Biodivers Conserv (2010) 19:39914002 DOI 10.

1007/s10531-010-9942-6 ORIGINAL PAPER

Habitat loss and possible effects on local species richness in a species-poor system: a case study of southern Baltic Sea macrofauna
Maria Wodarska-Kowalczuk Jan Marcin Wesawski Jan Warzocha Urszula Janas

Received: 5 May 2010 / Accepted: 21 October 2010 / Published online: 9 November 2010 Springer Science+Business Media B.V. 2010

Abstract The effects of habitat loss on local species richness depend on the characteristics of the endangered system (including its total species pool and the distribution of species among the habitats). The present study focuses on the species-poor southern Baltic marine benthic biota. Macrobenthic samples were collected in three habitats: (1) soft bottom covered with vegetation; (2) stony reefs; (3) unvegetated sands. Fourty one percent of 54 observed macrozoobenthic species were habitat specic, while 30% occurred in all three habitats. There were no signicant differences in total species richness among the three habitats. The accumulation curves plotted for subsets of data with selected habitats excluded lay below the curve plotted for the whole dataset, but only in one case the 95% condence intervals of the subset curve did not overlap with those plotted for the whole dataset. The exclusion of samples from selected habitats produced a species richness drop ranging from 9 to 13%. The present study showed that habitat loss in a species-poor area with a relatively large ratio of generalist species cannot produce local species richness declines similar to those predicted for diverse marine systems. However, it must be emphasized that in species-poor systems, the loss of ecological function accompanying habitat loss could be disproportionally higher than that predicted based on decreases in species richness, as some functions are performed by a single species. Keywords Biodiversity Habitat loss Macrozoobenthos Baltic Sea

M. Wodarska-Kowalczuk (&) J. M. Wesawski Institute of Oceanology PAS, Powstancow Warszawy 55, 81-712 Sopot, Poland e-mail: maria@iopan.gda.pl J. Warzocha Sea Fisheries Institute, Koataja 1, 81-332 Gdynia, Poland U. Janas Institute of Oceanography, University of Gdansk, Pisudskiego 46, 81-378 Gdynia, Poland

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Introduction Habitat heterogeneity and structural complexity are among the main drivers of biodiversity on both local and regional scales (Rosenzweig 1995). Habitat degradation is one the greatest threats to marine biodiversity (Airoldi and Beck 2007; Gray 1997; Dulvy et al. 2003). Habitat destruction can result in the extinction of marine species on local, regional, or global scales (Dulvy et al. 2003; Roberts and Hawkins 1999; Wolff 2000). McKinney and Lockwood (1999) predicted that the massive destruction of natural habitats on a global scale will lead to biotic homogenization and a decrease in global biodiversity. The rate and magnitude of habitat loss in the seas are comparable to those documented in terrestrial systems (Roberts and Hawkins 1999). For example, it was estimated that 5080% of the original wetlands and seagrass areas in Europe were lost due to human activities between 1960 and 1995 (Airoldi and Beck 2007). While the dramatic loss of complex marine habitats has been widely recognized, the effects of habitat loss on marine biodiversity has attracted much less attention than it has in the literature on terrestrial ecology (Airoldi et al. 2008). Despite growing concern regarding the scale of ongoing habitat destruction, there have been few attempts to document (and/or quantify) the effects of this process in the marine realm (Airoldi et al. 2008). Studies published to date mostly focus on single habitats and small-scale experiments that cannot be extrapolated to large-scale processes (e.g. Reed and Hovel 2006). Direct observations of the large-scale effects of habitat alternations are rare as they require long monitoring data series of both habitat and biota characteristics (but see Wolff 2000 and Graham 2004). There is an urgent need for a better understanding of the possible effects of habitat loss to support the management and conservation of marine natural resources (Airoldi et al. 2008). The effects of habitat loss depend on the characteristics of the endangered system; the impact on diversity can vary depending on the available species pool and/or the level of species habitat specicity (Thrush et al. 2006). An understanding of the processes operating across regions with different natural species pools is essential for marine diversity management and conservation (Elmgren and Hill 1997). The ecosystem effects of habitat loss can be especially severe in species-poor systems where the functional redundancy of species is low and even small decreases in species richness can induce dramatic changes in ecosystem functioning (Micheli and Halpern 2005). This paper presents the results of a study conducted in the Baltic Sea, which is a marine system of extremely low natural biodiversity, a semi-enclosed brackish sea connected to the North Sea only through the narrow Danish straits. The low species diversity of the Baltic biota has been attributed to low salinity (Elmgren and Hill 1997) and/or the relatively young geological age of the sea, which has been in its present state for no longer than 8,000 years (Bonsdorf 2006). Local diversity decreases along the sea axis/salinity gradient (from around 20 PSU in the Kattegat to below 2 PSU in the northernmost Bothnian Bay, Lepparanta and Myrberg 2009). The low natural biodiversity is also threatened by strong anthropogenic pressure created by extensive nutrient enrichment, pollution, overexploitation and physical disturbance (Elmgren and Hill 1997; Karlson et al. 2002; HELCOM 2009). Baltic Sea habitats have been listed on the Red List of Marine and Coastal Biotopes of the Baltic Sea (Nordheim and Boedeker 1998), which rates 83 habitats as endangered (68%) or heavily endangered (15%) by habitat destruction or signicant alteration. Thrush et al. (2006) predicted that habitat loss would not strongly effect local species richness in species-poor systems with high ratio of generalist species. In the current study, we focus on the species-poor southern Baltic macrozoobenthic communities and address two key questions for local biodiversity conservation: (1) how biodiversity is distributed

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across different habitats, and (2) if habitat loss will affect regional species richness. Benthic samples from three low diversity habitats are used to document variations in alpha diversity across habitats, the ratio of habitat-specic species, the species accumulation rates for each of the habitats, and estimations are made of whether the loss of any of the present habitats would signicantly decrease local species richness.

Methods Study area The present study was conducted in the Polish exclusive economic zone (Polish EEZ), which is a shallow subtidal area of the southern Baltic Sea, in the coastal waters between Ustka and Gdansk. The shallow subtidal area comprises the seaoor to depths of 25 m, which corresponds roughly to the extent of the summer thermocline (Piechura 1985) and the euphotic zone. Three basic habitats occur in the shallow sublittoral of the Polish EEZ: (1) soft bottom covered with vegetation (VEG); (2) stony reefs (STONY); (3) relatively homogenous and unvegetated sands (SANDY). VEG habitats were sampled in Puck Bay, which is sheltered from the open sea by the Hel Peninsula. Water exchange with the open Gulf of Gdansk is hampered by a belt of sandbar shallows that emerge periodically. The soft bottom is covered with underwater meadows composed of the vascular plant species Potamogeton spp., Zanichellia palustris, seagrass Zostera marina and green algae Chara spp. The macrozoobenthos is dominated by Cerastoderma glaucum (that makes up in average 43% of total benthic abundance and 42% of total benthic biomass) and two species of gastropods Hydrobia ventrosa and Hydrobia ulvae (comprising on average 30 and 22% of total benthic abundance and biomass, respectively). STONY habitats were sampled in the Supsk Bank and at the Czopino Shallows. The Supsk Bank is an elevated area of sea oor (minimum depth 8 m) located about 25 km to the north of the central Polish coast. About 80% of the bank is covered by almost at plains of sand and gravel deposits that occur on the washed-out surface of the till in the northwestern part of the bank at depths between 8 and 20 m. The stony-boulder substrate is concentrated on the north-west side of the bank (Andrulewicz and Wielgat 1999). The stones are covered with blue mussels (Mytilus edulis) and macroalgae, mostly red algae (Furcellaria lubricalis) and lamentous brown algae (Pilayella littoralis and Ectocarpus siliculosus) that are present to depths of 16 m (Andrulewicz et al. 2004). The macrozoobenthic community is dominated by Mytilus edulis (that makes up to 90% of the total benthic biomass and 70% of total benthic abundance and can occur with densities exceeding 3000 ind m-2), Balanus improvisus and Gammarus salinus (present study and Warzocha 1995). The Czopino Shallows are another area of raised sea oor in coastal shallows (with a minimum depth of 18 m) located in the nearshore area north of Stilo and Ustka. SANDY bottoms were sampled in the Gulf of Gdansk and offshore around Stilo. The Macoma balthicaMya arenaria macrozoobenthic community inhabits the whole area of the shallow sandy bottom along the Polish coast to depths of around 2025 m which approximately corresponds to the boundary between the sandy and the muddy soft bottoms in the western part of the Gulf of Gdansk and to the depth of summer termocline in Polish EEZ (Warzocha 1994, 1995).

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Table 1 Sampling details for the habitats studiednumber of samples, depths etc Habitat Depth range [m] 18 1021 524 Number of stations 111 39 68 Number of samples 264 150 186 Sampling gear

Vegetated soft bottom Stony reefs Sandy bottom

mK (53), VV (38), Ek (173) mK (150) VV (186)

Values in brackets indicate numbers of samples collected with a given gear in a given habitat Sampling gears: mK modied Kautsky sampler, VV van Veen grab, Ek Ekman grab

Fig. 1 Location of sampling stations in the Polish exclusive economic zone. Symbols represent the three studied habitats: SANDY homogenous and unvegetated sands, VEG soft bottom covered with vegetation, STONY stony reefs

Sampling and data analysis A total of 600 macrobenthic samples were collected at 218 stations located in the three different habitats (Table 1, Fig. 1). The stations were randomly spread to cover the whole extent of the studied habitats/localities. Samples were collected in summer seasons of 20052008. Three types of sampling gears were used to collect macrofauna: two types of grabs and scuba-diver operated modied Kautsky sampler. The grabs included van Veen grab with sampling area of 0.1 m2 (230 samples), Ekman grab with sampling area of 0.0225 m2 (173 samples). Two hundred and three samples were taken with use of modied Kautsky sampler with a catch area of 0.04 cm2 as described by Andrulewicz et al. (2004) (Table 1). Samples were collected with use of Kautsky sampler in the STONY habitat. Only van Veen grabs were used at the SANDY stations, while all three gears were used for sampling VEG fauna. Grabs and diver operated Kautsky sampler are gears that target infauna or epifauna, respectively, thus both groups were included in the collected materials. Macrobenthic invertebrates were identied to the lowest possible taxonomic level. Chironomidae larvae and semi-pelagic mysids were not included in the analysis. Oligochaeta were not identied to lower taxonomic level and therefore they were also excluded from the dataset used for statistical analysis.

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Habitat-specic species were dened as species occurring only in samples taken in that habitat and generalists were species that occurred in all three habitats. Differences in alpha species richness dened as number of species per sample (S) between groups of samples collected in the three habitats were identied using one-way ANOVA. Post-hoc comparative pair wise tests were performed using Tukeys test. Species accumulation curves permit comparing the diversity of faunal assemblages at comparable levels of sampling effort. Species accumulation curves of the observed numbers of species (Sobs) were computed for the three habitats studied. Computing 95% condence intervals (using the formulae by Colwell et al. 2004) allows for a statistical comparison of the species richness of the two data sets, i.e., the differences are not signicant at P \ 0.05 if the 95% condence intervals overlap (Colwell et al. 2004). Chao2, a non-parametric estimator of the true species richness, was applied to the data. The Chao2 estimator is based on the concept that rare and uncommon species carry information about the number of species missing in samples: Chao2 = Sobs ? Q2/2Q2, 1 where Q1 and Q2 are the numbers of species that occur in just one or two samples (uniques and duplicates). Along with log-linear 95% condence intervals (as described by Colwell et al. 2004), both Sobs and Chao2 were computed using EstimateS (Colwell 2005). To nd out how the loss of one of the habitats present in the studied area would inuence the local species richness, subsets of data were prepared by excluding samples collected at one habitat; thus, three subsets were created with VEG, SANDY, or STONY excluded. Species accumulation curves along with 95% condence intervals were computed for each of the subsets, which permitted comparing statistically the species richness of the subsets and of the original dataset containing all the samples. The predicted species richness drop associated with habitat loss was dened as SRdrop = (dSobs/ totSobs) 9 100, where dSobs is the difference between the mean values of Sobs of the whole material (totSobs) and of Sobs of the data subset, which were both recorded on species accumulation curves at the last sample of the subset curve.

Results Twenty-two species (41%) were specic to only one habitat; 9 were specic for vegetated soft bottoms, 7 were specic for sandy bottoms and 6 were specic for stony reefs (Table 2). Habitat specic species made 24% of all species noted in VEG samples, 21% in STONY samples and 19% in SANDY samples. Most of the habitat-specic species were rare as they occurred in less than 25% of the total number of samples collected in the respective habitats. The exceptions were the amphipod, Gammarus tigrinus, that occurred in 29% of samples collected in VEG habitat, as well as the atworm, Procerodes litoralis, and the polychaete, Bylgides sarsi, that occurred with a frequency of 80 and 28%, respectively at STONY and SANDY stations (Table 2). Sixteen species (30%) occurred in all three habitats; thus, they could be dened as generalists (Table 3). Generalists made 43% of all species noted in VEG samples, 55% in STONY samples and 44% in SANDY samples. Sixteen other species occurred in two of the three studied habitats. There were signicant differences in S (representing alpha species richness) among the studied habitats (ANOVA F = 29, P \ 0.001, Fig. 2). Post-hoc pairwise tests showed that there were signicant differences between all pairs of habitats in S (Tukey test, P \ 0.05). Mean S varied from 7.6 in SANDY to 9.7 in STONY samples. S was signicantly lower in samples taken with Ekman grabs and modied Kautsky sampler than in those taken with van Veen grabs.

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3996 Table 2 Species specic for only one habitat VEG Gammarus tigrinus Lekanesphaera hookeri Radix balthica Rhithropanopeus harrisii Lekanesphaera rugicauda Gammarus duebeni Heterotanais oerstedti Palaemon adspersus Palaemon elegans F[%] 29 8 8 2 2 1 1 0 0 SANDY Bylgides sarsi Diastylis rathkei Pontoporeia femorata Saduria entomon Corophium lacustre Eurydice pulchra Manayunkia aestuarina

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F[%] 28 6 3 3 2 1 1

STONY Procerodes litoralis Melita palmata Planaria torva Dendrocoelum lacteum Piscicola geometra Calliopius laeviusculus

F[%] 80 19 12 6 3 1

Frequency of occurrence of the species in a given habitat is presented (F, 0 indicates F \ 0.5%) VEG vegetated soft bottom, SANDY sandy bottom, STONY stony reef

Table 3 Generalists (species occurring in all three habitats) and frequences of their occurrence in the three habitats

Species

VEG F[%] 6 5 95 10 19 8 90 88 49 0 9 65 42 42 14 42

SANDY F[%] 6 19 54 41 6 14 97 61 2 6 2 98 81 66 35 97

STONY F [%] 92 5 2 13 87 92 68 70 53 89 5 6 2 11 99 36

Balanus improvisus Bathyporeia pilosa Cerastoderma glaucum Corophium volutator Electra crustulenta Gammarus salinus Hediste diversicolor Hydrobia ulvae Idotea chelipes Jaera albifrons Leptocheirus pilosus Macoma balthica Marenzelleria neglecta Mya arenaria

VEG vegetated soft bottom, SANDY sandy bottom, STONY stony reef (0 indicates F \ 0.5%)

Mytilus edulis Pygospio elegans

The Chao 2 estimate of the true species richness of the area studied indicated 55 species and 54 species were noted in the material analyzed, which was within the 0.95 condence interval of the estimate (from 54 to 62, Fig. 3). The total number of macrobenthic species noted was 37 in the VEG, 36 in the SANDY, and 29 in the STONY habitats and these values lay within the 0.95 condence intervals of Chao2 estimates of the total species richness for each habitat. Ninety ve percent condence intervals plotted for the accumulation curves representing the three habitats overlapped indicating that there were no signicant differences between the three habitats at P \ 0.05 (Fig. 4). For example, for the

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Biodivers Conserv (2010) 19:39914002 Fig. 2 Mean (0.95 condence intervals) numbers of species per sample (S) in samples taken in three habitats. For VEG habitat the values for groups of samples taken with the three different gears are also presented (Ek Ekman grab, vV van Veen grab, mK modied Kautsky sampler)

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Fig. 3 Species accumulation curves plotted for the observed number of species (Sobs) and the true number of species estimated using Chao2. Sobs and Chao2 are plotted with 0.95 condence intervals. For the clarity of the graph, only values for every tenth sample are presented

150th sample, the 0.95 condence intervals for VEG extended from 31 to 39, for STONY from 26 to 32 and for SANDY from 32 to 38. The exclusion of the VEG habitat produced SRdrop = 13%, for SANDY SRdrop = 11%, and for STONY SRdrop = 9%. However the comparison of species accumulation curves plotted for the whole dataset and for subsets of data showed that only exclusion of samples collected in VEG habitat produced a signicant difference in total species richness. (Fig. 5). The 95% condence intervals of STONY and SANDY excluded subsets curves did overlap with 95% condence intervals plotted for the whole dataset indicating no signicant differences in observed species richness at P \ 0.05.

Discussion Modeling and observational studies of New Zealand soft-bottom macrofauna indicated that the magnitude of the impact of habitat loss on species richness is related to the ratio of habitat-specic species and to species richness variation among the habitats (Thrush et al. 2006). Thrush et al. (2006) stated that the impact of habitat loss is stronger when the ratio of generalist species is lower and the variation of habitat species richness is greater. The

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Fig. 4 Species accumulation curves for the three habitats. Sobs are plotted with 0.95 condence intervals. For the clarity of the graph, only values for every tenth sample are presented. The mean 0.95 condence intervals for the whole dataset are also presented (only for the rst 270 samples)

Fig. 5 Species accumulation curves for subsets of data (produced by excluding samples taken at one of the habitats). Sobs are plotted with 0.95 condence intervals. For the clarity of the graph only values for every tenth sample are presented. The mean 0.95 condence intervals for the whole dataset are also presented (only for the rst 450 samples)

ratio of generalists in the dataset presented (30%) is much higher than the values recorded in a study of two New Zealand localities (6%), in which only different soft-bottom habitats located within small areas (of 5 and 10 km extent) were studied (Thrush et al. 2006). The difference in the generalists ratios between the Baltic Sea and the New Zealand benthic systems would probably be even larger if comparable datasets (in terms of both spatial extent and the scale of the structural variation of the habitats) were available. The variation of species richness on the habitat scale was negligible in the study area as comparisons of species accumulation curve yielded no signicant differences at P \ 0.05. The communities associated with the three habitats differ in species composition and alpha diversities,

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but these differences were not translated into the differences in species richness examined on the habitat scale. The southern Baltic Sea macrofauna has a relatively high ratio of generalist species and reduced variation in habitat species richness. The drop in estimated species richness with habitat removals ranged from 9 to 13%, and only exclusion of VEG habitat produced signicant difference in regional species richness. These effects contrast to the those expected for New Zealand fauna by Thrush et al. (2006) who recorded loss of 22 and 31% of species. The small changes in species richness in the present study suggest that habitat loss in a species-poor area with a relatively large ratio of generalist species and little between-habitat variation cannot produce local species richness declines similar to those predicted for diverse marine systems, as predicted by Thrush et al. (2006). Sources of bias in comparative diversity studies of different habitats can stem from the various habitat-specic sampling techniques applied. In the VEG habitat, two sampling techniques were employed to get a comprehensive representation of benthic species richness in this structurally complex habitat. Grabs for infauna sampling and scuba-diver operated Kautsky samplers for epibenthic biota sampling were both used. To get as complete a picture as possible of the species pools in these habitats, a large number of samples were included that had been taken with an Ekman grab sampler that has a smaller sampling area that does the standard van Veen sampler. While this difference had little impact on density records (unpublished data), the alpha species richness was much lower in samples collected with Ekman sampler than they were with the van Veen sampler. The total number of species collected was very close to the estimated total given by the non-parametric Chao2 estimator. The overlap of the 0.95 condence limits conrmed no statistical difference between Sobs and Chao2 accumulation curves and both curves appeared to approach an asymptote at about 150 sample. This suggests that with a total number of 600 samples it was possible to document the local species richness of the area studied, and a reasonable diversity estimate may be available if about 150 samples are collected. The numbers of species recorded in the habitats studied were slightly higher than or similar to those reported by studies based on a smaller sampling effort. Andrulewicz et al. (2004) noted 28 species, while Warzocha (1995) noted 18 species on the Slupsk Bank, the main sampling area for the STONY habitat in the current study, as compared to 29 species observed in the present study. Warzocha (1995) reported 22 taxa for the Macoma balthica and Mya arenaria community inhabiting the SANDY habitat (as compared to 36 species recorded in the present study), while 37 species were documented in the VEG habitat of the inner Puck Bay by Wiktor (1993) (37 in the present study). These authors applied similar sampling methods to those used in the present study: Andrulewicz et al. (2004) used Kautsky sampler, Warzocha (1995) took samples with use of van Veen grab, while Wiktors (1993) study was based on a material collected with use of Petersen, Ekman and van Veen grab samplers. The present study encompassed three habitat in Polish EEZ. Most species that were shown to be generalists in the present study are widespread and common species across other habitats and regions of the Baltic Sea. M. balthica, M. arenaria, M. edulis, B. improvisus, H. diversicolor as well as other species listed in Table 3 were noted among the most common species e.g. in Lithuanian and Estonian coastal Baltic Sea waters, each species occurring in a number of different habitats (Kotta and Moller 2009; Olenin and Daunys 2004; Veber et al. 2009). The majority of species specic to only one habitat in our study were rare in terms of frequency of occurrence. Both in terrestrial and marine systems the distribution of species range sizes is typically right-skewed with a large proportion of species restricted to a small number of sites (Gaston 1994). The ecological processes driving the rare species

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distribution patterns are not fully understood. It can be questioned if the rare species are actually habitat specic or if they arent found in the other habitats because of the insufcient sampling effort. Ellingsen et al. (2007) have recently shown that the number of rare species was related to a number of epibenthic habitats which suggests that rare species in marine benthic environments are habitat-related rather than randomly distributed. It may be that commonly observed positive relationship between regional species richness and habitat diversity may be largely driven by habitat-specic rare species (Ellingsen et al. 2007). Habitat degradation is usually produced by transition from a more complex to a less complex habitat such as may occur if, for example, seagrass bed is dredged or damaged by changes in water quality. The transformation from a less complex to a more complex habitat does not occur naturally without active habitat restoration (Airoldi et al. 2008). The largest (and the only signicant) decrease in species richness was observed for the dataset that excluded VEG samples and the vegetated soft bottom is also actually the most endangered among the three studied habitats. The drastic decrease of both species richness and biomass in Puck Bay vegetation was caused by eutrophication between the 1970 and 1990s (Plinski and Florczyk 1993). The stony reefs in the Polish EEZ are located in the open sea, and while they are not greatly threatened by drastic eutrophication or pollution (Herbich and Warzocha, 1998), they could be destroyed by commercial mineral exploitation (Andrulewicz and Wielgat 1999). Habitat loss can have a profound impact not only on species numbers, but also on community functioning. It has been demonstrated that communities associated with seagrass and macroalgae are much more productive in comparison to communities inhabiting less structurally complex habitats such as sandy bottoms (Duffy 2006). The simplication of habitats leads to the simplication of trophic food webs (Graham 2004). The loss of ecological function accompanying habitat loss could therefore be disproportionally higher than that predicted based on decreases in species richness (Dobson et al. 2006; Wesawski et al. 2009). This might be especially relevant in species-poor regions, such as the Baltic Sea, where some functions are performed by a single species and the loss of one species can mean losses of whole functional groups (Elmgren and Hill 1997). The effects of the loss of structurally complex habitats can also have ramications that reach beyond the destroyed habitat and its associated biotic communities, when important ecosystem services, such as shelter and nursery areas for invertebrates and sh, water turbity control, buffers from waves and storms, sediment stabilization, etc. are lost altogether (Airoldi et al. 2008; Bostrom and Bonsdorff 1997; Bostrom et al. 2006). The STONY habitat in the study area serves as herring spawning and cod feeding grounds (Andrulewicz and Wielgat 1999). SANDY bottom communities provide important ecosystem functions related to oxygenation, organic matter mineralization and cycling of nutrients in surface sediments (Norling et al. 2007). Sea grasses and macroalgae, that form the habitat of VEG communities, provide a number of ecosystem regulating services, including storm and ood protection, erosion and siltation control as well as sediment retention and accumulation of organic matter (Ronnback et al. 2007). Loss of any of these habitats would have serious implications for the ecosystem beyond changes in diversity. Thus, it must be emphasized that the conservation and management of natural marine resources must be based on a deep understanding of the functioning of habitats and their associated biota, and that it cannot be based only on estimations of species numbers.
Acknowlegments The present study was a part of the project Ecosystem approach to marine spatial planning in Polish Marine Areas PL0078, funded by Norway, Iceland and Lichtenstein through EEA

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Financial Mechanism. Samples have been collected and processed in the laboratories of Sea Fishery Institute, Marine Institute in Gdansk and University of Gdansk.

References
Airoldi L, Beck MW (2007) Loss, status and trends for coastal marine habitats of Europe. Ocean Mar Biol Ann Rev 45:345405 Airoldi L, Balata D, Beck MW (2008) The gray zone: relationship between habitat loss and marine diversity and their applications in conservation. J Exp Mar Biol Ecol 366:815 Andrulewicz E, Wielgat M (1999) Selection of southern Baltic banksfuture marine protected areas. Hydrobiologia 393:271277 Andrulewicz E, Kruk-Dowgiallo L, Osowiecki A (2004) Phytobenthos and macrozoobenthos of the Slupsk Bank stony reefs, Baltic Sea. Hydrobiologia 514:163170 Bonsdorf E (2006) Zoobenthic diversity-gradients in the Baltic Sea: continuous post-glacial succession in a stressed ecosystem. J Exp Mar Biol Ecol 330:383391 Bostrom C, Bonsdorff E (1997) Community structure and spatial variation of benthic invertebrates associated with Zostera marina (L.) beds in the northern Baltic Sea. J Sea Res 37:153166 Bostrom C, Jackson EL, Simenstand C (2006) Seagrass landscapes and their effects on associated fauna: a review. Est Coast Shelf Sci 68:383403 Colwell RK (2005) EstimateS: statistical estimation of species richness and shared species from samples. Version 7.5. Users Guide and application published at: http:/purl.oclc.org/estimates Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:27172727 Dobson A, Lodge D, Alder J, Cumming GS, Keymer J, McGlade J, Mooney H, Rusak JA, Sala O, Wolters V, Wall D, Winfree R, Xenopoulos MA (2006) Habitat loss, trophic collapse, and the decline of ecosystem services. Ecology 87:19151924 Dulvy NK, Sadovy Y, Reynolds JD (2003) Extinction vulnerability in marine populations. Fish Fish 4:2564 Ellingsen KE, Hewitt JE, Thrush SF (2007) Rare species, habitat diversity and functional redundancy in marine benthos. J Sea Res 58:291301 Elmgren R, Hill C (1997) Ecosystem function at low biodiversitythe Baltic example. In: Ormond RFG, Gage J, Angel M (eds) Marine biodiversity: patterns and processes. Cambridge University, Cambridge, pp 319336 Gaston KJ (1994) Rarity. Chapman and Hall, London Graham MH (2004) Effects of local deforestation on the diversity and structure of Southern California giant kelp forest food webs. Ecosystems 7:341357 Gray JS (1997) Marine biodiversity: patterns, threats and conservation needs. Biodiv Conserv 6:153175 HELCOM 2009, Biodiversity in the Balic seaan integrated thematic assessment on biodiversity and nature conservation in the Baltic sea: executive summary. Baltic sea environmental proceedings No. 116A Herbich J, Warzocha J (1998) Introduction to the marine and coastal environment of Poland. In: Nordheim H, Boedeker D (eds.) Red list of marine and coastal biotopes and biotope complexes of the Baltic sea, Belt sea and Kattegat. Baltic sea environment proceedings No. 75 Karlson K, Rosenberg R, Bonsdorf E (2002) Temporal and spatial large scale effects of eutrophication and oxygen deciency on benthic fauna in Scandinavian and Baltic watersa review. Oceanog Mar Biol Ann Rev 40:427489 Kotta J, Moller T (2009) Important scales of distribution patterns of benthic species in the Gretagrund area, the central Gulf of Riga. Estonian J Ecol 58:259269 Lepparanta M, Myrberg K (2009) Physical oceanography of the Baltic Sea. Springer-Verlag, Berlin McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450453 Micheli F, Halpern BS (2005) Low functional redundancy in coastal marine assemblages. Ecol Lett 8:391400 Nordheim H, Boedeker D (1998) Red list of marine and coastal biotopes and biotope complexes of the Baltic sea, Belt sea and Kattegat. Baltic sea environment proceedings No. 75 Norling K, Rosenberg R, Hulth S, Gremare A, Bonsdorff E (2007) Importance of functional biodiversity and species-specic traits of benthic fauna for ecosystem functions in marine sediments. Mar Ecol Pro Ser 332:1123

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Olenin S, Daunys D (2004) Coastal typology based on benthic biotope and community data: the Lithuanian case study. In: Schernewski G, Wielgat M (eds.) Baltic sea typology, coastline reports 4, p. 6583 Piechura J (1985) Temperatura i zasolenie wod w polskiej stree wylacznego rybolostwa w lipcu 1981. Rep Sea Fish Inst Gdynia 20:538 Plinski M, Florczyk I (1993) Macrophytobenthos. In: Korzeniewski K (ed) Puck Bay. Fundacja Uniwersytetu Gdanskiego, Gdansk, pp 416421 Reed BJ, Hovel KA (2006) Seagrass habitat disturbance: how loss and fragmentation of eelgrass Zostera marina inuences epifaunal abundance and diversity. Mar Ecol Prog Ser 326:133143 Roberts CM, Hawkins JP (1999) Extinction risk in the sea. Trends Ecol Evol 14:241246 Ronnback P, Kautsky N, Pihl L, Troell M, Soderqvist T, Wennhage H (2007) Ecosystem goods and services from Swedish coastal habitats: identication, valuation, and implications of ecosystem shifts. Ambio 36:534544 Rosenzweig ML (1995) Species diversity in space and time. Cambridge University, Cambridge Thrush S, Gray JS, Hewitt JE, Ugland KI (2006) Predicting the effects of habitat homogenization on marine biodiversity. Ecol Appl 16:16361642 Veber T, Kotta J, Lauringson V, Kotta I (2009) Inuence of the local abiotic environmenta, weather and regioanl nutrient loading on macrobenthic invertebrate feeding groups in a shallow brackish water ecosystem. Oceanologia 51(4):541559 Warzocha J (1994) Spatial distribution of macrofauna in the southern Baltic in 1983. Bull Sea Fisher Inst 1(131):4759 Warzocha J (1995) Classication and structure of macrofaunal communities in the southern Baltic. Arch Fishery Mar Res 42:225237 Wesawski JM, Warzocha J, Wiktor J, Urbanski J, Bradtke K, Kryla L, Tatarek A, Kotwicki L, Piwowarczyk J (2009) Biological valorisation of the southern Balic Sea (Polish Exclusive Economic Zone). Oceanologia 51(3):415435 Wiktor K (1993) Macrozoobenthos. In: Korzeniewski K (ed) Puck Bay. Fundacja Uniwersytetu Gdanskiego, Gdansk, pp 442454 Wolff WJ (2000) Causes of extirpations in the Wadden Sea, an estuarine area in the Netherlands. Conserv Biol 14:876885

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