AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 397–406 (2010) Published online 3 December 2009 in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/aqc.1085

Distribution of benthic communities in the fjord-like ecosystem, south-western , a globally anomalous estuarine protected area

NEVILLE S. BARRETTÃ and GRAHAM J. EDGAR Tasmanian Aquaculture and Fisheries Institute, University of Tasmania, GPO Box 252-49, Hobart, Tasmania 7001

ABSTRACT 1. Benthic assemblages in the fjord-like Bathurst Channel estuarine system, south-western Tasmania, vary over horizontal scales of 1–5 km and vertical scales of 1–10 m. Multivariate analysis indicated a total of eight major assemblages that characterize different sections and depths of the channel. 2. Because tannins in the low-salinity surface water layer block light, foliose algae reach 5 m depth in the marine western region but do not penetrate below 1 m in the east. By contrast, sessile invertebrates are most abundant below 5 m depth in the west and below 2 m in the east. Deeper assemblages are unlikely to be continuous with assemblages in deeper waters off the Tasmanian coast as they are highly constrained by depth within particular sections of the estuary. 3. While the species composition of the Bathurst Channel biota is most similar to that found elsewhere in Tasmania, the structural character of the biota in terms of major taxonomic groups is more closely allied to that found in fjords of south-western Chile and south-western New Zealand. These three regions all possess wilderness settings, high rainfall that is channelled through estuaries as a low-salinity surface layer, deep-water emergence of fauna, rapid change in biotic communities over short horizontal and vertical distances, and high levels of local endemism. They also include some of the most threatened aquatic ecosystems on earth due to increasing human activity from a near pristine base, and the potentially catastrophic impacts of climate change. Copyright r 2009 John Wiley & Sons, Ltd.

Received 4 February 2009; Revised 2 September 2009; Accepted 13 September 2009

KEY WORDS: climate change; endemism; estuary; macroalgae; marine protected area; sessile invertebrates; threatened habitats

INTRODUCTION indicated that the geomorphological resemblance with fjords is superficial (Baker and Ahmad, 1959). Regardless of origin, Bathurst Channel comprises a narrow 12 km long passage that physical processes operating within Bathurst Channel have connects the large coastal embayment of with the many characteristics in common with fjords because of the equally large estuarine basin at Bathurst Harbour (Figure 1). shallow (o8 m depth) constricted sill at the western entrance It is located on the south-western coast of Tasmania within the and deeper waters within. The narrow central channel is South West National Park and Tasmanian Wilderness World generally about 300 m wide and 20–45 m deep mid- channel, Heritage Area, and forms part of the only large estuarine with shallows (o10 m depth) on the margins extending into system in southern Australia without significant human impact numerous adjacent bays. throughout the adjacent catchment (Edgar et al., in press). Recent studies in the region indicate that Bathurst Channel Because of steep-sided valleys and a convoluted shoreline, possesses a highly distinctive marine flora and fauna (Edgar, Bathurst Channel was long considered glacial in origin–the 1990; Resource Planning & Development Commission, 2003), only example of a fjord in Australia. Subsequent studies with high conservation value (Edgar et al., in press). Its biotic

*Correspondence to: Neville S. Barrett, Tasmanian Aquaculture and Fisheries Institute, University of Tasmania, GPO Box 252-49, Hobart, Tasmania 7001. E-mail: [email protected]

Copyright r 2009 John Wiley & Sons, Ltd. 398 N. S. BARRETT AND G. J. EDGAR

Port Davey

Bramble Cove Turnball Breaksea Island Island Munday Little Waterfall Woody Bay Beabey Island Island Joan Pt Pt Forrester Eve Pt Pt Bathurst Channel Platypus Bathurst Pt Harbour

Figure 1. Location of sites surveyed by video in the Bathurst Channel region of south-western Tasmania in spring 2002. distinctiveness is due in part to the phenomenon of deep-water METHODS emergence, which involves uplifted vertical distribution (Edgar Field surveys and Barrett, in press), and also to a large component of endemic species, including a fish species not recorded elsewhere In total, 23 sites off rocky headlands distributed along (Edgar et al., in press). Partly in recognition of these Bathurst Channel from Port Davey to Bathurst Harbour biodiversity values, waters within the broader Port Davey were investigated in October and November 2002 (Figure 1). region were formally declared a multi-zoned marine protected Sites were chosen to describe variation in the sessile biota area (MPA) in January 2005. This MPA includes both Bathurst associated with the main channel from marine to upsteam Channel and Bathurst Harbour, which are together zoned as a ends, with patterns assessed using multiple transects separated fully protected sanctuary zone—the largest estuarine ‘no-take’ at scales of hundreds of metres nested along the estuary at conservation area in Australia and perhaps the largest scales of kilometres. At each site, single transect lines were set worldwide for a complete estuarine ecosystem. normal to the shore with the 0-m mark situated as close as Within Bathurst Channel, tannin-stained waters severely possible to the high tide mark. A diver swam the transect reel restrict light penetration, with consequent constriction of the offshore until the 20 m depth contour or the end of the 100 m depth range occupied by algal species. Below 5 m depth, the transect line was reached, whichever came first. Transects were benthic biota is dominated by filter feeding cnidarians, marked every 5 m so that positions along the transect line bryozoans, tube worms, ascidians and sponges, while could be interpreted from the subsequent video recordings. scavenging and predatory molluscs, crustaceans and After setting the transect line, the diver swam back to the echinoderms are relatively depauperate (Edgar et al., in press). shore along the line, recording the depth every 5 m to provide a Despite the scientific and conservation value of the depth profile of each transect for comparison with the video Bathurst Channel biota, no quantitative study has reported record. Concurrently, a second diver entered the water and on the distribution of species within the ecosystem, while swam down the line, using a Sony TRV 900 digital video relationships with biotas elsewhere have never been evaluated. camera in an underwater housing to record benthic The only other documented similar assemblages are found in assemblages present along the transect. Digital video was similar latitudes in fjords off south-western New Zealand and chosen as the format for this survey because output quality Chile, where the waters of coastal estuarine systems can be was immediately clear to the operator, and the video frame- tannin-stained and stratified, and taxa more typical of deeper grabbing capability was not substantially different to images water are present at depth o20 m, such as stony corals, black produced by digital still cameras available at the time. Higher corals, sea pens and brachiopods (Miller, 1997; Schiel and resolution film-based cameras were not used because variable Hickford, 2001; Fo¨rsterra and Ha¨ussermann, 2003). underwater lighting in the region increased the possibility of The aim of the present study is to quantitatively describe poor film exposure during logistically-challenging surveys that the distribution of the dominant macroalgae and sessile could not be repeated. animals within Bathurst Channel, and to clarify broader In initial trials, digital images of benthic assemblages within biogeographic relationships. Our study is based on a a 0.5 m  0.5 m quadrat placed on the sea bed were recorded quantitative video survey of the region undertaken in spring using the still image capacity of the video camera. However, 2002 that also aimed to provide a baseline MPA data set for the distance between the camera and quadrat was found to be assessment of future human impacts. Human activity is too great for the use of photoquadrats in shallow tannin- increasing in Bathurst Channel, which is appropriately stained waters of Bathurst Channel. Despite optimal placing of regarded as environmentally sensitive due to the presence of video lights, species and substratum types could not be threatened and endemic species, and habitats with highly adequately resolved on images because of tannins in the restricted distributions and fragile structural complexity. water between the camera and the quadrat, and viscous mixing Potential risks to the ecosystem include nutrification of the of saline and brackish waters, which strongly attenuated and oligotrophic waters, disturbance to fragile biota on the sea bed distorted light. The video technique was consequently modified by scuba divers, invasion of exotic taxa, oil spills, climate by placing the camera closer to the sea bed. change, and mechanical damage due to propeller wash and The modified technique involved the diver moving the anchoring of vessels (Edgar et al., in press). vertically downward orientated video camera very slowly at a

Copyright r 2009 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 397–406 (2010) DISTRIBUTION OF BENTHIC COMMUNITIES IN A FJORD-LIKE ECOSYSTEM 399 height 0.5–0.7 m above the substratum, giving an image width With the exception of common species that were clearly of approximately 0.4 m. The camera was swum over a distance identifiable, reference images were taken of all species, life of about 10 m perpendicular to the transect at defined depths forms and substratum categories. All video collected during (0, 1, 2, 5, 10, 15, 20 m) below low water mark. During this study was transferred to MPEG format on DVD, which computer processing, still images were extracted from the should be durable and allow for reliable archiving. This will video footage by interlacing two adjacent frames, producing provide a baseline for detecting future change. images of c.1.2 Mb resolution. Within these images, 1 cm sized objects such as solitary corals could be resolved providing sufficient contrast was available. Approximately 10–20 Statistical analyses replicate quadrats were captured at each defined depth at each site, with additional depths investigated at Faunal relationships between sites were examined using some locations. Images at a few depth/site combinations cluster analysis, non-metric multidimensional scaling (MDS), could not be interpreted because of distortion at the brackish permutational distance-based linear modelling (DISTLM) and water/seawater interface. These data are regarded as missing principal coordinates analysis (PCoA). For all analytical values. All still images used in analyses are available from methods, mean percentage cover was calculated for each the authors. depth and site at 0, 1, 2, 5, 10, 15 and 20 m depth strata. Data Photoquadrat images were imported into Microsoft pertaining to intermediate depths were assigned to the nearest Powerpoint and a grid with 50 points superimposed over of these depth strata. Rare taxa (i.e. those present at two or each image. A point intercept method was then used to less depth strata among all sites) were amalgamated into a estimate the percentage cover of different taxa and substratum higher taxonomic unit. Thus, for example, if the morpho- types. In a pilot study, a score of 50 points per image species ‘grey finger sponge’ was only recorded at one depth at (500–1000 points per depth stratum) represented the best two sites, then density information for this taxon was compromise between time taken for scoring each image, the amalgamated into the ‘other sponges’ taxon, but if recorded amount of data extracted per image, and the total available from three or more depth/site combinations then the taxon time for scoring and recording data (200 h). ‘grey finger sponge’ was retained in analyses. Although the total area within each photo-quadrat varied Mean percentage cover data included in the depth by site somewhat due to differences in distance that the video was matrix were square root transformed to reduce the influence of held from the substratum (0.5–0.7 m), bias associated with this the most abundant species, and converted to a matrix of biotic variability was considered low. The index of density used, i.e. similarity between pairs of sites using the Bray–Curtis percentage cover, should only be affected by image size if similarity index, which is relatively insensitive to data sets habitats were highly heterogeneous and the total area covered with many zero values (Faith et al., 1987). Major biotic groups along a depth stratum was inadequate for encompassing the identified in cluster analysis (based on group average linkages range of major biotic objects, or objects were too distant from of the similarity matrix) were identified on the MDS plot. the video to be identified. The usefulness of the two-dimensional MDS display of Macroalgae and animals were categorized at the lowest biotic relationships is indicated by the stress statistic, which taxonomic level practical; however, in many cases organisms signifies a good depiction of relationships when o0.1 and poor could not be resolved at the species level from the still images. depiction when 40.2 (Clarke, 1993). Species that charac- Taxa belonging to groups such as large algae, octocorals and terize the major assemblage groups identified during cluster anemones were generally identified to species (some not yet analysis and MDS were identified using SIMPER protocols in scientifically described), while sponges, bryozoans and the PRIMER statistical package (Carr, 1996). compound ascidians were generally identified to morpho- PERMANOVA1with PRIMER was used for DISTLM species; and inconspicuous algae and invertebrates were (Anderson et al., 2008), a permutational procedure analogous grouped within higher taxonomic groups. Thus, for example, to multivariate regression modelling that is more appropriate sponges with a recognizable growth form were placed into for ecological studies with highly zero-inflated data sets categories such as ‘orange finger sponge’ or ‘grey vase sponge’, because of fewer assumptions regarding distribution of data and reference images of each morphotype compiled. (Legendre and Anderson, 1999). Models were fitted stepwise to Identifications and splitting at the morphotypic level were maximize Akaike’s Information Criterion. Position along the only made where distinct differences were present and estuarine cline, as measured using distance from Breaksea considered unlikely to be ecotypic variants. Commonly, Island in Port Davey, and log depth were included as predictor a large proportion of the substratum within quadrats variables in the model. Quadratic and interaction terms were appeared to be bare rock, or in some images, rock overlain also added to the model to account for any major non- with a fine sediment cover or a periphyton film (mixed linearities in trends, such as maxima at an intermediate depth hydroids, bryozoans, filamentous algae). In this situation the or distance. substratum was recorded as bare reef. Species identifications Patterns of community structure in the region were also were based upon guidance from a previous study in Bathurst analysed using PCoA, as run by the CAP program (Anderson, Channel during which most common species were identified 2003; Anderson and Willis, 2003). The environmental variates through extensive collections made by divers, and that were depth and distance along estuary were related to each of the lodged in the Museum of South Australia (Last and Edgar, first three principal coordinates using Pearson correlation 1994). A list of all macroalgal and invertebrate species coefficients. Associations of common species with different recorded in Bathurst Channel and Port Davey is provided as community types were also assessed by calculating correlations supplementary material with an associated paper (Edgar et al., with PCoA axes using mean species cover data for each site, in press). depth and species.

Copyright r 2009 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 397–406 (2010) 400 N. S. BARRETT AND G. J. EDGAR

RESULTS Carpoglossum confluens, a species restricted to progressively shallow water eastward up the estuary to Joan Point, and Hormosira banksii, a low intertidal species not found in the Biotic distribution patterns western region (Figure 2). Foliose macroalgae were abundant near low water mark The green algal taxon Ulva spp. possessed an intertidal throughout the estuary; however, subtidal macroalgae were distribution almost identical to that of Hormosira. Red algae, largely restricted to western Bathurst Channel (Figure 2). most notably Thamnoclonium dichotomum and encrusting Within the western region, few macroalgae were recorded at ‘lithothamnion’ type corallines, were largely distributed in depths 45m. the western region of Bathurst Channel in water depths of The ‘bullkelp’ Durvillaea potatorum, a species of wave 2–5 m. They thus typically occurred below the zone of foliose exposed coasts, was abundant between 0 m and 2 m depth at brown algae, close to the euphotic limit for growth of algae. western sites, but was not found east of Turnbull Island Distribution patterns of sessile invertebrates contrasted (Figure 2). A similar distribution pattern was evident for most greatly with patterns exhibited by macroalgae. Invertebrates as other large brown algal species, including species not included a group were consistently abundant in water depths 42m in Figure 2 such as Lessonia corrugata, Xiphophora gladiata along Bathurst Channel, with perhaps a slight decline at the and Macrocystis pyrifera. These species all declined in eastern entrance (Figure 3). abundance eastward from Breaksea Island to Turnbull Sponges occurred consistently at locations 45 m depth Island, and were absent further east. Brown algal species throughout Bathurst Channel (Figure 3). More detailed with atypical distribution patterns included Ecklonia radiata, information on sponge composition is required to adequately which was most abundant in the central estuary at 1-2 m depth, assess how the species composition of the sponge fauna varies,

us Point Eve Point Eve Point Joan Point Joan Point yp Waterfall Bay Waterfall Waterfall Bay Waterfall Beabey Point Beabey Beabey Point Beabey Bramble Cove Bramble Bramble Cove Bramble Munday Island Munday East Eve Point Munday Island Munday East Eve Point Platypus Point Plat Turnbull Island Turnbull Turnbull Island Turnbull Forrester Point Forrester Point Little Woody Is. Little Woody Little Woody Is. Little Woody Breaksea Island Breaksea Island Figure 2. Mean percentage cover of total foliose algae and common algal species at different sites and depths in the Bathurst Channel estuary. Sites are distributed in order along the estuarine cline from Breaksea Island (Port Davey) to the Bathurst Harbour entrance. Depth strata are shaded with respect to percentage cover; heavy shading indicates strata with 450% cover; moderate shading indicates 25–50% cover; light shading 10–25% cover; and open oblique hatching 0.1–10% cover. Depth strata with missing values are shaded similarly to the majority of adjacent blocks.

Copyright r 2009 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 397–406 (2010) DISTRIBUTION OF BENTHIC COMMUNITIES IN A FJORD-LIKE ECOSYSTEM 401

Total sessile animals Sponges 0 000000000000 0 000001111600 1 00000000100 1 00000002113 2 1041001240 0 2 1041001441936 5 114106589175211 5 1 15 12 35 6 25 28 46 46 53 7 42 10 12 19 12 7 4 3 1 0 10 12 31 22 14 24 18 45 2 15 18 13 4 2 15 11 0 15 29 17 10 11 23 45 9 20 11 23 12 11 11 7 20 14 30 14 22 29 12

Corynactis spp. Mytilus galloprovincialis 0 000000000000 0 000001111600 1 00000000000 1 00000002013 2 0000000000 0 2 0000000005 34 5 000000000100 5 000000000000 10 00 000314 1 10 00 00000 0 15 0 00027 0 15 0 00000 0 20 00064020 0 00000

Drifa sp. Bryozoans 0 000000000000 0 000000000000 1 00000000000 1 00000000000 m) 2 0000000200 0 2 0000000000 0 5 00126000213633024 5 000000071501 10 05 00020 0 10 00 11100 0 15 0 00017 0 15 2 21002 0 20 Depth (m 20 0 00170 151200

BbtiithiBarbatia pistachia ClliClavularia sp. 0 000000000000 0 000000000000 1 00000000000 1 00000000000 2 0000000000 0 2 0000000000 0 5 000000000200 5 000004213000 10 00 001427 0 10 00 441673 0 15 0 000016 0 15 0 24821 0 20 0 0002020 0 11220

Primnoella sp. Balanophyllia bairdiana 0 00000000000 0 00000000000 1 00000000000 1 00000000000 2 0000000000 0 2 0000000000 0 5 01001141800000 5 000000000000 10 02 31000 0 10 01 00000 0 15 0 00000 0 15 0 00000 9 20 00000020 0 00014 Eve Point Eve Point Joan Point Joan Point Waterfall Bay Waterfall Waterfall Bay Waterfall Beabey Point Beabey Beabey Point Beabey Bramble Cove Bramble Bramble Cove Bramble East Eve Point East Eve Point Island Munday Munday Island Munday Platypus Point Platypus Point Turnbull Island Turnbull Turnbull Island Turnbull Forrester Point Forrester Point Little Woody Is. Little Woody Little Woody Is. Little Woody Breaksea Island Breaksea Island Figure 3. Mean percentage cover of total sessile invertebrates and common invertebrate taxa at different sites and depths in the Bathurst Channel estuary. Sites are distributed in order along the estuarine cline from Breaksea Island (Port Davey) to the Bathurst Harbour entrance. Depth strata are shaded with respect to percentage cover; heavy shading indicates strata with 450% cover; moderate shading indicates 25–50% cover; light shading 10–25% cover; and open oblique hatching 0.1–10% cover. Depth strata with missing values are shaded similarly to the majority of adjacent blocks. although the number of sponge taxa noticeably declined in very high abundance in 10–15 m depth at locations with towards the east. Among the other major sessile faunal taxa, good water flow in Bathurst Narrows, and the solitary jewel anemones (Corynactis spp.) were localized in deep water ahermatypic coral Balanophyllia bairdiana was widely in eastern Bathurst Channel, the blue mussel (Mytilus distributed in deeper water but rarely covered much of the galloprovincialis) occurred abundantly in the same region but reef surface (Figure 3). in water depths of 0–2 m, and soft corals (Drifa sp.) was distributed over the full length of the channel, particularly at Multivariate analyses 5 m depth. In depths 45 m, bryozoans were widespread, the stoloniferous octocoral Clavularia sp. was abundant in the Cluster analysis revealed eight major multivariate groups in central channel, and seawhips (Primnoella spp.) were present the depth strata-by-site data set when classified at the 30% near Forrester Point. The bivalve Barbatia pistachia occurred similarity level. The distribution of each of these biotic groups

Copyright r 2009 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 397–406 (2010) 402 N. S. BARRETT AND G. J. EDGAR Forrester Point Forrester MundayIsland Little Woody Is. Joan Point Point Eve Platypus Point East Eve Point East Eve BreakseaIsland Cove Bramble Island Turnbull Bay Waterfall BeabeyPoint

0 8 5 8 5 5 5 5 5 5 5 5 5 5 5 5 5 5 1 8 6 6 8 8 5 6 6 5 6 6 6 6 5 6 7 7 7 2 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 6 7 7 7 5 6 2 2 2 2 4 2 2 2 2 2 2 4 4 4 4 4 4 4 4 4 10 2 1 4 1 1 3 1 3 3 3 3 3 3 3 3 Depth (m) 15 1 1 1 1 1 3 3 4 3 4 3 3 20 1 1 1 1 1 3 4 3 4 3 3

Figure 4. Distribution of the eight identified biotic assemblages in the Port Davey estuary. Sites are distributed in order along the estuarine cline from Breaksea Island to Bathurst Harbour entrance. Depth strata are shaded with respect to different biotic groups. Depth strata not investigated are shaded similarly to the majority of adjacent blocks.

Stress: 0.11

Groups 1: Sponges/zoanthids 2: Thamnoclonium 3: Clavularia/Barbatia 4: Drifa 5: Hormosira 6: Ecklonia 7: Mytilus 8: Durvillaea

Figure 5. MDS plot outlining biotic relationships between the eight major benthic assemblages in Bathurst Channel. at different depths and sites in Bathurst Channel is shown in Durvillaea potatorum. The characteristic species were all Figure 4. Biotic relationships between these groups are macroalgae – Ulva spp., Hormosira banksii and Carpoglossum indicated in the MDS plot (Figure 5), which has been confluens. Group 6 (Ecklonia Group) occurred below group 5 in rotated to reflect east–west variation along the x-axis and 1–2 m water depth, particularly in the western channel. As for depth related variation on the y-axis. Group 5, characteristic species were all macroalgae – Ecklonia Group 1 (sponge/zoanthid Group) comprised deep-water radiata, Carpoglossum confluens and encrusting corallines. (410 m) fauna present in the western half of Bathurst Channel Group 7 (Mytilus Group) was characterized by the blue mussel from Turnbull Island to Munday Island. SIMPER analysis Mytilus galloprovincialis, and occurred in similar depths to Group indicated that the characteristic components of this fauna were 6 but in the eastern channel. Group 8 (Durvillaea Group) cup sponges, ‘other sponges’ and yellow zoanthids (Parazoanthus occurred at shallow depths in the western region, where habitats sp.). Group 2 (Thamnoclonium Group) occurred in the same were dominated by Durvillaea potatorum. region in intermediate depths of 5–10 m. It was characterized by Figure 4 indicates that rapid ecosystem change occurred at the red alga Thamnoclonium dichotomum, encrusting coralline three locations along Bathurst Channel. Low intertidal algae, sea whips (Primnoella spp.) and sponges. Group 3 assemblages changed from Durvillaea dominated to Ulva and (Clavularia/Barbatia Group) was present at depths from Hormosira dominated between Turnbull Island and Waterfall 10–20 m in eastern Bathurst Channel from Forrester Point, and Bay. Shallow (1–2 m depth) sublittoral assemblages changed was characterized by the octocoral Clavularia sp., the mollusc from algal dominated (Ecklonia and Carpoglossum) to mussel Barbatia pistachia, the jewel anemone Corynactis spp. and dominated (Mytilus) at Joan Point. The deeper water sponges. Group 4 (Drifa Group) overlapped with Group 3 in assemblage (45 m depth) changed eastward from Munday the eastern region, but was most prevalent at 5 m depth. It can be Island from a predominance of cup sponges, yellow zoanthids, recognized by the soft coral Drifa sp. and sponges. Group 5 red algae (Thamnoclonium) and sea whips (Primnoella spp.) to (Hormosira Group) dominated intertidal shores throughout the the conspicuous presence of the bivalve Barbatia pistachia, the channel, other than at sites in the west occupied by bull-kelp jewel anemone Corynactis spp., and the soft coral Drifa sp.

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Figure 6. Results of principal coordinate analysis showing relationships between the eight major biotic groups identified in Bathurst Channel. Correlation coefficients with first two coordinate axes are shown for cover of individual species with highest correlations, and for depth and distance along estuary from Port Davey. Species affinities within groups are discussed in the results.

Table 1. Results of DISTLM using predictor variables log depth, log contributed significantly to the DISTLM model and together depth squared, distance along estuarine cline, log depth  distance and explained 35% of total variation, a value considerably lower distance squared. than the 54% of total variation explained in DISTLM analysis Variable df SS Pseudo-F P % total with the eight identified biotic groups considered as levels of a variation single categorical factor ‘biotic groups’. Depth 130 93884 29.445 0.001 18.5 Depth2 129 30184 10.132 0.001 24.4 Distance 128 27346 9.806 0.001 29.8 Depth  distance 127 17989 6.740 0.001 33.3 DISCUSSION Distance2 126 10610 4.071 0.001 35.4 The Bathurst Channel biota Biotic relationships indicated by principal coordinate Plant and animal assemblages present in Bathurst Channel analysis (PCoA; Figure 6) differed in several respects differ markedly from those observed elsewhere in Tasmania compared to those identified from the MDS plot (Figure 5). and Australia (Edgar and Barrett, in press). The primary dis- Sites dominated by a single species, particularly Group 8 sites tinguishing characteristic, particularly in the eastern channel, dominated by Durvillaea potatorum and Group 7 sites is the paucity of subtidal macroalgae and predominance of dominated by Mytilus galloprovincialis, grouped centrally delicate sessile invertebrates in current-swept areas. The maxi- within the PCoA plot rather than occurring as outliers. mum depth at which algal species can survive is presumably Three distinctive assemblage groupings were evident in the highly limited in Bathurst Channel as a consequence of tannin PCoA plot, a shallow intertidal grouping dominated by stained surface waters that severely restrict light penetration. Hormosira banksii and Ulva spp. (Group 5), an intermediate A lack of fast growing algal competitors in turn apparently depth grouping dominated by Ecklonia radiata (Group 6), and allows sessile invertebrates to dominate space on rock surfaces a mixed deep-water grouping composed of sponges and other (Miller and Etter, 2008). Sessile animals colonize much sessile invertebrates (predominantly Groups 1, 2 and 4). shallower habitats than elsewhere along the Tasmanian coast Depth showed an extremely high correlation with the first (Edgar and Barrett, in press). Characteristic species within coordinate axis and low correlations with the second and third Bathurst Channel include filter feeding bryozoans, sponges, axes (R 5 0.83, 0.20 and À0.11 for PCoA axes 1, 2 and 3, anemones, sea pens, soft corals, hard corals, sea whips and respectively), while distance along Bathurst Channel from the other octocorals, tubeworms, and ascidians. Many undes- entrance had a relatively low correlation with the first axis and cribed invertebrate species are also present in this system, as moderate correlations with the second and third axes well as species only recorded elsewhere in deep offshore waters (R 5 À0.27, 0.32 and 0.41 for PCoA axes 1, 2 and 3, (Edgar et al., in press). respectively). The influences of depth and distance along the The Bathurst Channel biota cannot, however, be estuary were at right angles to each other when the first two characterized as a deepsea assemblage displaced into shallow coordinate axes are plotted (Figure 6). PCoA axes 1, 2 and 3 water. The fauna includes a mixture of elements from estuaries explained 25%, 14% and 7% of total variation, respectively. (e.g. mussels) and both deep and shallow marine ecosystems, DISTLM also indicated that depth was the primary and lacks many species that are widely distributed and environmental factor affecting biotic patterns, with 19% of common elsewhere around the Tasmanian coast. total variation explained (Table 1), compared with only 6% for Mobile invertebrate groups that are typically abundant on distance along the estuarine cline when variables were assessed shallow coastal reefs, such as molluscs, crustaceans and independently. Quadratic and interaction terms added 2–6% of echinoderms, are relatively depauperate in eastern Bathurst total variation explained. The five variables investigated each Channel (Edgar and Barrett, in press). A likely explanation is

Copyright r 2009 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 397–406 (2010) 404 N. S. BARRETT AND G. J. EDGAR the low ecosystem productivity, which is also indicated by a the biota of Groups 6 and 7 changed to Groups 2 dearth of sessile invertebrates away from sites with strong (Thamnoclonium) and 4 (Drifa) between 2 and 5 m depth, current flow. Sheltered reef habitat generally appears as bare and Groups 1 (sponges) and 3 (Clavularia) were consistently rock with a fine coating of silt. dominant only at 10 m depth and below (Figure 4). Bathurst Numerous distinctive community types were evident in Channel faunal assemblages are thus unlikely to extend into Bathurst Channel. The eight biotic groups identified in this deep water off the south-western Tasmanian coast and show study (Figures 4 and 5) had little biotic similarity to each other continuity with assemblages there, but rather appear to be (o30% when calculated as Bray-Curtis Similarity Index using associated with the particular set of environmental conditions square root transformed percent cover data) and could prevailing at particular depths within this system. presumably have been subdivided into finer groupings with addi- tional data. Much of this variability reflected depth stratification, Relationships with biotas in New Zealand and Chilean which included pronounced changes in species composition over fjords vertical scales of a metre in the shallow subtidal. Biotic variability with depth and along the estuary was While the species composition of the Bathurst Channel biota is much better explained in DISTLM using a single categorical most similar to that found elsewhere off the southern variable ‘biotic groups’, with eight levels pertaining to different Tasmanian coast (Edgar and Barrett, in press), the structural community types (54% of total biotic variation explained), than character of the biota in terms of major taxonomic groups is by linear and quadratic models involving depth and distance more closely allied to that found in fjords of south-western along the estuary (35% of total biotic variation explained). Chile and south-western New Zealand. The western coasts of Community types were apparently reasonably homogeneous, all three Southern Hemisphere land masses at c.431 S latitude changing quickly at particular depths and locations rather possess important similarities in geomorphology, including than varying gradually along environmental clines. estuarine systems with narrow convoluted channels, near Ecological changes along the axis of the Bathurst Channel vertical walls, and deep basins constricted at the seaward estuary were much more evident in the MDS plot (Figure 5) entrance by relatively shallow sills. New Zealand and Chilean than in the PCoA plot (Figure 6). Whereas the MDS plot fjord basins are, however, much deeper (4100 m depth) than indicated that depth and distance along Bathurst Channel Bathurst Channel (45 m maximum depth). contributed about equally to biotic changes, the first two The three regions also all possess a wilderness setting and principal coordinate axes were extremely highly correlated are affected by high rainfall, with runoff channelled through with depth (R 5 0.87) but much less so for distance along estuaries as a low salinity surface layer. This low salinity layer estuary (R 5 0.37). Distance along estuary was, however, extends to a depth of 3–7 m in Chile (Fo¨rsterra and moderately correlated with a number of minor PCoA axes, Ha¨ussermann, 2003) and 2–6 m in New Zealand (Witman including PCoA axis 3 (R 5 0.41). This outcome indicated that and Grange, 1998). The salinity of the surface layer in the effects associated with distance along the estuary were Chilean fjords varies, with some systems similar to Bathurst complex, involving a number of factors not easily reduced in Harbour (7–31%; Fo¨rsterra and Ha¨ussermann, 2003) and multidimensional space. others (o2%; Galea et al., 2007) matching the the much lower The different graphical outcomes of MDS and PCoA surface values found in New Zealand fjords (0–14%; Smith reflected their mathematical foundations, with MDS providing and Witman, 1999). The bottom layer is close to fully marine the better overall description of biotic relationships in the in all three regions, although Fo¨rsterra and Ha¨ussermann region. The PCoA plot did not separately distinguish outlying (2003) indicate that salinity can decline to 28.5% below the data points (including the Breaksea Island shallows with 100% halocline in Chile. cover of Durvillaea potatorum) because the low number of Dark tannin stained surface waters appear to be much more samples meant that outlying data contributed only a small a feature of Bathurst Channel than the New Zealand and percentage of total biotic variation, so was not indicated in Chilean fjords, although tannin staining is also evident in the coordinate axes 1 or 2. By contrast, the two biotic groups latter two regions, particularly amongst inner fjords. Ryan and which numerically provided most of the samples included in Paulin (1998) suggest that light levels at 15 m depth in New analyses, Groups 5 and 6, were resolved strongly in the PCoA Zealand fjords are equivalent to 60 m depth on the open coast, because coordinate axes that separated these large groups whereas no light penetrates to 15 m depth in Bathurst Channel accounted for much of the variation between all samples. for much of the year. Moreover, underwater photographs Major distributional breaks in biotic assemblages along the taken with available light in fjords of New Zealand (Ryan and estuarine cline were depth specific. The major biotic break at Paulin, 1998) and Chile (Rochet, date unknown) lack the low tide level occurred about Turnbull Island when Durvillaea distinctive orange tinge always present in photographs from assemblages gave way to Hormosira assemblages; the major Bathurst Channel. The flatter topography of surrounding discontinuity at 2 m depth was located about Joan Point; and hinterland in Tasmania, and lower but still considerable assemblages from 5–20 m changed most rapidly between annual rainfall (4 m cf 6–7 m in New Zealand and Chile), Munday Island and Little . probably act to reduce drainage run-off times, increase In contrast to expectations that biotic assemblages would percolation time through humic soil layers, and increase the respond to decreasing light penetration up the estuary by concentration of tannins in riverine waters. colonizing progressively shallower habitats in an eastward A consequence of greater water transparency in the New direction, assemblages generally maintained good depth Zealand and Chilean fjords is greater algal penetration to stability along the estuary. For example, the change from depth. Encrusting coralline algae are common below the low Group 5 (Hormosira) to Groups 6 (Ecklonia) and 7 (Mytilus) salinity surface layer in New Zealand (Smith and Witman, occurred between 0 and 1 m depth along the full estuary, while 1999) and Chile (Fo¨rsterra and Ha¨ussermann, 2004), whereas

Copyright r 2009 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 397–406 (2010) DISTRIBUTION OF BENTHIC COMMUNITIES IN A FJORD-LIKE ECOSYSTEM 405 coralline algae did not reach 10 m depth in Bathurst Channel. species with calcareous skeletons including bryozoans, Ecklonia radiata has been reported to 23 m depth and isolated gorgonians and ahermatypic corals will be negatively Macrocystis pyrifera to 15 m depth in New Zealand fjords affected by increasing ocean acidity (Orr et al., 2005; (Ryan and Paulin, 1998). Poloczanska et al., 2007), and (iii) warming sea temperatures Regional similarities in biota are most evident in the low will disproportionately impact biotas on the temperate coasts salinity surface layer, particularly between Bathurst Channel of Southern Hemisphere land masses as these biotas have and New Zealand fjords, where similar dominant mussels nowhere further poleward to retreat (Edgar et al., 2005). (Mytilus spp.) and algae (Ulva spp. and Hormosira banksii) are Because of the potential scale of impacts, levels of endemism, present. Ulva spp. are also very abundant in low salinity and highly restricted distribution patterns, the various fjord- surface water habitats in the Chilean fjords, which are domi- like ecosystems in the Southern Hemisphere should be nated by different mussel species, with Mytilus chilensis domi- recognized as among the most threatened ecosystems on earth. nating the upper part of the mussel band and Aulacomya ater (Fo¨rsterra and Ha¨ussermann, 2004) dominating the lower part. Aulacomya ater is also common in the New Zealand ACKNOWLEDGEMENTS fjords, where it is also found to be most prominent in the lower part of the band, with Mytilus species above. This project was initiated by Michael Driessen in response to The surface mussel layer in New Zealand fjords was found concerns about the potential impacts of increasing tourist in experimental studies to be maintained by the low salinity visitation levels in Bathurst Channel. The project was funded water layer, which excluded predatory marine sea stars and by the South-West World Heritage Area Steering Committee, urchin grazers from the shallows and thus generated a refuge the Australian Research Council, and by the Tasmanian for mussels (Witman and Grange, 1998). A similar mechanism Aquaculture and Fisheries Institute. We thank Matthew probably operates in Chile, where sea stars and sea urchins Francis and Jac Gibson for boat support, Bob Connell for also occur abundantly on reefs below the low salinity layer. dive assistance, Vreni Ha¨ussermann and Gunter Fo¨rsterra for Large predatory and grazing invertebrates were, however, personal observations on threats and biota associated with largely absent from Bathurst Channel, particularly on the Chilean fjords, and Karen Miller for information on the New easternmost reefs where the bivalves Mytilus galloprovincialis Zealand fjords. and Barbatia pistachia were most abundant. 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Copyright r 2009 John Wiley & Sons, Ltd. Aquatic Conserv: Mar. Freshw. Ecosyst. 20: 397–406 (2010)