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CITATION Denisenko, N.V., and J.M. Grebmeier. 2015. Spatial patterns of bryozoan fauna biodiversity and issues of biogeographic regionalization of the Chukchi Sea. Oceanography 28(3):134–145, http://dx.doi.org/10.5670/oceanog.2015.62.

DOI http://dx.doi.org/10.5670/oceanog.2015.62

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Spatial Patterns of Bryozoan Fauna Biodiversity and Issues of Biogeographic Regionalization

of the Chukchi Sea By Nina V. Denisenko and Jacqueline M. Grebmeier

Bryozoan Parasmittina tatiani found in the Chukchi Sea.

134 Oceanography | Vol.28, No.3 ABSTRACT. Based on extensive data from a variety of sources, including Russian- biomass, estimating biomass for a major- American Long-term Census of the Arctic expeditions in 2009 and 2012, this paper ity of bryozoan species is difficult due to provides an update on the richness of bryozoans in the Chukchi Sea and evaluates the colonial and often encrusting nature the variation in bryozoan biodiversity along environmental gradients (e.g., depth, of the organism (N. Denisenko, 1983). bottom water temperature, and bottom sediment composition). Though bryozoans Moreover, old archived data do not con- have been studied in only about 77% of the Chukchi Sea, temperature gradients across tain information about bryozoan abun- geographical zones appear to control fauna richness. The inflow of Pacific water through dance. This fact may be one additional the Bering Strait into the Chukchi Sea strongly influences the distribution of the reason why there has been no statistical 204 registered bryozoan species, about 30% of which have a Pacific origin. The greatest estimation of bryozoan biodiversity for similarities between bryozoan fauna in the Chukchi Sea and those occurring further the Arctic. As a result, there has been no south in the Bering Sea are found in the southern and eastern parts of the Chukchi Sea. generalized report on bryozoan biodiver- The transitional zone between Arctic and Pacific high-boreal biogeographic regions sity or the relationship between faunal occurs in the western and northern areas of the Chukchi Sea. The dominance of boreal richness and environmental factors such bryozoan species over Arctic species in the southeastern and southern areas of the as depth, bottom water temperature, and Chukchi Sea identifies this area as part of a Pacific high-boreal region. The boundary bottom sediment composition. Taking between boreal and northern transitional zones corresponds to a 50:50 ratio of boreal to into account the intensity of zooben- Arctic species, with the transition extending from Cape Serdtse-Kamen’ in the western thos sampling in the Chukchi Sea (about Chukchi Sea northward to Point Franklin (68°30'N) in the eastern Chukchi Sea. 500 stations made by Russian expeditions and over a 1,000 stations by US expedi- INTRODUCTION (2008) increased the number of known tions alone), it could be assumed that the The study of Earth’s faunal biodiver- bryozoan species (see online supplemen- bryozoan records are sufficient to evalu- sity remains a pressing challenge within tary materials). Notably, most publica- ate the biodiversity of this faunal group; the field of biology. The number of pub- tions concerning bryozoans have been however, the quality of the available data lications devoted to this problem has mainly descriptive, with listings of spe- varies greatly and assumptions must be increased, although most studies are cies and their synonymy, and less focused made to utilize the different data sets. devoted to terrestrial ecosystems; only on their ecological importance. The Chukchi Sea is one of the world about 10% represent biodiversity stud- Understanding of Chukchi Sea bryo- ocean’s transitional areas, and there are ies in the marine environment (Hendriks zoan fauna has been enhanced by a syn- contrasting opinions regarding its bio- et al., 2006), and most of these have thesis using modern nomenclature of all geographic status. Some scientists con- been conducted in the temperate seas bryozoan faunal data based on both the sider the whole sea to be completely in the of the world ocean. collection of animals at the Zoological Arctic zone (Golikov, 1980; Andriyashev Biodiversity studies of fauna in Arctic Institute of the Russian Academy of and Shaposhnikova, 1985; Briggs, 1995), seas are steadily increasing, although Sciences and early data collected in the while others regard it as a transitional the number of publications on this issue framework of the Russian-American zone between the Arctic and boreo-Arctic​ remains limited. In recent years, a num- Long-term Census of the Arctic zones, depending on spatial location ber of reviews (e.g., Bluhm at al., 2011; (RUSALCA) program that began in 2004 (Grebmeier et al., 2006). Yet other scien- Kosobokova et al., 2011; Piepenburg (N. Denisenko, 2008; N. Denisenko and tists offer an intermediate interpretation, et al., 2011; Josefson et al., 2013) have Kuklinski, 2008). Additional collection where the southern part of the Chukchi been based on an increasing number of benthic samples during the RUSALCA Sea is a transitional zone, with the of field expeditions over the past two 2009 and 2012 expeditions further remainder belonging to the Arctic zone decades. However, the biodiversity and increased records of bryozoans and spe- (Mironov, 2013). Still others regard the spatial distribution of bryozoans, in par- cies counts beyond the 2008 publications. southern part of the Chukchi Sea as part ticular, still have not been estimated, We describe these findings here. of the Pacific boreal zone (Filatova, 1957; although this group is one of the most Magurran (2004) argued that spe- Scarlato, 1981; Petryashov at al., 2013). diverse fauna in the Arctic (Gontar and cies richness is the simplest way to esti- Based on our data compilations, first, Denisenko, 1989; Josefson et al., 2013). mate assemblage species diversity. we hypothesize that bryozoan diversity is Chukchi Sea bryozoans were one of However, estimation of species richness higher in the Chukchi Sea than previously the poorest known Arctic faunal types is quite difficult if information about recognized. Bryozoan species there are (around 140 species; Kluge, 1962; Gontar species composition is lacking, espe- distributed unequally and, in fact, form and Denisenko, 1989; Gontar, 2001) until cially for large regions. Although bio- local assemblages. The level of our under- recent compilations by N. Denisenko diversity is often estimated using quan- standing of bryozoan diversity depends (2008) and N. Denisenko and Kuklinski titative characteristics of abundance and on the intensity of bryozoan sampling

Oceanography | September 2015 135 in different regions of the Chukchi Sea, were preserved in 4% formalin in sea- (the ratio between local and regional coincident with the known relationship water, buffered by hexamine. Within two diversity) was used to show similar- between the variability of environmental to three months, animals were sorted, ity or dissimilarity of species composi- factors (e.g., seawater temperature, sed- identified as to species, counted, and tion of regional faunas (Magurran, 2004). iment grain size) and the different water weighed, and subsequently archived in The data on species numbers were pro- masses in the region. Second, we hypoth- 70% ethanol. The results from these new cessed statistically using Microsoft Excel esize that bryozoans, as sessile animals, bryozoan samples were combined with and StatSoft Statistica. Station-based are suitable organisms to use to determine published data, including information rarefication curves were used to compare biogeographic zonations within the sea. from American waters in the eastern sec- species numbers from the whole Chukchi Our current analysis of spatial changes in tion of the Chukchi Sea. Both physical Sea and at different depth ranges. The the biogeographic composition of bryo- samples and electronic data are archived nonparametric Chao2 estimator was cal- zoans within the Chukchi Sea should help at the Zoological Institute of the Russian culated by means using the statistical reduce the disparity in interpretations of Academy of Sciences. PRIMER software (v.4) in order to pre- their biogeographic status in this region. In preparing the list of species, we dict the expected number of species that used the most recent information about would be observed in the Chukchi Sea MATERIALS AND METHODS species taxonomy (Dick and Ross, 1988; (Clarke and Warwick, 1994). Similarity This work is based on an analysis of Grischenko, 2002; Dick et al., 2005; of the bryozoan fauna within the Chukchi archived data and data available in the Kuklinski and Taylor, 2006; Kuklinski Sea and in comparison with nearby literature, faunal collections held at et al., 2007; N. Denisenko, 2008; Bock, areas (Bering Sea, Canadian Arctic the Zoological Institute of the Russian 2015). The determination of biogeo- Archipelago, East Siberian Sea) was esti- Academy of Sciences that were evaluated graphic groups was based on a literature mated using presence-absence informa- previously (N. Denisenko, 2008), and new review of species habitats and thermal tion of species with the Czekanowski- material collected in the Chukchi Sea in tolerances (Golikov and Scarlato, 1972; Sørensen index (Czekanowski, 1909; the framework of the RUSALCA program Golikov, 1982). Sørensen, 1948), based on the formula:

in 2009 and 2012, resulting in bryozoans Is = 2 c/(Di + Di+1) * 100%, where c is being identified in 170 samples collected Data Analysis the number of species in common to

at 128 stations (Figure 1). Equipment Variation in bryozoan diversity was both stations, Di is the number of species used to collect the recent bryozoan sam- estimated at station (α-diversity) and found at the first station, and iD + Di+1 is ples included dredges, trawls, and grabs; regional (γ-diversity) levels, where spe- the number of species at the second sta- all samples collected at the same stations cies richness is seen in large areas of tion. Similarity values were used for clus- were combined for the analysis. Animals embayments and seas. Beta (β) diversity ter analysis using a moving average rou- tine (Pesenko, 1982; Pielou, 1984). Fauna heterogeneity was evaluated using the 5 multidimensional scaling (MDS) method

72°N on 10

ny in PRIMER (v.4). In order to evaluate on 30 ny 50 the reliability of the MDS analysis, the Wrangel 75 ANOSIM (analysis of similarity) statisti-

Island Herald Ca Barrow Ca 125 Long Strait Point cal program was used in Primer (Clarke 70°N Barrow 250 Point Franklin Depth (m) 750 and Warwick, 1994). 1,250 Icy Cape Chukchi Sea 1,750 2,500 STUDY AREA Cape 5 3 68°N Schmidt Cape Lisburne 3,500 About 50% of the Chukchi Sea is shal- 4 Point Hope el lower than 50 m (Hunt et al., 2013),

ann Alaska

Chukotka Ch and the seafloor slopes gently north- Peninsula 2 ward to the edge of the Arctic basin 66° Central N Cape Kotzebue (Figure 1). Irregular seafloor relief in Serdtse Sound Kamen’ 175°E the Chukchi Sea is more pronounced 155°W 180°E 1 160°W in the northern region. In the central 175°W 170°W 165°W part of the sea, there is a small depres- FIGURE 1. Station locations in five separate areas of the Chukchi Sea where bryozoan spe- sion with depths up to 55 m that extends cies were collected in RUSALCA 2009 and 2012 and prior cruises. 1 = Bering Strait region. 2 = Southern region. 3 = Northeastern region. 4 = Northwestern region. 5 = Northern to the north (Weingartner et al., 1999; region. Further details on the characteristics of each area are provided in the text. Pisareva et al., 2015, in this issue), and

136 Oceanography | Vol.28, No.3 two canyons—Herald and Barrow, with present permanently, forming a cyclonic flow are the highest in our study area. depths of up to 120 m—are located in water flow circulation in the southern Bering Strait is characterized by rel- the northern portions of the western and part of the Chukchi Sea (Sirenko and atively high bottom water tempera- eastern areas, respectively, at the edge of Gagaev, 2007). The second is that there tures in summer (~4°C), with fast near- the continental slope (Dobrovolsky and is a variable current that reverses peri- ​bottom currents coincident with coarse- Zalogin, 1982; Weingartner et al., 1999). odically between the East Siberian and grained bottom sediments. The Chukchi Sea is characterized Chukchi Seas (Münchow et al., 1999; AREA 2: The southern part of the by intense hydrodynamics, with cur- Weingartner et al., 2005). Chukchi Sea is relatively shallow (<50 m rent speeds ranging from 15–75 cm s–1, The current flowing northward deep). The influence of Pacific waters is depending on location (Woodgate et al., through Bering Strait is well mixed and highest here, with above 0°C bottom water 2005; Weingartner et al., 2005, 2013). has high nutrient content. As the cur- temperatures during the ice-free season. There are two main currents. The Alaska rent moves northward, it slows down Current speeds are lower at this site than Coastal Current (ACC) generally flows and spreads out north and northwest in Bering Strait further south, result- northward along the Alaskan coast of the strait, resulting in enhanced pro- ing in a mixture of mud and sand frac- toward Barrow Canyon (Aagaard and duction in the southern Chukchi Sea tions, with some intermixing of coarser Carmack, 1989; Walsh et al., 1989), and (Weingartner et al., 2005). Bering Strait sediments (S. Denisenko et al., 2015, and it advects Alaska Coastal Water (ACW) and southern Chukchi Sea waters are Pisareva et al., 2015, both in this issue). into the region. ACW is present from rich in organic matter, driven by both AREA 3: This region is influenced by May to about the end of December the high nutrient inflow water support- ACW in the coastal areas to the east, with (Woodgate and Aagaard, 2005). Bottom ing high seasonal in situ production as depths of less than 20 m. It has large con- water temperatures can reach 10°C over well as advected organic carbon from the centrations of coarse-grained sediments the shallow southeastern portions of south (Feder et al. 2005, 2007; Grebmeier mixed with boulders and rocks near the the Chukchi Sea. By comparison, the et al., 2006, 2015; Hirawake et al., 2012). capes (e.g., Cape Lisburne). bulk of the water transiting the Chukchi Although soft sediments dominate the AREA 4: This region in the south- Sea (>80%) is a combination of Anadyr seafloor in this region, coarse-grained western part of the Chukchi Sea includes Water and Bering Shelf Water that mixes sediments are found in some areas of the Long Strait, the coastal waters of Russia, through the Bering Strait to form Bering Chukchi Sea. Their distribution is related and the offshore waters of the Chukchi Sea Water (BSW; Coachman et al. 1975; to variable current flow and transport Sea north to 70°N. This shallow area is Weingartner et al., 2005; Woodgate et al., within ice, with subsequent deposition of characterized by predominantly below 2005). BSW during summer is colder heavier particles when the currents slow 0°C bottom water temperatures, and (about 2°–4°C) and saltier (>31.8) than down and the ice melts. The most favor- coastal erosion that is the source of the ACW (T >4°C and S<31.8) (Weingartner able habitats for bryozoans are coarse fine-grained sediment that dominates the et al., 2005). Topographic shoals in the bottom sediments, which mainly occur seafloor in this region and that is not suit- northern Chukchi Sea split the north- near capes, in Bering Strait, in near- able for bryozoan settlements. ward flow of BSW into three branches. shore coastal areas, and with patchy dis- AREA 5: This region is located in One branch flows east toward Barrow tribution in the Chukchi Sea (Kosheleva the northern Chukchi Sea. It covers the Canyon, one flows west through Herald and Yashin, 1999). coastal waters around Wrangel Island Canyon, and the other flows between To evaluate the similarity of local and the offshore regions of the Chukchi the shoals via the Central Channel bryozoan fauna among different sites Sea extending to 73°N and eastward (Woodgate et al., 2010; Weingartner and to identify the biogeographic sta- to Barrow Canyon. Compared to the et al., 2013; Danielson et al., 2014). tus of the species within the Chukchi other sites, Area 5 as a whole is char- In the extreme southwestern Chukchi Sea as part of an MDS analysis, we acterized by a significant variation in Sea, the seasonal Siberian Coastal assigned each station to one of five areas depths that reach 100–150 m in the can- Current (SCC) flows southward along (Figure 1) based on habitat descriptions. yons. Bottom water temperatures in both the coast in some years (Weingartner These areas, summarized below, differ in shallow and deep waters in this region et al., 1999, 2013). This cold, fresh SCC environmental conditions that include are low, often dropping to negative val- (bottom water temperature 0°–1.5°С) thermal regime, duration of ice cover, ues (Weingartner et al., 2013). Although may occasionally reach the Bering Strait, hydrodynamic activity, and grain size soft sediments exist in this area, rocks but it is usually deflected into the cen- of bottom sediments. and mixed sediments that include peb- tral Chukchi Sea. There are two opin- AREA 1: The most distinctive area ble and gravel fractions form local sub- ions about outflow from the East Siberian is the Bering Strait region, where the regions (Kosheleva and Yashin, 1999; Sea in the SCC. One is that the flow is influence of Pacific waters and current Grebmeier et al., 2006).

Oceanography | September 2015 137 TABLE 1. Taxonomic structure of bryozoan fauna of the Chukchi Sea. RESULTS

TOTAL GENERA FOR EACH FAMILY WITH ASSOCIATED General Characteristic of FAMILY NUMBER OF SPECIES IDENTIFIED IN PARENTHESES Bryozoan Fauna Adeonidae Adeonella (1) The present study increased the num- Alcyonidiidae Alcyonidium (9), Alcynioides (1) ber of bryozoan species identified in the Annectocymidae Entalophoroecia (2) Chukchi Sea from 187 (N. Denisenko, Aspidostomatidae Reussinella (1) 2008; N. Denisenko and Kuklinski, 2008) Bitectiporidae Schizomavella (2), Hippomonavella (1), Hippoporina (6) to 204. These species belong to 87 genera, Bugulidae Bugula (1), Crisularia (1), Dendrobeania (9), Semibugula (1), Bugulopsis (2) 40 families, three orders, and two classes Callopora (5), Cauloramphus (3), Tegella (8), Bidenkapia (2), Septentriopora (1), Calloporidae Doryporella (1), Amphiblestrum (2) (Table 1). Five families (Calloporidae, Candidae Caberea (1), Notoplites (1), Scrupocellaria (2), Aquiloniella (2), Tricellaria (5) Bugulidae, Candidae, Lepraliellidae and Celleporidae Celleporina (3), Buffonellaria(1) Smittinae) were the richest in species Cerioporidae Borgella (2), Fungella (1) composition (Table 1). The most diverse Cheiloporinidae Cheiloporina (3) fauna were found within four genera: Cribrilinidae Membraniporella (1),Cribrilina (2) Alcyonidium, Tegella, Dendrobeania, and Crisiidae Crisiella (1), Crisia (5), Diplosolen (2) Rhamphostomella (Table 1). Cryptosulidae Harmeria (1) Electridae Einhornia (2) Local or α-Diversity and Its Escharellidae Escharella (5), Hincksipora (1), Hemicyclopora (1) Relation to Environmental Eucrateidae Eucratea (4) Parameters Exochellidae Escharoides (1) Bryozoan species richness varied from Fascigeridae Fasciculiporoides (1) one to 89 species per station. Higher diver- Flustrellidridae Flustrellidra (3) sity (from 30 to 89 species) was found at Flustridae Carbasea (2), Serratiflustra (1), Securiflustra(1), Hincksina (1), Terminoflustra(1) stations located near capes, regardless of Gigantoporidae Cylindroporella (1) sampling gear, but in most samples, the Hippothoidae Hippothoa (1), Plesiothoa (1), Celleporella (2) number of species varied from one to five. Lepraliellidae Lepraliella (1), Hippoporella (2), Rhamphostomella (10) Changes in bryozoan species richness Lichenoporidae Lichenopora (1), Patinella (2), Disporella (2) at the local level were not significantly Microporellidae Microporella (3) related to changes of depth, but there Microporidae Microporina (1) was a trend of increasing species richness Myriaporidae Myriapora (2), Myriozoella (2) with bottom water temperature (Table 2). Oncousoeciidae Oncousoecia (3), Proboscina (1) There was also no significant relationship Plagioeciidae Plagioecia (2) of α-diversity of bryozoan richness with Porellidae Porella (13), Cystisella (3) a latitudinal gradient (Table 2), but there Romancheinidae Arctonula (1) was some trend toward increasing bryo- Schizoporellidae Schizobrachiella (2) zoan richness longitudinally, from west to Smittiniidae Smittina (6), Smittoidea (1), Parasmittina (4) east in the Chukchi Sea (Table 2). Stomachetosellidae Stomachetosella (6), Pachyegis (2), Lepralioides (1) Teuchoporidae Phylactella (1) Regional or γ-Diversity and Its Tretocycloeciidae Tetrocycloecia (1) Relation to Environments Tubuliporidae Tubulipora (3), Diaperoecia (1), Bathysoecia (3) As noted above, analysis of material col- Umbonulidae Umbonula (1), Ragionula (1), Posterula (1) lected during RUSALCA cruises in 2009 Vesiculariidae Amathia (2), Vesicularia (1) and 2012 increased the number of iden- TABLE 2. Correlation analysis of bryozoan diversity at individual stations (α-diversity) with envi- tified bryozoan species to 204 (Table 1). ronmental and geographic parameters. However, applying the Chao2 index for PEARSON estimating the number of expected spe- CORRELATION cies within this group indicates that the PARAMETER VALUE p-LEVEL Chukchi Sea bryozoan fauna could con- Depth 0.11 0.156 tain 264 ± 20 species. Assessment of spe- Bottom water temperature 0.33 0.016 cies richness by the rarefication method Latitude 0.02 0.850 (Clarke and Warwick, 1994) indicates Longitude 0.37 0.000 that the curve of changes in the number

138 Oceanography | Vol.28, No.3 250 were not significantly correlated with a regional level, we compared the five 200 those parameters (Figure 3b and 3c, Chukchi Sea areas in our study with respectively). However, bryozoan spe- neighboring seas (East Siberian and 150 0–20 21–60 cies richness increased significantly with Bering Seas) and the Canadian Arctic 100 2 61–140 longitude from west to east (R = 0.25; Archipelago. Using the MDS method, p < 0.01; Figure 3e). the results indicate that the southern part yozoan species number 50 0–140 Br of the Chukchi Sea (Area 2), the Bering 0 020406080 100 120 140 Differential or β-Diversity Strait (Area 1), and the eastern part of the Number of samples The level of similarity of species com- FIGURE 2. Station-based rarefication position at different depths indicated curves of bryozoan species richness in r 120 that at a similarity level of 13%, calcu- a

the Chukchi Sea (average curves from 100

900 permutations). Depth range (m) is lated as the average value for the matrix, n umbe 80 shown by different symbols and colors. there are two different bathymetric com- 60 pecies plexes of bryozoan species in the Chukchi s 40 Sea (Figure 4): (1) the shallow complex, 20 of species, even including all the collec- covering almost all the waters of the sea Bryozoan 0 0–9 tions from stations in the Chukchi Sea, (depth <100 m), and (2) the deeper sub- 10–1920–2930–3940–4950–5960–6970–7980–8990–99 100–110 has not approached the asymptote, sug- littoral faunal complex found deeper than Depth (m) 160 gesting that there are still bryozoan spe- 100 m in canyons and at the edge of the r b 140 cies to be found (Figure 2). Examination continental shelf. The 45% level of simi- 120 numbe of bryozoan species richness at different larity separates nearshore (0–20 m) from 100 es water depths indicates that most bryo- offshore (>20 m), and shelf (20–50 m) ci 80 pe zoan species occur at 20–60 m depth, a from canyons and upper slope (50–100 m) s 60 40 range that covers most of the Chukchi (upper branches of Figure 4). 20 Bryozoan Sea (Figure 2). However, species richness The level of similarity of bryozoan spe- 0 2 3 4 5 6 7 –0 >7 0<1 1≤ 2≤ 3≤ 4≤ 5≤ 6≤ is low at depths less than 20 m (particu- cies composition among selected areas <–1.5 –1 Bottom water temperature (°C) larly in the eastern Chukchi Sea along the of the Chukchi Sea (see Figure 1) was Alaska coast) as well as in deeper areas also evaluated by MDS, coincident with 120 c within the canyons and troughs with results from the similarity cluster anal- 100 depths >60 m (Figure 2) and the upper ysis. The calculations indicate the pres- 80 slope regions likely due to the small num- ence of two faunistic complexes at a 45% 60 ber of stations that were sampled at these dissimilarity level (Figure 5). One com- s pecies number 40 depths. It is possible that since most of plex is composed of stations in the south- 20 the samples were collected at depths from ern and eastern parts of the sea, includ- Bryozoan 0 20 m to 60 m, a region supporting the ing Bering Strait (Areas 1–3), and the 12345678 maximum diversity of bryozoans, our second complex is composed of stations Sediment typ e data are biased by the inequity of sam- in the remainder of the sea and extend- 140 d 120 pling at shallower depths (Figure 3a), as ing to the shelf edge (Areas 4 and 5). could also be the case with α-diversity Subsequently, using ANOSIM to test dif- 100 80 that focused on depths of 30 m to 50 m. ferences between predetermined regional

species number 60 Most bryozoan species were found in groups indicated that the level of their 40 the temperature range from 1°C to 2°C difference is high, although barely signifi- 20 Bryozoan and on mixed muddy-sand and pebble-​ cant (R = 0.875; p = 0.06). 0 65 66 67 68 69 70 71 72 gravel bottom sediments, although they In order to evaluate biodiversity on Latitude (°N ) 120 e FIGURE 3. Variation of regional diversity of bryozoans within the Chukchi Sea along the general 100 environmental gradients of (a) depth, (b) bottom water temperature, and (c) sediment types, and 80 along the geographical gradients of (d) latitude and (e) longitude (R = 0.51; p <0.01) in the Chukchi 60 species number Sea. The line in (e) is the trend in variation of the bryozoan fauna. Types of sediments in (c): 1 = Mud 40 with clay (0.005–0.1 mm). 2 = Muddy or fine sand (0.1–1.0 mm). 3 = Coarse sand (2–3 mm). 4 = Sand 20 0 with small pebbles and gravel (1–5 mm). 5 = Pebbles, gravel (5–20 cm). 6 = Shells with gravel and Bryozoan sand (1–5 cm). 7 = Stones, boulders, rocks (>20 cm). 8 = Rocks with pebbles. Sediment data were 176 178 180 –178 –176 –174 –172 –170 –168 –166 –164 –162 obtained from Kosheleva and Yashin (1999) and ZIN RAS data sets. Longitude (°)

Oceanography | September 2015 139 Resemblance: S17 Bray Curtis similarity Chukchi Sea (Area 3) form a common cluster with the Bering 11-20 Sea bryozoan fauna at a 45% similarity level (Figure 6). The 6-10 western (Area 4) and northern (Area 5) parts of the Chukchi 0-5 Sea form a separate cluster that shows low similarity with the 50-100 Bering Sea bryozoan fauna as well as with the bryozoan fauna 31-50 of neighboring Arctic regions, specifically the East Siberian Depth Interva l 21-30 Sea and the Canadian Arctic Archipelago (Figure 6). Testing 100-200 the differences between station clusters using ANOSIM indi- 0 20 40 60 80 100 Similarity (%) cates a high level of difference between these groupings FIGURE 4. Bathymetric complexes of bryozoan species of the Chukchi (R = 0.675; p = 0.005) Sea. The red line divides the shallow shelf complex from the deeper sublittoral faunal complex. Biogeographic Composition of the Bryozoan Fauna of the Chukchi Sea and Its Change Along Environmental Gradients Resemblance: S17 Bray Curtis similarity Biogeographic characteristics of bryozoan species in the Resemblance: S17 Bray Curtis similarity Area 1 2D Stress: 0 Similarity Area 1 Chukchi Sea were evaluated by analyzing geographical distri- 2D Stress: 0 Similarity 47 47 bution data in the world ocean (see Materials and Methods section). We determined that 204 species found in the Chukchi Sea can be attributed to 12 biogeographic catego- Area 2 ries (Table 3). Boreo-Arctic species that have a wide range Area 2 Area 5 dominated all other bryozoan species in the study. No boreo- Area 5 Arctic bryozoan species of Atlantic origin were found in the Chukchi Sea, whereas boreo-Arctic bryozoans of Pacific ori- Area 3 Area 3 gin made up about 17% of the whole faunal group. By com- parison, the majority of boreal species (60%) was of Pacific Area 4 origin. Arctic bryozoans were mainly represented by circum- Area 4 polar species (>50%). The numbers of Arctic and boreal spe- cies in the Chukchi Sea were roughly equal (31 and 30 species, FIGURE 5. Bryozoan complexes inhabiting the Chukchi Sea. Area 1 = Bering Strait region. Area 2 = Southern region. Area 3 = Northeastern respectively; Table 3). region. Area 4 = Northwestern region. Area 5 = Northern region. The text Rather than providing a detailed analysis of the formation contains further details on the characteristics of each area. of modern bryozoan fauna in the Chukchi Sea here, we com- bined categories in Table 3 into three main groups for further analysis: Arctic, boreal, and boreo-Arctic. The latter two cate- gories mainly describe the biogeographic status of the Chukchi

Resemblance: S17 Bray Curtis similarity Resemblance: S17 Bray Curtis similarity Bering Sea 2D Stress: 0.11 Similarity Bering Sea 2D Stress: 0.11 Similarity TABLE45 3. Biogeographic composition of bryozoan fauna 45 of the Chukchi Sea. Area 3 Area 3 Area 1 Area 1 BIOGEOGRAPHIC SPECIES NUMBER PORTION CATEGORY ACCORDING OF EACH WITHIN TO GOLIKOV (1982) CATEGORY CATEGORY Area 2 Area 2 Arctic, Circumpolar 17 53.1% Canadian Arctic Archipelago Canadian Arctic Archipelago Arctic, Amerasian 6 18.8% Area 5 Area 5 Arctic, Eurasian 9 28.1% Boreal, Pacific 8 25.0% High Boreal, Pacific 20 62.5% East Siberian Sea East Siberian Sea Area 4 Area 4 Amphiboreal 4 12.5% Subtropic-Arctic 3 2.1%

FIGURE 6. Species composition similarities in subareas of the Chukchi Boreo-Arctic, Widespread 72 51.4% Sea compared with neighboring Arctic seas. Area 1 = Bering Strait High Boreo-Arctic, Circumpolar 31 22.2% region. Area 2 = Southern region. Area 3 = Northeastern region. Area 4 = Boreo-Arctic, Pacific, Circumpolar 3 2.1% Northwestern region. Area 5 = Northern region. The text contains fur- ther details on the characteristics of each area. High Boreo-Arctic, Pacific 31 22.2%

140 Oceanography | Vol.28, No.3 Sea. We found that proportions were not Also, a comparison of our bryozoan data Chukchi Sea and that it will be compa- constant in the five different Chukchi with published information on other fau- rable to bryozoan richness of the south- areas of our study (Figure 7), and regres- nal groups (Piepenburg et al., 2011) indi- ern part of the sea (Figure 7). This south- sion analysis (Figure 8) indicated that cates that despite fewer stations with bryo- ern area is most influenced by bryozoan the most significant relationship was for zoan records (136 stations), the current larvae carried into the region by Pacific boreal species that occur where bottom level of bryozoan diversity in the Chukchi waters (Bering Sea Water, Alaska Coastal water temperatures vary. Sea is comparable to the level of poly- Current) through Bering Strait (Aagaard Changes in the ratio of boreal to chaete diversity (77.4%). However, both and Carmack, 1989; Walsh et al., 1989; Arctic species indicated the dominance groups are still less studied than other Woodgate and Aagaard, 2005). of boreal species in the southern part of fauna, such as mollusks, arthropods, and Comparison of the total number of the Chukchi Sea (Areas 1 and 2) and in echinoderms, where nearly 90% of the bryozoan species identified in the Chukchi the coastal zone of the Alaskan Arctic species are known. Sea with those found in other Arctic seas (Area 3; Figures 1 and 7). In addition, Higher bryozoan diversity may be indicates that they are nearly equal in tax- two small regions dominated by boreal expected in the eastern part of the onomic richness (Gontar and Denisenko, bryozoans were found in the northern Chukchi Sea (Area 3) where, despite 1989; Gontar 2001, 2004; N. Denisenko, and western areas of the Chukchi Sea a larger number of samples, bryozo- 2008, 2010). The most diverse families (Areas 4 and 5; Figure 7). The biogeo- ans were not identified as to their spe- in the Chukchi Sea are also common in graphic boundary between the boreal cies (Feder et al., 2005, 2007; Grebmeier the Arctic Ocean (Table 1); however, the and the Arctic regions is located where et al., 2006). It is expected that bryozoan bryozoan fauna in the Chukchi Sea differs the ratio of boreal and Arctic species is species richness is higher in the eastern from Arctic Ocean fauna in the higher 50:50 (N. Denisenko, 1990). Mapping of the proportions of boreal to Arctic 100 species in the Chukchi Sea indicates a boundary that divides the southern and 72˚N

on on 80 eastern areas from the western and north- on ny ern areas of the Chukchi Sea (Figure 7). Wrangel 60

Island tic (%)

ny Ca Herald Barrow Ca Point Barrow 70˚N Long Str DISCUSSION Chukchi Sea eal/Arc 40 ait 5 Point Franklin Bor Bryozoan Fauna Diversity Icy Cape Because bryozoan fauna of the Chukchi 3 20 Cape 68˚N 4 Cape Lisburne Sea remains understudied, knowledge of Schmidt Alaska 0 their distribution patterns is limited. The Point Hope present study is the most comprehen- sive investigation of bryozoan ecological Chukotka 2 66˚N Peninsula Cape Kotzebue diversity in the Chukchi Sea ever under- Serdtse Sound Kamen’ taken. Sampling during the RUSALCA 175°E 155°W 180°E 1 2004 to 2012 cruises increased our doc- 160°W 175°W 165°W umentation of bryozoan species richness 170°W by 14%, resulting in a total of 204 spe- FIGURE 7. Predicted proportion of boreal and Arctic species of bryozoans and biogeo- graphic boundary (solid black line) between the Arctic and the North Boreal Pacific biogeo- cies identified overall. Despite the high graphic zones corresponding to the 50:50 ratio of boreal to Arctic species. Subareas 1–5 number of bryozoan samples collected to are separated by dashed black lines; the subarea dominated by Arctic species within the date, expected species richness is still low area of stable, on average, cyclonic water circulation is indicated by the solid red line. (Chao2 = 264 species). As indicated by

bryozoan species accumulation curves, the r most poorly studied regions are at depths 12 10 FIGURE 8. Number of less than 20 m and deeper than 60 m. Our boreal bryozoan species 8 work found the maximum diversity of in relationship to bottom bryozoans in the Chukchi Sea at 20–60 m 6 water temperatures (°C) 4 in the Chukchi Sea (R = depth; however, because most of the ben- boreal species numbe 0.63; p <0.09). thic samples were collected at depths of 2 30–50 m, our findings may be biased rela- 0 Bryozoan 012345678910 tive to the less sampled shallower depths. Bottom water temperature (°C)

Oceanography | September 2015 141 portion of boreal and boreo-Arctic spe- and their composition should be sen- with low similarity to bryozoans in the cies with Pacific origin that occur due to sitive to multiple environmental fac- southern Chukchi Sea areas, the Bering the strong influence of Pacific waters. The tors. However, our analysis of variations Sea further south, and the coastal waters Chukchi Sea bryozoan fauna is charac- in bryozoan species richness at small of the East Siberian Sea and Canadian terized by a larger number of species in localities (α-diversity) in the Chukchi Arctic Archipelago. the families Flustrellidridae, Electridae, Sea indicated significant positive trends Hippothoidae, and Microporellidae that only with longitude and bottom water Biogeographic Aspects inhabit mainly the boreal regions of the temperatures (Table 2). Traditionally, the description of the bio- shelf seas of the world ocean (Osburn, Latitude has also been suggested as geographic regionalization of the Chukchi 1950, 1952, 1955; Dick and Ross, 1988; a moderator for epifaunal megazoo- Sea is based on comparative studies of Grischenko, 2002). The Chukchi Sea is benthos, and it is considered an indi- regional fauna of different areas (species a transitional area between the Pacific rect indicator of some environmental fea- or biotic regionalization) and their evolu- boreal and the Arctic biogeographic tures characteristic of the Chukchi Sea tionary adaptation to their specific envi- regions, just as the Barents Sea is a tran- (e.g., water mass type, primary produc- ronments (Filatova, 1957; Golikov et al., sitional area between the Atlantic boreal tion) impacting bottom fauna (Bluhm 1989; Briggs, 1995). Another approach to and the Arctic biogeographic regions. But et al., 2009; Nelson et al., 2014). Bryozoan analyzing the spatial-geographic distri- there are considerably fewer bryozoan species variation was spatially high, and bution of zoobenthos is community-level species in the Chukchi than in the Barents our study indicates that latitude as well or biocenotic regionalization, where the Sea (N. Denisenko, 1990). The differ- as longitude are important indicators of importance of species differs with respect ence is due not only to the geographic environmental variation (e.g., bottom to quantitative characteristics of the zoo- positions of the seas and the origins of water temperatures). Although a direct benthos (e.g., biomass and/or abundance; their associated water masses but also to relationship between bryozoan diversity Feder, 2005, 2007; Grebmeier et al., 2006; a much greater variety of biotopes in the and most environmental parameters was Blumn, 2009; Day et al., 2013) and the Barents Sea, its greater depth and width, not observed, the presence of five bathy- lower trophic taxa (e.g., microbes and and its deeper straits through which warm metric bryozoan complexes, determined plankton, Nelson et al., 2014). Population Atlantic Water enters the sea. at a 45% similarity level, can reflect the changes due to natural and anthropo- The ecological importance of spa- influence of variable environmental fac- genic impacts primarily take place at the tial diversity is related to the determi- tors. This finding may be explained by the species level, which can be regarded as the nation of key factors that influence the high variability of environmental charac- most sensitive. To understand how fauna biological diversity over different spatial teristics over small spatial scales (Aagaard will respond to an impact, we should scales. One of the most important find- and Carmack, 1989; Walsh et al., 1989; know what changes can be expected and ings of terrestrial and aquatic biodiver- Weingartner et al., 1999; Woodgate we should understand the state of an eco- sity studies of the temperate latitudes et al., 2010). Comparison of our results system prior to any impact, so knowl- was the determination that many animal with macrozoobenthic studies in differ- edge about biogeographic regionalization and plant taxonomic groups decrease in ent parts of the Arctic shelf systems sup- (zonation) will be very useful for map- species richness from the tropics to the ports the presence of variable relation- ping ecosystem status and trends. There is poles, as well as with increasing depth ships of bottom fauna with environmental no unique opinion about biogeographic in the ocean (Buzas and Culver, 1991; gradients (Feder et al., 1994; Grebmeier regionalization of the Chukchi Sea Kendall and Aschan, 1993; Kendall, 1996; et al., 2006; Conlan et al., 2008). Variation even in the most recent faunal reviews Gray, 1997; Gray et al., 1997; Clarke and in the Sørensen similarity coefficients (Mironov, 2013; Petryashov et al., 2013). Lidgard, 2000; Crame, 2000; Culver and (β-diversity) also results from the com- Bryozoans are sessile animals that Buzas, 2000; Roy et al., 2000; Włodarska- plex effect of environmental heterogene- have limited dispersal ability because the Kowalczuk et al., 2004; Clarke and Crame, ity. The presence of two major bryozoan planktonic larvae of a majority of species 2010; Josefson et al., 2013). A similar lat- assemblages located in both the south- are lecithotrophic (lipid-rich), a charac- itudinal trend has been observed in the ern and the northern parts of the Chukchi teristic that can be used as a reasonable Chukchi Sea for megabenthos richness Sea is a result of large-scale physical fac- parameter for determining biogeographic (Bluhm et al., 2009). Moreover, depth and tors, specifically in our case the Pacific zonation in Arctic seas. The bryozoan sediment type are two important factors water masses that have reduced influence fauna of the Chukchi Sea are mainly that influence small-scale species compo- and more complexity in the northern por- characterized as allochthonous (originat- sition (α-diversity; Grebmeier et al., 1989; tions of the Chukchi Sea. The remain- ing outside of the local area). The major- Kostylev et al., 2001). Bryozoans form der of the northern bryozoan assem- ity of bryozoan species are widely distrib- epibenthic attached faunal assemblages, blage in our study is self-maintained, uted (boreo-Arctic elements) and include

142 Oceanography | Vol.28, No.3 a large number of species with Pacific ori- United States, as part of the boreal Pacific zone. This hypothesis is supported by our gin (boreo-Arctic and boreal elements) zone and the remainder of the Chukchi study’s MDS analysis, which indicates that most likely penetrated into the Sea toward the north as a transitional low similarity between the northern part Chukchi Sea in the late Pleistocene after zone between the boreal and Arctic bio- of the Chukchi Sea and the East Siberian the opening of Bering Strait. During the geographic regions. A similar region is Sea and Canadian Arctic Archipelago. In thermal maxima in the Holocene, heat characterized by an epibenthic commu- general, our view that the northern part output of water temperatures was lower nity dominated by Pacific species (Bluhm of the Chukchi Sea is transitional between than at present, which caused penetra- et al., 2009). Our results support the stud- Arctic and boreal zones does not con- tion of Pacific waters, and Pacific boreal ies that suggest the southern part of the tradict the research on mollusks, crus- and boreo-Arctic species with them, far Chukchi Sea is part of the boreal zone taceans, and echinoderms (Petryashov into the northwest up to the Laptev Sea. and, in addition, we propose an extension et al., 2013). However, station-by-station Also, Arctic fauna occupied the Chukchi of the boundary toward the northeast analysis of species composition revealed Sea after the glaciers receded and with near Point Franklin, Alaska. This pro- several small localities in the northern increasing sea level resulting from melt- posed extension is supported by results of Chukchi Sea where boreal bryozoan spe- ing periods before thermal maxima biocenotic research on macrozoobenthos cies were dominant, likely the result of (Golikov and Scarlato, 1989; Dunton, that reflect a sharp change in community interannual variability and intense inflow 1992; Petryashov, 2002, 2009). At present, structure not far from Point Franklin at of Pacific waters into the Chukchi Sea. atmosphere-ocean interactions and cur- Icy Cape (Blanchard et al., 2013a,b). The The distribution of zoobenthos is rent flow directly influence the spreading location of a boundary in the US sector of closely related to changes in environmen- of Arctic species south and boreal species the central Chukchi Sea also corresponds tal characteristics (e.g., Feder et al., 2005; north into the Chukchi Sea. to a known hydrographic front located Grebmeier et al., 2006; Hirawake et al., The transition in benthic community just north of Icy Cape (Feder et al., 1994). 2012). When unsuitable environmental composition or ecotone is discrete in Therefore, according to bryozoan distri- conditions occur, some bryozoan spe- the Chukchi Sea due to changes in water butions, the biogeographic boundary in cies either become sterile or their repro- masses and sediment types. The result is the Chukchi Sea begins just south of Cape ductive functions are depressed. Thus, that dramatic ecological differences are Serdtse-Kamen’ and extends north to boreal as well as Arctic species can sur- found in closely spaced communities over 69°00'N and then northeast to just above vive in areas where bottom water tem- a scale of a few tens of kilometers (Day Point Franklin (Figure 7). The features of peratures vary greatly and may warm et al., 2013). The transitional zone(s) of our proposed revised Chukchi Sea bio- above 4°C. However, the temperature epibenthic communities occurs around geographic boundary are similar to those range for reproduction is more limited, 71°N, 166°W, an area in the northeastern of the Barents Sea, the other boreal to (Golikov and Scarlato, 1972) although part of the Chukchi Sea where bottom Arctic transitional sea, where the bound- reproduction will occasionally occur water temperatures range from 2°C to ary also reflects a 50:50 ratio of Arctic to when water masses warm to optimal val- 4°C (Blanchard et al., 2013a,b). Analyses boreal species (N. Denisenko, 1990) that ues, even for brief periods (Kaufman, carried out using either the biotic or the corresponds to the largest bottom water 1977). A similar situation can occur for species approach indicate a wider transi- temperature range observed in that sea Arctic species in areas where tempera- tional zone, although its exact location has (S. Denisenko, 2013). Again, our results tures are higher than optimal for them. not yet been established. Mironov (2013) indicate that where great variability in Earlier reviews of Arctic phylogeography suggests that the boundary between the bottom water temperatures are observed (Weider and Hobæk, 2000; Hardy et al., Arctic and boreal Pacific biogeographic seasonally, a variety of the bryozoan 2011) described observations of a gla- regions is not a discrete line, but instead fauna are adapted to these oscillations cial refuge in the southern Chukchi Sea. it corresponds to a wide transitional zone (Figure 7). The bryozoan biodiversity The occurrence of low bottom water tem- that occupies half of the Chukchi Sea, variations observed in the Chukchi Sea peratures just north of Bering Strait (the from Cape Schmidt on the Chukotka are also likely due to the relative youth of area indicated by the red line in Figure 7) Peninsula coast of Russia to Point Barrow the fauna and the variable environmental within the southern portion of the Pacific on the Alaskan coast of the United States, conditions in this region. boreal biogeographic zone (area bounded with the remainder of the Chukchi Sea The remainder of the Chukchi Sea by the solid line in Figure 7) supports the belonging to the Arctic zone. Petryashov located north of the boundary delineated finding that Arctic bryozoans are domi- et al. (2013), by comparison, regard the in Figure 7 is dominated by Arctic bryo- nant in this area. In comparison, the high southern part of the Chukchi Sea from zoan species that are distinct from other bryozoan species richness in the Pacific Cape Serdtse-Kamen’ on the Chukotka neighboring Arctic regions, but it should boreal biogeographic zone surround- Peninsula, Russia, to Point Hope, Alaska, nevertheless be regarded as a transitional ing this Arctic patch is also characterized

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Sirenko for bryozoan sample col- of the USSR. Izdatel’stvo Akademii nauk SSSR, http://dx.doi.org/10.1007/s12526-010-0059-7. lections during cruises carried out in the RUSALCA Moscow-Leningrad, 582 pp. [in Russian] Pisareva, M.N., R.S. Pickart, K. Iken, E.A. Ershova, project. Research was supported by the Russian Kosheleva, V.A., and D.S. Yashin. 1999. Bottom J.M. Grebmeier, L.W. Cooper, B.A. Bluhm, C. Nobre, Academy of Sciences (Project N 01201351181, “Fauna Sediments of the Arctic Seas of Russia. R.R. Hopcroft, H. Hu, and others. 2015. The rela- and ecology of invertebrates of the Russian east- VNII Oceangeologia, St. Petersburg, 286 pp. tionship between patterns of benthic fauna and ern Arctic seas and neighbouring areas”). Financial Kosobokova, K.N., R.R. Hopcroft, and H.J. Hirche. zooplankton in the Chukchi Sea and physical forc- support was provided by the US National Oceanic 2011. Patterns of zooplankton diversity through ing. Oceanography 28(3):68–83, http://dx.doi.org/​ and Atmospheric Administration Arctic Office to the depths of the Arctic’s central basins. Marine 10.5670/oceanog.2015.58. J. Grebmeier for RUSALCA synthesis activities via Biodiversity 41:29–50, http://dx.doi.org/10.1007/ Roy, K., D. Jablonski, and J.W. Valentine. 2000. NOAA Cooperative Agreement #NA09OAR4320129: s12526-010-0057-9. Dissecting latitudinal diversity gradients: WHOI CINAR #19930.00 UMCES. We are very Kostylev, V.E., B.J. Todd, G.B.J. Fader, R.C. Courtney, Functional groups and clades of marine bivalves. thankful to the two anonymous reviewers who G.D.M. Cameron, and R.A. Pickrill. 2001. Benthic Proceedings of the Royal Society B 267:293–299, made constructive comments and suggestions that habitat mapping on the Scotian Shelf based on http://dx.doi.org/10.1098/rspb.2000.0999. improved the manuscript. multibeam bathymetry, surficial geology and sea Scarlato, O.A. 1981. Bivalves of the Temperate Waters floor photographs. Marine Ecology Progress Series of the Northwestern Part of the Pacific Ocean. 219:121–137, http://dx.doi.org/10.3354/meps219121. Nauka, Leningrad, 480 pp. [in Russian] AUTHORS Kuklinski, P., and P.D. Taylor. 2006. A new genus Sirenko, B.I., and S.Y. Gagaev. 2007. Unusual abun- Nina V. Denisenko ([email protected]) is Senior and some cryptic species of Arctic and boreal dance of macrobenthos and biological invasions Researcher, Zoological Institute of the Russian calloporid cheilostome bryozoans. Journal of in the Chukchi Sea. Russian Journal of Marine Academy of Sciences, St. Petersburg, Russia. the Marine Biological Association of the United Biology 33:355–364, http://dx.doi.org/10.1134/ Jacqueline M. Grebmeier is Research Professor, Kingdom 86(5):1,035–1,046, http://dx.doi.org/​ S1063074007060016. University of Maryland Center for Environmental 10.1017/S0025315406014019. Sørensen, T.A. 1948. A new method of establish- Science, Chesapeake Biological Laboratory, Kuklinski, P., P.D. Taylor, and N. Denisenko. ing groups of equal amplitude in plant sociology Solomons, MD, USA. 2007. Arctic cheilostome bryozoan species based on similarity of species content and its appli- of the genus Escharoides. Journal of Natural cation to analysis of vegetation on Danish com- History 41:219–228, http://dx.doi.org/10.1080/​ mons. Kogelige Danske Videnskabernes Selskab ARTICLE CITATION 00222930601162878. Biologiske Skrifter 622(5):1–34. Denisenko, N.V., and J.M. Grebmeier. 2015. Spatial Magurran, A. 2004. Measuring Biological Diversity. Walsh J.J., C.P. McRay, L.W. Coachman, J.J. Goering, patterns of bryozoan fauna biodiversity and issues Blackwell Publishing, Oxford, 256 pp. J.J. Nihoul, T.E. Whitledge, T.H. Blackburn, of biogeographic regionalization of the Chukchi Mironov, A.N. 2013. Biotic complexes of the Arctic P.L. Parker, C.D. Wirick, P.G. Shuert, and others. Sea. Oceanography 28(3):134–145, http://dx.doi.org/​ Ocean. Invertebrate Zoology 10(1):3–48. 1989. Carbon and nitrogen cycling within the 10.5670/oceanog.2015.62. Münchow, A., T.J. Weingartner, and L.W. Cooper. Bering/Chukchi Seas: Source regions for organic 1999. The summer hydrography and surface cir- culation of the East Siberian Shelf Sea. Journal

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