and Mediterranean today, from the Arctic to the tropics [17]. However, taxonomic revision incorporating molecular data is needed to test whether this name has been applied to more than one species, which this broad latitudinal (and thermal) distribution would suggest. In Scotland at the present-day it is known from three regions (Minches and Malin Sea, Rockall and West Shetland) but has not been recorded from the Clyde region [9].  Figure 3A Taxonomy 2021, 1, FOR PEER REVIEW 5 length of brood chamber, attached to the distal side of an autozooidal peristome, oriented distolaterally, gently dilated distally, straight and tubular, distal end probably broken off; ooeciopore about the same diameter as an autozooidal aperture. Kenozooids developing on branch abfrontal side as patches or a more extensive proximally directed overgrowth; frontal walls lacking, apertures oblique, irregular in size and shape.
Remarks. Idmidronea atlantica is represented in the Clyde Clay Fm. by broken branches from what would originally have been erect colonies in the form of two-dimensional fans. Vine (1885, p. 214) [7] described this species as the 'most important' in the Garvel Park bryozoan fauna, possibly meaning that it is the most abundant or conspicuous. Idmidronea atlantica is a widely distributed species in the Atlantic and Mediterranean today, from the Arctic to the tropics [17]. However, taxonomic revision incorporating molecular data is needed to test whether this name has been applied to more than one species, which this broad latitudinal (and thermal) distribution would suggest. In Scotland at the present-day it is known from three regions (Minches and Malin Sea, Rockall and West Shetland) but has not been recorded from the Clyde region [9].  1851 Cellularia peachii Busk [20], p. 82 1966 Bugulopsis peachii (Busk): Prenant and Bobin [21], p. 442 1998 Tricellaria peachii (Busk): Hayward and Ryland [22], p. 284, fig. 96 Material examined. NHMUK D1633. J. Young Collection. Description. Small branch internode preserving 6 zooids arranged biserially, opening alternately on either side of the internode frontal side. Autozooids elongate pyriform, c. 700 µm long by 300 µm wide; proximal gymnocyst occupying slightly less than half of frontal surface, forming a short prolongation at the outer distal angle of the zooid, brokenoff in the fossil to leave an elongate depression; cryptocyst narrow; opesia longitudinally elliptical, about 400 µm long by 200 µm wide. Avicularia lacking. Ovicells not developed in the single specimen studied, when present globose and with an uncalcified window in the ectooecium.
Remarks. Living examples of species are slender, tuft-like colonies consisting of articulated internodes of seven to nine zooids attached to the substrate by rhizoids. In the eastern Atlantic, the geographical range of B. peachii extends from the Yorkshire coast of England northwards to Shetland, Spitsbergen and the White Sea [22]. It has been recorded living in several regions around Scotland [9], though not on the west side of the country including the Clyde region. Remarks. Living colonies of Caberea ellisii are fan-shaped and 2-3 cm in height [22]. The vibracula on the abfrontal surface have long setae that are serrated. In Britain, this distinctive and widespread species occurs today mostly in Scotland where it is recorded from two regions: North Scotland and West Shetland [9]. Its northerly range extends to Iceland [25] and the White Sea [16].
Remarks. This Arctic-Boreal species is not known to occur in the seas around Britain at the present-day. In Europe it has been recorded from the Barents Sea, White Sea, Iceland and northern Norway [34]. Elsewhere, it has been found in the Canadian Arctic, Labrador, western Greenland, Alaska and Hokkaido. However, neither R. radiatula nor any other species of Rhamphostomella have been recorded living in the seas around the British Isles at the present-day. The abundance of ovicells in the colonies found in the Clyde Clay Fm. imply that this species prospered in the latest Pleistocene at a latitude well south of its current range in Europe. Description. Three small fragments of encrusting colonies detached form their substrates, the largest preserving 10 zooid. Autozooids separated by narrow grooves, hexagonal, 400-577 µm long (mean 507 µm; SD 41 µm; N = 12) by 345-422 µm wide (mean 386 µm; SD 24 µm; N = 12); frontal shield convex, pustulose, imperforate centrally but with marginal areolar pores in one row, occasionally two, radially elongated; orifice semielliptical, wider (c. 120 µm) than long (c. 100 µm), an anvil-shaped lyrula present on the proximal edge; six stout oral spine bases around distolateral edge, four in ovicellate zooids. Ovicells visible in one colony, broken, about 200 µm long by 230 µm wide. No avicularia.
Remarks. This cold-water, Boreal-Arctic species is abundant today in the North Atlantic [28], recorded as far south as the Iberian Peninsula [36]. It has been reported from several Scottish regions, including the Clyde [9].   frontal shield with large areolar pores separated by buttresses prolonged as radial ridges towards the imperforate centre of the frontal shield; primary orifice not visible, hidden by the peristome; oral spines lacking. Ovicells globular, 200 µm long by 250 µm wide, ooecium imperforate, crossed by similar radial ridges to those on the frontal shield. Avicularia adventitious, small, about 80 µm wide, suboral, oriented in a plane oblique to colony surface, directed proximally, rostrum rounded, pivotal bar calcified, usually broken.
Remarks. The single tiny specimen of this Porella is insufficient for the species to be identified with certainty. It does, however, show the greatest similarities with P. alba among the species of Porella recorded from British waters, although published figures of P. alba do not show the ridges on the ovicells that are so conspicuous in the Clyde Clay Fm. specimen. Porella alba is described as an Arctic-Boreal species distributed pan-globally [28]. Although present elsewhere in Scotland, it is unknown from the west coast including the Clyde region [9]. Remarks. This Arctic-Boreal species has a wide distribution [28,33], and has been recorded living in the Clyde region [9]. , boundary walls raised; frontal shield convex, areolar pores located at the corners of the zooid, large pseudopores covering the rest of the surface; orifice relatively large, 130 µm long by 120 µm wide, with a broad sinus demarcated from the rest of the orifice by a pair of prominent, horizontal condyles; peristome low, cormidial, with the distal edge formed by the distal autozooid; oral spine bases occasionally visible. Ovicells common, about 180 µm long by 270 µm wide, ectooecium uncalcified, entooecium with numerous irregularly shaped pores surrounded by raised rims, distal edge of ovicell overgrown by calcification of the distal zooid. Avicularia adventitious, suboral, included within the calcification of the peristome, small, about 60 µm wide, oriented proximally, inclined obliquely to surface, rostrum spoon-shaped, rounded, pivotal bar calcified.
Remarks. Regarded as a pan-Arctic species, S. porifera lives today in the western Atlantic from Greenland south to the Gulf of Maine, and across the Arctic from Iceland to northern Norway, the White Sea and the Sea of Japan [33]. It has not been reported from the seas around Britain.

Discussion
Pleistocene bryozoans from the late Devensian Clyde Clay Formation of Garvel Park, Greenock on the Firth of Clyde are described for the first time using historical material in the collections of the NHMUK. Two cyclostome and eight cheilostomes are identifiable. A recent checklist of Scottish bryozoans records seven of these ten species now living in the sea around Scotland. However, the Clyde Clay Fm. includes three species (Tubulipora cf. marisalbi, Rhamphostomella radiatula and Schizomavella porifera) that are unknown in the modern Scottish fauna, while a further four species (Idmidronea atlantica, Bugulopsis peachii, Caberea ellisi and Porella cf. alba) have not been recorded from the Clyde region. The three species currently unknown in Scotland are today distributed in colder, more northerly waters: their local extinction (extirpation) in Scotland is therefore consistent with warming of the sea around Scotland during the last 15,000 years. Thus, the Clyde Clay bryozoan fauna demonstrates the contraction towards the pole of the ranges of a few cold-water species as the Pleistocene icecaps receded.
Dealing only with the ten species identifiable in the collections of the NHMUK, this paper is not a comprehensive account of all of the bryozoan species from the Clyde Clay Fm. Faunal lists published during the 19th century name additional species. Vine [7] listed 15 species from Garvel Park, Robertson [6] the same number while noting the presence of a few more that were too imperfect for identification. Unfortunately, neither of these lists from the 1880s are accompanied by descriptions or figures, making the accuracy of the identifications impossible to evaluate. However, some of the species cited are unlikely to be among those described in the current paper, for example, Cribrilina annulata, Crisia eburnea and Diastopora [Diplosolen] obelium recorded by Vine [7] belong to distinctive genera quite unlike any of those described in the current paper.
Four species of non-calcareous algal fossils have been described from the Clyde Clay Fm. [30]. These extant species, together with an associated echinoid (Strongylocentrotus drobachiensis), have a wide latitudinal range at the present-day but predominantly inhabit cold seas. The algae live today between the low water mark and about 20 m depth, suggesting a similar depth of deposition for the Clyde Clay Fm. Most of the Clyde Clay Fm. bryozoans that are encrusting lack substrates and it is quite possible that they were epiphytic on algae no longer preserved. Indeed, algae are the most common substrates today for one of the Clyde Clay bryozoans, Celleporella hyalina [28].
The Clyde Clay Fm. Garvel Park is well-known for its rich mollusc fauna, the most diverse Pleistocene fauna from Scotland according to Peacock [10]. This author noted similarities between the Clyde Clay Fm. mollusc assemblage and modern shallow water Arctic communities in northeast Greenland and Spitsbergen today, consistent with the existence of Arctic water rather than Atlantic water off western Scotland at the time of deposition. This is corroborated by the bryozoan fauna described here.
Research on Upper Pleistocene bryozoans in NW Europe has been woefully neglected. Faunal lists published in the 19th century make it clear that bryozoans do occur in coastal marine sediments of this age, yet none seem to have been studied in recent years. Scanning electron microscopy, an essential tool in the taxonomy of bryozoans with mineralized skeletons, seems not to have been applied prior to the current study. There are two compelling reasons why Upper Pleistocene bryozoans in NW Europe merit study. The first is that they can provide information on how species distributions have changed with rapid global warming and sea-level rise. This has clear relevance to contemporary global change and how the geographical ranges of species might be impacted. The second is that knowledge of the composition of Late Pleistocene bryozoan faunas can help to assess which species are native to the biotas of particular regions. Although the fossil record is incomplete and will always fail to record the existence of many native species, especially those with weakly mineralized skeletons, fossils have the potential for furnishing positive evidence for the indigenous nature of those species that are preserved [41]. This is important because widespread anthropogenic dispersal of bryozoan species is known to have occurred through shipping [42], and this could date back to times when humans first undertook long distance sea voyages in wooden boats. Thus, while it is often easy to pinpoint species that have been introduced during the 150 or so years since scientific records have been kept, Upper Pleistocene bryozoan faunas have the potential to prove that other species were a component part of the native biota prior to the time when human activities perturbed natural distributions.