The aim of this study was to assess the distribution and biodiversity of bryozoans in Scotland, using a combination of mapping techniques and biodiversity indices. The results provide baseline data on Scottish bryozoans and highlight the regions and habitats that remain poorly studied.
Ecological insight into the distribution and diversity of bryozoans is somewhat confounded by variations in data quality and availability. The MESH-EUNIS data layers have a fairly coarse resolution because of underlying limitations in seabed substratum data from the British Geological Survey. Resolution is lowest in coastal areas (0–3 m) and on rocky substrates, both of which contain a high proportion of the bryozoan records. Moreover, the layers are based on a predictive model and therefore may not accurately represent the benthic habitat of all areas. This, along with the fact that the location of many bryozoan records is only approximate, and that the benthic habitat varies over a relatively small spatial scale, means that the species numbers in each marine zone may not be fully representative of the true distribution of bryozoans in Scotland. It may well be expected that given the modest sampling effort, bryozoan diversity is underestimated in almost all locations.
The inclusion of museum specimens in the present dataset provides information on the historical state of diversity. Museum data has the advantage of being able to confirm species identifications. The date of museum specimens, however, can be misleading, reflecting the date when the specimen was registered, rather than collected. Furthermore, changes in taxonomic usage and place names, and imprecisely defined locations or sampling methods can restrict comparisons of present day and historical data. Alternatively, present-day survey data will tend to provide accurate information on the location, date and depth of sampling; however, specimens are rarely retained, preventing the identification being checked at a later date.
Comparison of diversity (as measured by AvTD/VarTD) with other studies, and therefore ecological interpretation of the results, is limited, as few studies have considered the relationship of AvTD/VarTD to physical characteristics of the environment (e.g. Ellingsen et al. 2005). Fewer still have considered the average taxonomic distinctness of bryozoans (e.g. Rowden et al. 2004). Some insight may be gained by considering factors that influence species number, but it is unclear whether species richness and AvTD/VarTD are governed by similar environmental parameters. Preliminary work shows that species richness and taxonomic distinctness relate to different environmental gradients (Ellingsen et al. 2005; Heino et al. 2005). Assemblages with lower species richness do not necessarily have a lower AvTD than those of many other species, e.g. when there is a limited number of species, but the species represent a broad phylogenetic range.
Despite these problems, the results give an indication of the broad-scale patterns in bryozoan occurrence and enable the identification of localities and habitats that represent future sampling priorities in Scotland.
The location of bryozoan records largely mirrors the MNCR sampling sites, suggesting that the observed distribution reflects a greater sampling intensity on the west coast and the archipelagos of Shetland, Orkney and the Western Isles. Few species have been recorded from offshore areas, and again this is likely to reflect a bias towards sampling coastal areas, which are both easier and cheaper to access.
Patterns of offshore versus near-shore species richness remain ambiguous, with several studies finding fewer species in offshore shallow benthic areas compared with near-shore areas (e.g. Barnes 2000), and others finding the reverse of this pattern (Schopf 1969). Offshore seamounts in the north of Scotland may be expected to support bryozoan species, as they provide suitable substrate and are generally associated with high primary productivity and current speeds (Rogers, 1994). There are so few records of offshore bryozoans in the present study that no conclusions can be drawn regarding offshore versus coastal patterns.
Limited surveys have been conducted in areas of the eastern and northern coasts where bryozoans appear to be absent. Potentially, therefore, the distribution of bryozoans reflects underlying differences in the marine environment. Norman (1869) notes that within the British Isles, bryozoan species that are typical of the Mediterranean region can colonise higher latitudes on the west coast than on the east coast. He attributes this to the influence of the Gulf Stream on the west coast, which results in higher temperatures and a more stable temperature regime on the western coast of Scotland (Bennett & Covey 1998a). Temperature has previously been suggested as an important factor in determining the bryozoan assemblages in the English Channel (Hayward & Ryland 1978), Norway (Ryland 1963) and Hawaii (Soule et al. 1988). Many bryozoan species have a narrow temperature tolerance, and variation in temperature impacts growth rates and tolerance to salinity (Dick et al. 2006). In addition to temperature differences, water in the east of Scotland can become highly stratified in the summer, with a lack of vertical mixing (Dyer et al. 1983). This results in a restricted supply of nutrients to the photic zone, and low primary productivity (McIntyre 1961). It may therefore be expected that little organic material reaches the seabed. In contrast, strong winds on the west coast generally prevent stratification in the summer (Lee 1981) and hence there is a greater availability of phytoplankton to bryozoans. The availability of phytoplankton as a food source is thought to be important in determining bryozoan distribution (Best & Thorpe 1983, 1986; Pratt 2008) and may, in part, be responsible for differences between the west and east coast. Alternatively, differences between the two coasts may not be ecological, but instead represent evolutionary trends, with Lusitanian species having had insufficient time to colonise the east coast.
The number of species present in the different MESH-EUNIS marine zones gives a further indication of the potential factors influencing bryozoan distribution in Scotland. Bryozoans are typically expected to inhabit intermediate energy zones where there is some degree of shelter (Ryland 2005). Currents and wave exposure will influence bryozoans through impacts on food supply, attachment ability and substrate-mediated effects (Cabioch 1968; Dick et al. 2006). The greatest number of bryozoan species in Scotland are from high-energy, rather than intermediate energy, environments, and the greatest biodiversity (AvTD) is within low-energy environments. The three energy zones have similar numbers of bryozoan records, such that sampling should have less of an influence on the number of species. However, the energy layer of the MESH-EUNIS model is constructed only from information on tidal currents and excludes any measure of wave exposure. High energy, therefore, represents areas of strong or very strong tidal currents with unknown exposure. If wave action were to be incorporated, our understanding of the distribution and diversity of bryozoans across the different energy zones might differ.
Currents will also affect the distribution of bryozoans through their influence on substrate availability and heterogeneity. For all marine species, environmental heterogeneity is one of the strongest correlates of species number (Huston 1994), and peaks in bryozoan species number have been found previously to correspond to increased substratum heterogeneity (Hayward & Ryland 1978; Clarke & Lidgard 2000). Rock, as defined by the MESH-EUNIS model, includes a range of substrates available for bryozoans to colonise, such as rocks and biogenic reefs. Kelp and other species that may be colonised epizooically by Bryozoa will also be available on rocky substrata. In contrast to the results presented here, the greatest number of boreal species has generally been encountered on coarse sediments (Eggleston 1972; Kuklinski et al. 2005); however, biodiversity (AvTD, rather than species number) of bryozoans in Scotland was found to be highest on coarse sediments. This further emphasises the need for greater sampling of coarse and mixed sediments in Scotland. The lack of available substratum may be a determining factor influencing low species number on the north coast of Scotland. North of the mainland, there are large areas of sediment and only one sea loch (Bennett & Covey 1998b), therefore much of the area is likely to be unsuitable for bryozoan colonisation.
Both the availability and heterogeneity of substratum, and current strength will vary with depth. The MESH-EUNIS biozones GIS layer indicates the depth at which Bryozoa have been recorded. The greatest numbers of species have been recorded from the infralittoral zone; however, this category has more than 10 times the number of records as any other zone. The diversity measured by AvTD is highest in the deep circalittoral.
Overall, it is likely that a variety of physical factors contribute to the observed patterns of bryozoan distribution in Scotland and between different marine habitats. It is necessary to ensure that sufficient sampling has been undertaken to eliminate sampling bias as an explanatory factor for bryozoan occurrence. Gaining a better idea of substrate, temperature and exposure differences between sub-regions and offshore and coastal areas will allow for further explanation of the observed patterns. As seabed maps improve in the future, it will be possible to establish the patterns in bryozoan distribution with greater confidence.
Spatial patterns in bryozoan diversity
The average taxonomic distinctness was calculated for all sites with 10 or more species and from Scottish sub-regions as an index of biodiversity. Depth alone appeared to have little influence on bryozoan diversity. However, the range in diversity values was less variable in deeper waters, which may be due to the lower number of records. Substrate, currents, temperature and food availability vary with depth, and these are factors that are known to influence bryozoan assemblages (Eggleston 1972; Hayward & Ryland 1978; Hughes 2001; Kuklinski et al. 2005). The AvTD of bryozoans in New Zealand was found to vary with depth, peaking between 10 and 40 m in areas consistent with high habitat heterogeneity (Rowden et al. 2004). Similarly, Ellingsen et al. (2005) concluded that the relationship between AvTD and depth for soft-sediment macrobenthos in the Norwegian continental shelf was due to depth-related differences in the abundance and variation of habitat types. Although it is generally expected that habitat heterogeneity will vary with depth due to reduced light and wave scour, this is not necessarily the case in Scotland. In addition, the diversity within the MESH-EUNIS biozones suggests that habitat heterogeneity is influential for bryozoan diversity. Diversity peaks in the deep circalittoral zone (Table 2), which is defined as starting at the maximum depth that the seabed is influenced by waves, and extending to 200 m (Coltman et al. 2008). This zone will tend to be diverse with a variety of substrates including gravel, shingle, cobbles and shells, typically with a low silt content and reduced wave scour (Connor et al. 2004). It is also possible that the lack of a relationship between diversity and depth is the result of the limited depth data available for sampling sites and lack of sampling from deeper water locations.
Bryozoan biodiversity varied across Scotland, with a concentration of high values in Orkney and West Scotland. Both of these regions contain sites in which the bryozoan fauna has an AvTD significantly higher than the expected regional mean. Lower biodiversity values were widely spread across the region, from Shetland to the Clyde Sea, and were significantly lower than the expected regional mean in Shetland and West Scotland. The concentration of sites with a high diversity in Orkney may reflect the variety of habitats present in this area. As discussed above, habitat heterogeneity is a major factor influencing diversity. Additionally, the stable temperature regime and the availability of sheltered areas with strong tidal currents in Orkney (Bennett & Covey 1998a) are likely to contribute to the high diversity of the area. Hiscock & Breckel (2007) found that the AvTD for benthic assemblages, including species of Bryozoa, was highest in Scottish sea loch environments, followed by island habitats, and similarly attributed this to the variety of habitats that these environments provide. Orkney is made up of 70 islands and has many sea lochs; this is likely to contribute to the higher than expected values of AvTD found for bryozoans in Orkney. Likewise, the West Scotland sub-region has many of these habitat types.
At a regional scale, values of biodiversity of the MNCR sub-regions did not show much variation. The greatest diversity was in the Rockall sub-region, followed by the Clyde Sea and the Outer Hebrides. The lowest values were in North Scotland, which has only one sealoch, and Shetland. Regional patterns for bryozoans were similar to those described by Hiscock & Breckel (2007) for benthic assemblages, who found the highest AvTD at sites within the Northwest Scotland, West Scotland and the Outer Hebrides MNCR regions.
Neither the diversity of individual sites nor the diversity of sub-regions shows any cline with latitude. Latitudinal patterns have generally only been considered in terms of species richness and little work has been done on the relationship between average taxonomic distinctness and latitude. Furthermore, poleward clines in species richness appear to be taxon-specific. For example, Ellingsen et al. (2005) found that the AvTD of annelids, crustacean and molluscs (combined) decreased with latitude on the Norwegian continental shelf, yet if annelids alone were considered, AvTD increased with latitude. Any interpretation of species gradients is confounded by similar latitudinal gradients in the physical characteristics of the environment (Narayanaswamy et al. 2010). A more detailed study of bryozoans, possibly over a greater latitudinal range, would be necessary to decipher any relationship.
Temporal patterns in bryozoan diversity
Temporal patterns in the diversity of bryozoans were assessed by calculating the AvTD for each time period. AvTD varied over time, peaking between 1792 and 1849, and then again between 1975 and 2000 (Table 3). AvTD was lowest in the present time period (2000–2010). The greatest diversity (AvTD) was associated with the fewest number of species and records. It is likely that during this early time period, a few conspicuous intertidal bryozoans would have been collected. In the intertidal zone the key members of the bryozoan community most likely to be encountered will represent a very broad phylogenetic range. An example of a typical sample could be the Ctenostome Flustrellidra hispida, the Cheilostome Electra pilosa and the Cyclostome Crisia denticulata. This would give a species richness of 3, which is low; however, the AvTD for this would be high due to each species belonging to a different Order. From 1850 to 1949, sampling effort increased due to the activities of the British Dredging Association. More species would have been collected, increasing the species richness and number of records. Additional species will of necessity belong to one of the three Orders sampled from the intertidal example in the previous time period. It follows then that large increases in the AvTD would not be expected.
With the current data it is not possible to separate genuine temporal changes in Scottish bryozoan diversity from the effects of an uneven spread of records across the time periods and changes in methods of collecting and identifying specimens. Additionally, the geographical range of records in each time period is not equal. This means that the biodiversity for one time period may not be comparable with that of another time period. Data were insufficient to calculate the AvTD for each time period in each of the Scottish sub-regions, which would have helped to overcome this problem. A more thorough search of historical records, including other museum collections, may yield more data and enable a more robust assessment of diversity through time, in the future.
Implications and recommendations
The data presented here provide baseline information on the distribution and diversity of bryozoans in Scotland, which is a vital prerequisite for conservation and environmental monitoring. The identification of sites with a high biodiversity may be used to identify priority sites for protection and conservation.
However, it is important not just to value sites of high diversity. Sites with a low AvTD may represent a small number of closely related species, but those species may be ecologically rare. For example, few species are present in tide-swept faunal communities, yet the species that are able to tolerate such conditions, such as Alcyonidium diaphanum and Flustra foliacea, may be considered to be valuable. Benedetti-Cecchi (2004) noted that the identity of the species in an assemblage, rather than a diversity index, may be needed to make inferences on ecosystem function. The distribution of bryozoans must, therefore, also be considered in terms of individual species, rather than just the broad-scale patterns.
Taxonomic distinctness, like other indices, does not capture all aspects of diversity. Most notably, AvTD measures based on presence–absence data do not account for the abundance of species within an assemblage. Not only were abundance data not available for many of the bryozoan records, but the quantification of abundance for modular or colonial animals is problematic and varies across studies (Mckinney & Jackson 1989). It is, therefore, likely that policy decisions based on biodiversity assessments will need to make use of a variety of diversity measures, including taxonomic distinctness and species richness, to capture fully all aspects of diversity.
The sensitivity of AvTD, and its application in environmental monitoring, still remains uncertain. Salas et al. (2006) found that only total, not average, taxonomic distinctness was satisfactory in determining disturbed situations, and AvTD was less sensitive than other commonly used diversity measures. Furthermore, Heino et al. (2005) found that the AvTD varies along natural gradients, thereby reducing its ability to discriminate between the effects of human disturbance and natural variability.
The availability of regional species pool data is a basic requisite for the application of AvTD to biodiversity assessment but it cannot be certain that the regional species pool, here assumed to be bryozoans of the Celtic and North Sea, is truly representative. Comparisons of Scottish fauna to that of other regions are therefore limited. Moreover, a fully resolved phylogenetic framework is not available for bryozoans, and relatedness is based on the somewhat arbitrary Linnaean classification system (Warwick & Clarke 1995). For bryozoans, as with most phyla, certain groups have received more taxonomic attention than others. In particular, the taxonomy of cyclostomes remains unclear (Waeschenbach et al. 2009). This results in a truncation of the hierarchy towards the more studied groups. Weighting taxonomic ranks on a linear scale is also somewhat arbitrary, and it must be remembered that the AvTD is an index that provides only a relative measure of biodiversity, for use in comparing areas, rather than providing an absolute measure.
Despite these problems, AvTD is one of only a few indices that make historic, diffusely collected species lists amenable to valid biodiversity analysis. As the historic dataset for Scottish bryozoans represents a significant proportion of the total dataset (~2300 records), and a common aim of biodiversity assessment is to understand temporal changes, it is important that these historical data are included in analysis and not simply ignored because of the limitations of sampling effort. While limitations in taxonomy may limit comparisons between Scotland and other regions, and between Bryozoa and other Phyla, comparisons between sites within Scotland should give a reasonably accurate indication of spatial differences in diversity within Scotland.
The present analysis highlights the need to maintain meticulous records and transparency across institutions. Recent EU and UK legislation aim to make data collection consistent and improve accessibility. In particular, the EU Inspire Directive (2007) focuses on maintaining spatial data and improving transparency across agencies.