Sydney Harbour: its diverse biodiversity Pat A. Hutchings, Shane T. Ahyong, Michael B. Ashcroft, Mark A. McGrouther and Amanda L. Reid The Australian Museum, 6 College Street, Sydney NSW 2010 All records of crustaceans, molluscs, polychaetes, echinoderms and fishes from Sydney Harbour were extracted from the Australian Museum database, and plotted onto a map of Sydney Harbour that was divided into four regions. Records were analysed according to the number of species, genera and families T present and over 3000 species were recorded, approximately double to triple the number of species C found in the neighbouring Hawkesbury River, Botany Bay and Port Hacking. We examined the rate of A accumulation of records and species over time since the 1860s, which followed a stepwise pattern usually correlated with the research activity of specific curators at the Australian Museum. The high R species richness of Sydney Harbour is probably the result of multiple factors including significant tidal T flushing and the high diversity of habitats present. Not all parts of the harbour have been well sampled, S however, and we highlight areas and habitats that should be prioritised for further biodiversity surveys. An Appendix is provided listing all species in the five groups of animals considered here. The present B study highlights the remarkable richness of the Sydney Harbour fauna and provides a consolidated A background to guide future management and research, and emphasises the values of museum collections. Key words: Sydney Harbour, diversity, crustaceans, molluscs, polychaetes, echinoderms, fishes http://dx.doi.org/10.7882/AZ.2012.031 Introduction Sydney Harbour is a drowned river valley that formed area of about 50 km2 and a total catchment of 500 km2 during a rise in sea level approximately 10,000 years (Birch and McCready 2009). Most of the harbour (49.7 ago. The entrance, between North and South Heads km2) is under tidal influence (Middleton et al. 1997). (~33°50’S, 151°17’E), is about 3 km wide, with a depth of The shores of Sydney Harbour are largely developed, 30 m. The estuary then opens up into Port Jackson, which with 90% of the catchment urbanised. Sydney is is fed by three main branches, the Parramatta and Lane Australia’s largest city with a population of 4 million Cove Rivers to the west and Middle Harbour to the north people and all projections indicate it will continue to (Figure 1). The estuary is about 30 km long with a surface grow. The original shoreline of Sydney Harbour has been a. Figure 1a. The bathymetry of Sydney Harbour, (depths in m) in relation to zero on the Fort Denison tide gauge (courtesy of Phil Mulhearn and based on the soundings database from Roads and Maritime Services). Australian 2013 Zoologist volume 36 (3) 255 Hutchings et al. b. Figure 1b. The four regions that were analysed in this study (East, West, Central and North), and the locations of places mentioned in the text are shown. Figure 2. Members of John Paxton’s Macquarie University Figure 3. Site of the first marine Biological Station at Camp Biology of Fishes class sampling in Duck River, upper Cove, circa 1885-1895. The station, a charming colonial Sydney Harbour, 12th October 1974. The only fishes cottage, was built on the foreshores of Sydney Harbour in collected were one specimen of a Southern Shortfin 1881 for Russian scientist and explorer Nikolai Nikolaevich Eel, Anguilla australis and 36 Eastern Gambusia, Gambusia de Miklouho-Maclay to study Australia’s marine environment. holbrookii. Photo, John Paxton Built of timber with sandstone foundations, the cottage is typical of the practical colonial architecture of the time. It was extensively modified since European settlement, with located at historic Camp Cove, where the First Fleet rested the development of seawalls, removal of mangroves and for a night before landing at Sydney Cove. Miklouho-Maclay salt marshes, and small creeks now lined with concrete, worked at the Marine Biological Station for just four years, forming storm water drains (Figure 2). As an iconic before returning to Russia where he died in 1888. After the feature of the city, Sydney Harbour has strong aesthetic late 1880s until 2001 the cottage was a residence for army values and is heavily used for recreational purposes, such officers. Today it is a private residence. Photo: courtesy of the State Library. For more details see http://www.harbourtrust. as sailing, swimming and fishing. Land values of water- gov.au/docs/brochure-marine.pdf front property, especially east of the Harbour Bridge, are among the highest in the world. Commercial fishing has Thus, it is somewhat surprising that no comprehensive been totally banned from the harbour since 2006 due examination of the biodiversity of Sydney Harbour has been partly to streamlining of commercial fishery licensing undertaken to date, given that Sydney is home to one of the and reported high levels of dioxins (http://www.dpi. oldest natural history museums in the world (The Australian nsw.gov.au/fisheries/recreational/info/Sydney-closure), Museum), five universities and, more recently, the Sydney although recreational fishing still occurs. Institute of Marine Sciences (SIMS). Back in the 1880’s Australian 256 Zoologist volume 36 (3) 2013 Sydney Harbour there was a marine station at Camp Cove which was built stating that the other groups were present, he indicated for the Russian scientist and explorer Nikolai Nikolaevich de that much work remained to be done on these groups. Miklouho-Maclay to study Australia’s marine environment Thus, the aims of this study are to provide the most up-to- (Figure 3). Prior to this he had been invited by William date summary of the harbour fauna. The present study John Macleay to live at Elizabeth Bay House and to use compiles all the Australian Museum records (plus a small its small laboratory. The New South Wales Government number of photographic records) from Sydney Harbour provided 300 pounds towards the cost of construction of polychaetes, crustaceans, molluscs, echinoderms and with Nikolai Nikolaevich de Miklouho-Maclay raising the fishes; documents and broadly evaluates the distribution remainder of the money through donations to the station of species within the harbour, and identifies areas of the which was built in 1881. This Russian scientist also visited harbour that have been poorly sampled. the Australian Museum and we are confident that some specimens collected from this station were subsequently Methods deposited in the Australian Museum. All Australian Museum database records from the Sydney Sydney Harbour is much less known than other estuaries region of polychaetes, crustaceans, echinoderms, molluscs in Australia such as Port Phillip Bay and Moreton Bay, and fishes were extracted (23 December 2011). Less diverse or overseas estuaries, such as San Francisco Bay and groups of marine invertebrates, such as sponges, bryozoans Chesapeake Bay in the USA. To provide a baseline and cnidarians, having relatively few collection records, for guiding future management and research, we have were not included. Geographic Information Systems examined the Australian Museum databases of fishes and software (ArcMap; ESRI) was used to select records that four numerically dominant marine invertebrate groups to were within Sydney Harbour according to the blue polygon begin to document the diversity of Sydney Harbour. in Figure 1a. Many records, especially early ones, have The Australian Museum collections date back to at least imprecise position data, so including records on surrounding 1828. The earliest documented fish record from the land helped ensure records with low positional accuracy harbour is from 1878, but many undated records may be were included. Terrestrial and freshwater species were older. Among the molluscs, the earliest records are from manually removed as well as those where the collection 1860, 1882 for crustaceans and 1885 for both polychaetes locality description suggested they were collected close to, and echinoderms. Australian Museum staff have actively but outside of the study area, such as Manly Beach and collected material over the decades from Port Jackson as Shelly Beach, on the ocean side of Manly. In addition, shown in Figures 4 and 5 (McNeil and Musgrave 1926). some specific types of records were deleted, such as records for beach-collected dry cuttlebones belonging to deepwater Previous attempts to compile faunal lists of the harbour species that probably drifted from some distance offshore were undertaken for fishes by Franz Steindachner and some fossil or sub-fossil molluscs. (1866) and invertebrates by Thomas Whitelegge (1889). Steindachner, of Vienna, dealt with 71 species, describing Some of the early records only give Port Jackson as the 21 as new (Saunders 2012), including the Eastern Sea locality; for these records the latitude and longitude Garfish, Hyporhamphus australis and the Eastern Pomfred, values were generalised as a position east of the Harbour Schuettea scalaripinnis. Whitelegge was a curator at the Bridge. In some cases, ‘Port Jackson’ could indicate the Australian Museum and assembled all the known data specimens were obtained from the Sydney Fish Market from the literature and the collections. Relevant here is and thus may not have been collected from within the that he recorded 112 species of echinoderms and while harbour, but further afield in the Sydney region; obviously Figure 4. Bottle and Glass Rocks from McNeill and Figure 5. Bottle and Glass Rocks from McNeill and Musgrave (1926) who quote, ‘when the tide is out long Musgrave (1926) who quote, ‘The crevices of the outer lines of rocks lie exposed in the bed of the channel rocks in the surf zone are encrusted with the hard limy and provide for the marine zoologist one of the richest tubes which are the dwellings of the vast numbers of collecting grounds in Australia’. Photo: Anthony Musgrave, Galeaolarian worms’. Photo: Anthony Musgrave, from from Australian Museum archives. Australian Museum archives. Australian 2013 Zoologist volume 36 (3) 257 Hutchings et al. this only applies to commercial species. The total number illustrate how the number of species in the Australian of records, as well as the numbers of families, genera and Museum collection has grown over time and give an species was calculated for each of the five taxa (fishes, estimate of known species richness in the harbour. molluscs, polychaetes, crustaceans and echinoderms) separately and in combination. Not all specimens Results have been identified to species, and some represent With the exception of molluscs, the majority of records for morphospecies or are species currently identified only to the selected groups are databased and each of these groups a higher taxonomic level. We used WoRMS (http://www. is now discussed. A complete list of species recorded is marinespecies.org/) to check currently accepted names. given in the Appendix. Each species list was checked by The number of records collected in each year was one of the authors with expertise in the group. The most calculated, with the mean used when a range of dates recent taxonomic names were used where available but was given. For example, a record with a stated collection no attempt was made to re-check the database records date of 1950–1960, was deemed as 1955. Records without against specimens. However, every record can be referred a collection date were counted separately. To display the back to a specimen, (or, in the case of a few fish records, to spatial pattern of records, the study area was divided into a photograph) in our collections. This is the first attempt a 500 m × 500 m grid, with the number of records in each to collate the fauna of Sydney Harbour since Whitelegge grid counted and displayed in ArcMap. These analyses (1889) and hopefully will encourage future studies and were performed to understand the spatial and temporal re-examination of these museum collections. biases in sampling, and do not necessarily represent the true distribution of biodiversity in the harbour. Polychaetes Sydney Harbour was divided into four regions: East, 1250 records of polychaetes representing 40 families, Centre, West and North (Figure 1a). We separately comprised of 308 species belonging to 189 genera, with counted the number of species in each of the taxonomic some only identified to genus or in some cases only to groups in each of the four regions. Accumulation curves family are recorded in the Australian Museum database were produced for each taxon and region based on the (Figure 6, Appendix). The families best represented in earliest record of each species. These accumulation curves the Appendix largely reflect the research focus of both Figure 6. The number of records from the Australian Museum database that were analysed in this study, along with the number of species (including morphospecies), genera and families represented for each group. Taxonomic identifications were based on the database, and were not checked against the actual specimens. Australian 258 Zoologist volume 36 (3) 2013 Sydney Harbour Australian Museum and visiting systematists. Over 80 primarily marine and while the upper reaches of polychaete families are known globally and currently the harbour are fully marine during dry conditions, 40 families are present in the harbour according to salinity levels fall in these regions after periods of the Australian Museum database. However, we know heavy rain. This probably prevents the establishment of several other families from the harbour, such as of diverse polychaete assemblages, although those Acoetidae, Magelonidae, Paraonidae and Pisionidae, species present can be abundant (for example, high although specimens of these are yet to be fully identified numbers were recorded during a bird feeding survey and databased. around Homebush Bay (Hutchings 1996)). The bulk of polychaete species are from the East and Central Polychaetes have been recorded throughout the regions (Figure 8), primarily from the shores or shallow catchment although records from Middle Harbour and water. Few are recorded from deeper water, especially Lane Cove are sparse and restricted to the lower reaches in the Eastern region as little sampling of sediments (Figure 7). In contrast, records from the Parramatta has occurred there. Many polychaete species occur in River are largely restricted to the upper reaches of the sediments and have very specific habitat requirements river, as a result of various surveys conducted prior to (Hutchings 1998) so we anticipate additional new the Sydney Olympics for the Olympic Co-ordinating species will be recorded based on the range of deeper Agency (Australian Museum Business Services 1993). water sediments types present in the harbour. This is not surprising given that polychaetes are Figure 7. The harbour was divided into a grid of 500 m × 500 m squares. Dots show the number of records in each square. Records vary in collection location precision. In some cases the actual collection locations may differ from those shown on the map. Australian 2013 Zoologist volume 36 (3) 259 Hutchings et al. Figure 8. Number of species recorded from each of the four regions of the harbour (Figure 1). Examination of the time periods when polychaetes were Sydney Harbour undertaken for Sydney Ports Corporation collected (Figure 9) reveals a small peak in the first decade (Australian Museum Business Services 2002) (Figure 10). of the twentieth century, followed by very spasmodic Another reason for the increasing number of species and collecting until the 1970s. After this, more intensive records after 1970 was the appointment of a polychaete collecting was undertaken, with a major spike recorded specialist, which has also encouraged overseas workers in 2001. This spike is reflected in all other groups and and postdoctoral researchers to study the collections, is the result of a major a marine biosecurity survey of including those from Sydney Harbour. Australian 260 Zoologist volume 36 (3) 2013 Sydney Harbour Figure 9. The number of specimens collected in each year since 1850, with unknown year of collection included separately to the left of the year 1860. Averages were used when the collection period included a range of years (e.g. 1955 for 1950–1960). If one considers the species accumulation curve (Figure 11), it is still rising, with most species recorded from the Eastern region (i.e., east of the Sydney Harbour Bridge). Most of the species have been recorded since the 1970s coinciding with the availability of SCUBA and the museum’s increased research effort. Far fewer species are recorded from the other regions although the numbers of species increased dramatically in the Central and Eastern regions following a marine biosecurity survey in which those areas associated with commercial shipping were systematically collected (Australian Museum Business Services 2002). Polychaetes predominantly occur as infaunal and encrusting species, although some are pelagic (Figures12-15 illustrate some common species). Figure 10. Museum staff sampling during the Sydney Port Comprehensive benthic sampling has not been carried Survey for Introduced Marine Species for Sydney Ports out in the harbour and most records are from the Corporation at Gore Bay. Photo, Penny Berents. Australian intertidal and from SCUBA diving where kelp holdfasts Museum. Australian 2013 Zoologist volume 36 (3) 261 Hutchings et al. Figure 11. Cumulative numbers of species recorded in the harbour over time. Records and species without a year of collection were not included in this analysis. Figure 13. Perinereis akuna (F. Nereididae). A mature polychaete with posterior segments modified for swimming and full of gametes, occurs under rocks in the intertidal and shallow subtidal. When fully mature it swims in the water column using the expanded parapodial lobes Figure 12. Hydroides ezoensis (F. Serpulidae). Animal and swimming chaetae and dehisces and releases gametes removed from its calcareous tube, an encrusting species into the water column where fertilisation occurs; the found on wharf piles introduced from Japan. Photo, deflated worm body dies. Spawning is co-ordinated by E. Nishi. environmental cues. Photo, Denis Riek. Australian 262 Zoologist volume 36 (3) 2013 Sydney Harbour Figures 16. Blue Swimmer, Portunus armatus, was previously known in Australia as Portunus pelagicus. It is an important commercial species around Australia and is common in Sydney Harbour on soft sediments, especially in the eastern region. Photo, S. Ahyong. Figure 14. Idanthyrsus australiensis (F. Sabellariidae) originally described from Sydney Harbour and may have been collected from the Marine Station at Watson’s Bay, occurs in sandy tubes cemented onto rocky surfaces, gregarious polychaete. Photo, Maria Capa. Figure 17. Mantis Shrimp, Erugosquilla grahami, is one of several large mantis shrimp species found in Sydney Harbour and was discovered in the mid 1990s. It is a marine predator ranging from Australia to Taiwan. In Sydney Harbour, it burrows in sand and mud in the eastern region. Photo, S. Ahyong. we would anticipate also finding many species new to science within the harbour. This is also reflected in the species accumulation curve for polychaetes (Figure 11) especially for the Eastern and Central regions that show little evidence of levelling off. In contrast, the apparent Figure 15. Loimia ingens (F. Terebellidae) a tubiculous levelling off in the Northern and Western regions is polychaete found living in muddy sediments and among possibly a sampling artefact rather than a real plateau. seagrass beds. Photo, Kathie Atkinson. Crustaceans and sponges are often collected to reveal associated polychaetes, plus scrapings from pylons. This suggests that Crustaceans are the dominant marine arthropods and many more species of polychaetes remain to be recorded include crabs, shrimps, lobsters, isopods, amphipods and from Sydney Harbour. Deeper water habitats east of the barnacles (Figures 16-18 illustrating some of the diversity). bridge, under Spit Bridge and areas inside of North and They occur throughout the harbour to the geographical South Heads have barely been sampled. The same applies limits of the study (Figure 7) and are represented by to subtidal soft sediments throughout the harbour. As 2778 records distributed in 163 families, 434 genera, and our knowledge of the coastal polychaete fauna increases 672 species (Figure 6, Appendix). The crustacean fauna Australian 2013 Zoologist volume 36 (3) 263 Hutchings et al. of the harbour is extremely rich, comprising temperate has increased across all regions in several large steps. From water species along with typically warm water species that the 1930s to the late 1960s, crustacean discovery in the are temporary residents brought by the East Australian harbour was low (Figure 11), corresponding with a lack Current, or for which Port Jackson is part of their southern of specimens collected during this period (Figure 9). It range limit (Ahyong 2004; Poore 2004). improved significantly with the appointment of curators such as Yaldwyn and Griffin in the late 1960s early 1970s, With many significant commercial species, such as School resulting in the peak in collection records and numbers Prawns (Metapeneaus spp.), Blue Swimmer Crabs (Portunus of new discoveries in the 1970–80s. The 2001 spike in armatus) (Figure 16), Mud Crabs (Scylla serrata) (Figure records is attributable to the Sydney Harbour Biosecurity 18) and Eastern Rock Lobsters (Sagmariasus verreauxi), Survey conducted for the Sydney Ports Authority (Figure crustaceans in the Australian Museum collection date 10), although the limited number of new species records back to at least 1876. Growth in the Sydney Harbour obtained at that time suggests that most species from the crustacean collections (and the number of species immediate port environment have already been observed. discovered, as new records for the harbour or species new to science) correlates with research effort, with a peak in As expected, the numbers of species recorded from the 1920–30s, a peak in the 1970–80s and a spike in 2001, different parts of the harbour differ significantly, with see Figure 9). As is evident from the species accumulation highest diversity in the Eastern region (Figure 8). This no curve, the number of species discovered in Sydney Harbour doubt is partially influenced by the higher level of sampling in the east, but also the wider range of habitat types including rocky reefs and seagrass beds, and more stable marine conditions that typically favour higher species richness (Edgar et al. 1999; Teske and Wooldridge 2001). The Northern and more westerly regions are increasingly estuarine and more strongly affected by freshwater input (and urban runoff) than the Eastern region. The harbour has consistently yielded new species records, even though research effort has been sporadic, especially in the past 20 years. For instance, Sydney Harbour holds the southernmost records for the tropical reef lobster, Enoplometopus occidentalis, the tropical mantis shrimps, Erugosquilla woodmasoni (Figure 17) and Levisquilla jurichi, and tropical swimming crab, Charybdis granulata (Ahyong 2001, 2006; Ahyong and Lee 2005). A large new species of mantis shrimp, Erugosquilla grahami, was discovered in Sydney Harbour only in 1994, among the commercial Figure 18. Mud Crab, Scylla serrata, is a popular commercial catch of prawns and other mantis shrimp, dominant among species that lives in muddy, mangrove habitats. It occurs them, the introduced Japanese mantis shrimp, Oratosquilla widely in the tropics and occurs all along the New South oratoria (Ahyong and Manning 1998; Ahyong 2001). The Wales coast. In the harbour, it occurs mostly in the central species accumulation curve for Crustacea is currently and western regions as well as in Middle harbour. Photo, S. Ahyong. plateauing and is most likely attributable to the low level of recent research effort (Figure 11). Targetted surveys in the harbour will almost certainly result in numerous new discoveries, especially in the Eastern region. Echinoderms Echinoderms, which include sea urchins, sea-stars and sea cucumbers, are a relatively small group with around 1200 species known from Australia. Sea urchins and sea-stars can be numerically abundant, especially on rocky reefs and other hard substrates (Figures 19-22 illustrate the diversity). For Sydney Harbour 1017 records, distributed in 45 families, 91 genera and 118 species exist in the Australian Museum collections (Figure 6, Appendix). The growth in harbour records and consequent number of echinoderm species discovered in the harbour has substantially increased from 1860 until now (Figure 11), Figures 19. Comb Sea Star, Astropecten polyacanthus, although the majority of old records do not have a specific burrows in sand and mud, and is common around Sydney. collection date (Figure 9). As with Crustacea, the rate It is one of the few echinoderms in the harbour to of discovery follows a step-wise pattern with the largest tolerate low salinities. Photo, S. Ahyong. jump in the late 1960s. This jump follows the expansion Australian 264 Zoologist volume 36 (3) 2013