Seagrass and Reef Program for Port Phillip Bay: Temperate Reefs Literature Review

Neil Hutchinson, Taylor Hunt and Liz Morris

May 2010 Fisheries Victoria Department of Primary Industries

If you would like to receive this Author Contact Details: Neil Hutchinson information/publication in an Fisheries Research Branch, Fisheries Victoria accessible format (such as large PO Box 114, Queenscliff Victoria 3225 print or audio) please call the Authorised by the Victorian Government, Customer Service Centre on: 2a Bellarine Hwy, Queenscliff, Victoria 3225 136 186, TTY: 1800 122 969, Printed by DPI Queenscliff, Victoria or email Published by the Department of Primary [email protected] Industries. Copyright © The State of Victoria, Department Copies are available from the website: of Primary Industries, 2010. www.dpi.vic.gov.au/fishing This publication is copyright. No part may be reproduced by any process except in accordance General disclaimer with the provisions of the Copyright Act 1968. This publication may be of assistance to you but Preferred way to cite: the State of Victoria and its employees do not Hutchinson, N., Hunt, T., and Morris, L. (2010). guarantee that the publication is without flaw of Seagrass and Reef Program for Port Phillip Bay: any kind or is wholly appropriate for your Temperate Reefs Literature Review. Fisheries particular purposes and therefore disclaims all Victoria Technical Report No. 11, 61 pages. liability for any error, loss or other consequence Department of Primary Industries, Queenscliff, which may arise from you relying on any Victoria, Australia. information in this publication. ISSN 1835‐4785 ISBN 978‐1‐74264‐141‐6 (print)

Risk Assessment of Pesticides for Yabby Farmers ii

Executive Summary

The purpose of this document is to review the The amount of research and level of existing scientific understanding, in an understanding has been greatest for intertidal international context, of the temperate reef reefs, is lower for subtidal reefs, and is very habitats in Victoria, particularly in Port Phillip limited for deep and canyon reefs. This is Bay. A variety of research has been conducted on probably a reflection of ease of accessibility and intertidal, subtidal, deep subtidal and canyon logistical constraints. reefs in Victoria both within Port Phillip Bay and Research on subtidal reefs in Port Phillip Bay has along the Victorian coast. been fragmentary, and there is a poor While some clear differences in species understanding of the drivers influencing the reef distributions and assemblage structure have been communities and how these differ from the open identified from eastern to western Victoria, the coast. Further research on the physiological and majority of information on reefs in Victoria ecological drivers affecting subtidal reefs in Port provides only a “snapshot” at one particular Phillip Bay is required. place or time of year. Examination of temporal Of special interest are the deep reef and canyon and spatial variation in the structure of habitats of Port Phillip Heads. This area has a assemblages on different reef types, and more unique combination of deep water, strong basic information on which species occur and currents, and coastal sedimentary processes. The their basic ecology and behaviour are lacking, sessile invertebrate communities are well especially for deep and canyon reefs. developed but their uniqueness is uncertain. More information is required to enable us to Detailed studies of taxonomy and assemblage understand what is shaping many of Victoria’s structure are required along with research into reef communities. There is a need to conduct the physical and ecological processes affecting research that examines Victoria’s marine the system. ecosystems in a broader geographical context across southern Australia, and also in the context of coastal oceanography.

Temperate reefs literature review iii

Table of Contents

Executive Summary...... iii

Introduction...... 1 Temperate reefs ...... 1 Key reef types in Victoria ...... 1 1. Intertidal...... 1 2. Subtidal...... 1 3. Deep: ...... 1 4. Canyon:...... 1

Biogeographic patterns across Victoria...... 2

Oceanographic and productivity context of Victorian reefs...... 5 Central Victoria ...... 5 Western Victoria...... 5 Eastern Victoria ...... 5 Upwelling...... 5

Current monitoring ...... 7 Monitoring ...... 7 Marine Habitat Classification...... 7

Ecosystem services ...... 8

Physical habitats and biological communities...... 9 Intertidal reefs ...... 9 Subtidal reefs...... 11 Exposed subtidal reefs...... 11 Sheltered subtidal reefs ...... 12 Deep reefs...... 14 Invertebrates ...... 14 Fish ...... 15 Canyon reefs ...... 17 Port Phillip Heads...... 17 Other canyons...... 17

Temperate reefs literature review iv

Ecological and physical environmental drivers ...... 19 Intertidal reefs...... 19 Top‐down / disturbance processes...... 20 Bottom‐up / supply side processes...... 22 Competition...... 24 Subtidal reef ...... 25 Physical drivers...... 25 Ecological drivers...... 27 Major commercial fisheries...... 30 Deep reefs and canyons...... 32 Physical drivers...... 32 Ecological drivers...... 33 Knowledge gaps...... 34 Intertidal reefs ...... 34 Subtidal reefs...... 34 Deep reefs and canyons ...... 35

References ...... 37

Appendix 1 Tables...... 51

Appendix 2 Conceptual Models...... 56

Temperate reefs literature review v

List of Figures Figure 1. Key relationships and drivers on intertidal reefs in Victoria...... 57 Figure 2. Key relationships and drivers on subtidal reefs in Victoria ...... 58 Figure 3. Key relationships between invertebrates on subtidal reefs in eastern and western Victoria...... 59 Figure 4. Key relationships and drivers on deep reefs in Victoria ...... 60 Figure 5. Key relationships and drivers on canyon reefs in Victoria...... 61

List of Tables Table 1. Six bioregions relevant to Victoria as presented in Interim Marine Coastal Regionalisation of Australia Technical Group, IMCRA (2006)...... 51 Table 2. Interim intertidal marine habitat (MHC) categories for Victoria, Ferns et al. (2000)...... 52 Table 3. Interim shallow subtidal (0 – 2.5 m) marine habitat (MHC) categories for Victoria, Ferns et al. (2000)...... 52 Table 4. Primary shallow habitat classification scheme as presented in Ball et al. (2000)...... 53 Table 5. Potential physical drivers responsible for shaping deep reef assemblages in Victoria. Summarised from Edmunds et al. (2006b) ...... 54 Table 6. Potential ecological drivers responsible for shaping deep reef assemblages in Victoria. Summarised from Edmunds et al. (2006b) ...... 55

Temperate reefs literature review vi

Introduction

Temperate reefs Key reef types in Victoria Temperate reefs are defined here as hard For the purposes of this literature review we substrata in marine waters averaging have grouped reefs in Victoria into four broad temperatures below 18°C (The University of categories: Queensland 2001; Port of Melbourne Corporation 2007c). They are widely distributed 1. Intertidal in Australia, and extend around southern Reef that is periodically exposed to air at low Australia from Kalbarri in Western Australia to tide but is submerged or directly influenced by Noosa in Queensland. sea water at high tide. Intertidal reefs are also known as rocky shores. In Victoria, temperate reef habitats cover extensive areas of the coastline and are known 2. Subtidal for their high biological complexity, species Reef that is never exposed to the air from tidal diversity, species richness, level of endemism influences, generally covering depths of 2.5‐20 and productivity (Keough and Butler 1996; m. The review will distinguish and discuss Edmunds et al. 2003). differences in communities and processes on These habitats are of social and cultural value to subtidal reefs split into two categories based on people due to a variety of indigenous, aesthetic, wave exposure and currents: recreational and historical aspects (Keough et al. • Exposed subtidal reefs found on the 1990; Edmunds et al. 2006a). They also hold open coast and Port Phillip Heads significant economic value by supporting two of the most valuable commercial fisheries in • Sheltered subtidal reefs found within Australia, in abalone and rock lobster, plus other Port Phillip Bay. valuable activities such as recreational fishing, 3. Deep: Reef that is located 20 m or deeper. diving and a range of other tourism activities (Environment Conservation Council 2000; 4. Canyon: Deep reef located in canyons Edmunds et al. 2003; Department of Primary (geomorphological formations). Particular Industries 2009b). But, despite the great attention will be given to the Port Phillip importance of temperate reefs, they are not well Heads deep reef canyon. known scientifically (Keough and Butler 1996). These categories were selected as they represent The purpose of this literature review is to reef types across Victoria. They distinguish reef critically evaluate the current understanding of types based on their exposure to key physical Victoria’s temperate reefs, with particular modifiers including depth, tidal range, energy reference to reef communities, ecological and (wave and currents) and photic influences. physical environmental drivers, dynamics, key These factors have been shown to be structuring and ecosystem services, key fundamental drivers of the distribution patterns relationships, and any key current relevant of benthic marine communities (OʹHara et al. research/monitoring programs. The review will 1999; Ferns et al. 2000; Ball et al. 2006; Coleman et also construct conceptual models, summarizing al. 2007). key relationships and provide an indication of scientific uncertainty.

Temperate reefs literature review 1

Biogeographic patterns across Victoria

Scientific research on temperate reef ear Parma microlepis and mado Atypichthys communities in Victoria has, to some extent, strigatus. focused on the classification of marine waters Prominent southern, Maugean, species on into bioregions. By examining qualitative Victorian reefs include: algae such as the string measures of biological or physical variables at kelp Macrocystis angustifolia, bull kelp Durvillaea intertidal and subtidal sites across Victoria, potatorum, Splachnidium rugosum, Zonaria broad‐scale biogeographic patterns have been angustata and Cystophora torulosa; the sea stars identified and subsequently supported in later Patiriella brevispina, Nectria ocellata and Fromia studies. polypora; and fish including southern hulafish Early studies of intertidal and subtidal Trachinops caudimaculatus and southern sea carp temperate reef communities along the coast of Aplodactylus arctidens. southern Australia categorised communities into In addition to provincial influences, Victorian three distinct marine biogeographic provinces communities are also composed of species (Bennett and Pope 1952; Dartnall 1974; Edgar distributed throughout all of southern Australia 1984; Womersley and King 1990). including algae such as common kelp Ecklonia These provinces were: radiata, Pterocladia capillacea, Phacelocarpus peperocarpus, Haliptilon roseum, Sargassum sp. and • The western, warm temperate, “Flindersian Cystophora sp.; the common sea urchin Province” Heliocidaris erythrogramma; and the eleven armed • The eastern, warm‐temperate, “Peronian sea star Coscinasterias muricata. Province” The high turnover of species in the central • The southern, cool‐temperate, “Maugean Victorian area was reaffirmed in a study based Province” on examining echinoderm and crustacean species distributions along the coast of southern Edmunds et al. (2000) briefly reviewed these Australia by OʹHara (2000a). OʹHara (2000a) studies and surmised that the coast of Victoria is analysed museum collections sampled from situated at the confluence of these provinces and within 62 spatial units between Western that the existing biological communities there Australia and northern New South Wales. The include a mixture of typically western, eastern study determined that 49% of the total species in and southern species. southern Australia (739) occur in Victoria (362) Typical western, Flindersian, species on and the species distributions and turnover were Victorian reefs include: the algae Caulerpa consistent with previous biogeographical brownii, Zonaria turneriana, Seirococcus axillaris, classifications (Bennett and Pope 1952; Edgar Carpoglossum confluens, Cystophora monilifera, 1984; Womersley and King 1990). Sargassum decipiens, Sargassum varians, Given the fact that these different regions meet Sonderopelta coriacea and Melanthalia obtusata; sea in Victoria, allowing comparative work to be urchins including Holopneustes porossisimus and carried out at similar latitudes within a Holopneustes inflatus; the abalone Haliotis relatively small geographic area, surprisingly laevigata and Haliotis scalaris; and fish such as the little work has been conducted on the ecology of horse‐shoe leatherjacket Meuschenia hippocrepis, rocky reefs in the State. yellow‐striped leatherjacket Meuschenia flavolineata and Victorian scalyfin Parma victoriae. Waters et al. (in press) recently provided an a priori test for the existence of Maugean, Typical eastern, Peronian, species on Victorian Flindersian and Peronian biogeographical reefs include: the algae Phyllospora comosa; the provinces across southern Australia. The study sea urchins Centrostephanus rodgersii and quantitatively analysed distributional data of Holopneustes purpurascens; the sea squirt Pyura 1,500 algal species and identified the three stolonifera; and fish including eastern hulafish distinct biogeographical assemblages, consistent Trachinops taeniolatus, silver sweep Scorpis with previous biogeographical classifications lineolatus, black drummer Girella elevate, white (Bennett and Pope 1952; Edgar 1984; Womersley

Temperate reefs literature review 2

and King 1990). The authors recommended that 2007; Connell and Irving 2008; 2009; Waters et al. broad provinces be applied as a regional in press). framework for understanding and managing Finer‐scale bioregions in Victoria have also been Australia’s marine biodiversity, particularly for described in order to better understand marine integrating the ongoing discovery of biological biodiversity at the ‘habitat’ and ‘community’ variation at finer scales. The authors support levels. Ferns et al. (2000) provided a review of their recommendation through (1) arguing classifying Victoria’s marine ecosystems, against the relevance of a biogeographical recognising the importance of both physical and classification of Australia’s coastline based on biological factors and the use of qualitative and physical variables (IMCRA 1998) and (2) quantitative attributes. The authors documented evidence for ecological variation acknowledge previous classifications at the (aside from species composition) across broad‐scale bioregion level, and then describe southern Australia. two approaches in assessing and understanding The Interim Marine Coastal Regionalisation of marine biological communities at the ‘habitat’ Australia Technical Group, IMCRA (1998), used and ‘community’ levels. measurements of bathymetry, coastal The first approach is to classify intertidal and geomorphology, sediments, currents, tides, subtidal marine ‘habitats’ using qualitative water chemistry and water temperature to attributes collected from remote sensing and classify Victoria into six bioregions (Table 1). field survey techniques. Qualitative descriptions Waters et al. (in press) argue that the broad of seafloor substratum and dominant biota are biological relevance of these bioregions remain generally arranged in a hierarchical system to unclear because they are derived from gross create Marine Habitat Classes (MHCs). MHCs are biophysical features rather than based on large applied over scales of 1 m – 100 km that have numbers of taxa. The authors go on to question distinct physical and/or biological ‘habitat’ the effectiveness of IMCRA (1998) studies in attributes. MHC attributes were identified for defining regional biodiversity and shaping intertidal and subtidal areas by Ferns et al. (2000) conservation policy. (Tables 2 and 3). Evidence exists for ecological variation across Edmunds et al. (2000) also provided a southern Australia aside from species quantitative classification of the biological composition (Connell and Irving 2009). Connell communities in Victoria. The classification was and Irving (2008) sought to provide a derived from quantitative sampling of biological biogeographical framework for the communities of macrophytes, interpretation of variation in the ecology of, and macroinvertebrates and fish associated with threats to, subtidal rocky landscapes. The study rocky reefs using visual census techniques. quantified the frequency and size of patches of These biological data provided attributes for major benthic habitats across the southern coast specifically defined Marine Ecological of Australia to establish biogeographical Communities (MECs), which were applied to patterns that may result from contrasting areas at scales from 1 m – 1 km and consisted of regional‐scale processes. Key findings from the distinct biological communities. The results of study include distinct biogeographical the study indicated that there was a patterning in the extent of kelp forests as related considerable overlap of the provincial to the Flindersian and Peronian provinces. influences, particularly in the area of central Flindersian coasts have higher kelp forest cover Victoria where the Flindersian components and higher kelp forest heterogeneity relative to extend as far east as Cape Liptrap, and the Peronian coasts. The patchwork of forests in the Peronian components extend as far west as Cape Peronian province is created by the foraging Otway. Ferns et al. (2000) state that MECs activities of the black urchin Centrostephanus potentially serve as useful indicators for rogersii, a species that is not recorded from the reporting on the long‐term status of marine Flindersian province. Distinct differences in communities. concentrations of nutrients, chlorophyll a, kelp forest canopy‐morphology, kelp forest Presently, MECs for macrophytes, invertebrates understorey associations and broad degree of and fish have been delineated for a selection of wave exposure between Flindersian and subtidal reefs across four areas of coastline in Peronian coasts also support the finding of Victoria including Port Phillip Heads, Phillip ecological variation, aside from species Island, Bunurong and Wilsons Promontory composition, across southern Australia (Connell (Ferns et al. 2000). But due to the lack of similar

Temperate reefs literature review 3

studies determining MECs along the remainder Habitat Mapping Project” and other projects are of the Victorian coast, local temperate reef covering reefs along the majority of Victoria’s community information is scarce. This is, coastline (Bax and Williams 2000; Bax and however, gradually being addressed. Williams 2001; Beaman et al. 2005; Ball and Blake 2007a; b; Holmes et al. 2007; Monk et al. 2008; In recent years, a number of studies have Blake et al. 2009a; b; Rattray et al. 2009). These examined Victoria’s subtidal reefs using surveys have described a wide range of reefs combinations of georeferenced aerial and along the Victorian coast at the habitat level and satellite images, echo‐sounders, GIS and broadly describe the make‐up and distribution ground‐truthed video drops/transects and diver of biota in relation to substrate type at the surveys. For example, the “Victorian Marine community level.

Temperate reefs literature review 4

Oceanographic and productivity context of Victorian reefs

circulation in Victoria is characterised by a west Central Victoria to east coastal current (Cirano and Middleton The oceanography of the central area of Victoria 2004). The eastward coastal current is partly is dominated by the relatively shallow waters of driven by the Leeuwin current to the west Bass Strait. The Strait consists of a shallow (Cirano and Middleton 2004). The Leeuwin platform, mostly about 70 m below sea level, current is a warm water current, and the flanked by 4‐5 km deep ocean to the east and significant inter‐annual variation that has been west and by land to the north and south. recorded in the eastern coastal current (Cirano Although tidal currents can be strong in certain and Middleton 2004) would be likely to lead to areas, such as the eastern and western entrances inter‐annual variation in water temperature to to Bass Strait (Black 1992), the net tidal the west of Bass Strait. The Leeuwin current, circulation tends to be small. In central Victoria, and by extension the eastern coastal current, is a the local tidal dynamics are strongly influenced warm, low‐salinity current that is considered to by the two large bays, Port Phillip Bay and be nutrient poor (Connell 2007; Suthers and Western Port. The primary determinants of net Waite 2007). water movement in the region are wind‐driven currents and coastal trapped waves (Middleton Eastern Victoria and Black 1994). The density structure of Bass Eastern Victoria is influenced by the major Strait ranges from well mixed in winter to eastern boundary current: the East Australian strongly stratified in central areas in summer Current (EAC) (Suthers and Waite 2007; ASR (Baines and Fandry 1983). Bass Strait is generally 2008). The EAC often generates warm‐core considered to have a low nutrient status because eddies, or circular flows, up to several hundred nutrient rich water from the deep ocean is kilometres across. These eddies drift south and generally absent or diluted (ASR 2008). can be found off the central east coast of Port Phillip Bay is a large (2000 km2), semi‐ Tasmania (Suthers and Waite 2008; ASR 2008). enclosed, predominantly tidal embayment Although most of the water from the EAC is linked to the ocean of Bass Strait by a narrow directed into the Tasman Sea, some EAC water entrance. The hydrodynamics are characterised also enters eastern Victoria, especially over by an entrance region where fast (3 m s‐1) ebb summer. The EAC is characterised by upwelling and flood jets dominate the circulation, a large in a number of areas (Suthers and Waite 2007) flood‐tidal delta known as the Sands region, and is generally considered more nutrient rich where strong currents occur in the major and productive than the Leeuwin current channels, and an ‘inner’ zone where tidal flows (Connell 2007). are weak and circulation is predominantly by wind‐driven currents (Black et al. 1993). Tides Upwelling are semidiurnal and the amplitude inside the bay is less than 1 m. Salinity in Port Phillip Bay As well as the influence of broad‐scale currents is essentially marine and recently has become and their associated nutrient regimes, local‐scale hypersaline in comparison with Bass Strait areas of upwelling, with associated nutrient and (Nicholson and Longmore 2009). Although there productivity increases, can occur though‐out is significant nutrient input to the Bay from Victoria when wind and oceanographic sewage treatment, effects of eutrophication are conditions are suitable. Upwelling is an presently only seen in localised areas. oceanographic phenomenon where surface winds along coastal areas drive dense, cool, and Western Victoria nutrient‐rich water towards the surface. Upwelling has been recorded in eastern Victoria The oceanography of western Victoria is (Gibbs et al. 1986; Rochford 1977; Butler et al. influenced by the major western boundary 2002b) and to a lesser extent in central areas of current: the Leeuwin current. The winter Bass Strait (ASR 2008). By far the strongest area

Temperate reefs literature review 5

of upwelling and nutrient enhancement in Victoria occurs in the west. The Bonney upwelling is the most prominent upwelling in southeast Australia and is driven by the prevailing south‐easterly winds in the region. Between November/December and March/April, upwelling plumes are regularly observed along the Bonney Coast from Robe, SA to Portland, Vic which make the area highly productive (Butler et al. 2002b), and all reefs in the area may be influenced to some degree by this phenomenon. The Bonney Coast is within the Otway region as classified by the IMCRA (Butler et al. 2002b) and was described by Womersley (1984) as being part of the Maugean province, of which it forms the western extension (Butler et al. 2002b).

Temperate reefs literature review 6

Current monitoring

2003), Ball et al. (2006) state that macrophyte Monitoring communities identified in the study have been The Victorian Subtidal Reef Monitoring generally compatible with dominant reef biota Program (SRMP) and Intertidal Reef Monitoring MHC categories. Program (IRMP) were established by the Victorian Government to provide information The Abalone Assessment Monitoring program on the status of Victorian reef flora and fauna run by Department of Primary Industries (DPI) (focussing on macroalgae, macroinvertebrates is an annual fishery independent survey across and fish). The SRMP uses standardised 250 subtidal reef sites in Victoria that underwater visual census methods based on an commenced in 2002. The data are collected by approach developed and applied in Tasmania underwater visual census and includes by Edgar and Barrett (1997). This includes quantitative estimates of abundance of abalone monitoring the nature and magnitude of trends and prevalent organisms other than abalone in species abundances, species diversity and such as macroalgae, predators and competitors community structure through time, with and abiotic features. particular emphasis on Marine National Parks and Sanctuaries in Victoria (Edmunds et al. Marine Habitat Classification 2003). Since the Victorian interim marine habitat classification scheme presented in Ferns and The SRMP was initiated in May 1998 with 15 Hough (2000) there has been several steps sites established on subtidal reef habitats in the forward in improving marine habitat vicinity of Port Phillip Heads Marine National classification not only on a temperate reef level Park. Since then, the SRMP has been expanded but on a nationwide marine habitat level. These to reefs in the vicinity of the Bunurong Marine advancements will allow future studies to National Park (12 sites), Phillip Island (6 sites), further our understanding of the distribution and Wilsons Promontory Marine National Park and abundance of different temperate reef (20 sites) and a further twelve Marine National habitats in Victoria. Parks and Marine Sanctuaries including: Point Cooke, Jawbone, Ricketts Point, Merri, Marengo Ball et al. (2006) reviewed and documented the Reef, Eagle Rock, Beware Reef and The Arches relationship between relevant Australian and Marine Sanctuaries and Point Addis, Cape international local‐level marine habitat Howe, Point Hicks and Twelve Apostles Marine classification systems and the Victorian interim National Parks. This program is currently marine habitat classification scheme presented implemented by Parks Victoria, in association in Ferns and Hough (2000). The authors then with the Department of Sustainability and presented a revised marine habitat classification Environment (Edmunds et al. 2006a). The data system to support mapping of shallow (assumed include quantitative estimates of large mobile 0 ‐ 20 m depth) habitats at Victoria’s Marine fishes, cryptic fishes, megafaunal invertebrates National Parks and Sanctuaries. The primary and macroalgal species. habitat classification scheme divides classification into five levels of modifiers to The IRMP was initiated in April 2003 with 14 classify habitats mapped from underwater sites established on intertidal reef habitats (Table 3). The purpose of this habitat mapping within, and in the vicinity of, the following classification is to assist in the selection and marine protected areas: Point Addis Marine evaluation of candidate representative marine National Park and Point Danger, Barwon Heads, protected area locations, to allow more accurate Point Cooke, Jawbone, Ricketts Point and description of the spatial extent and distribution Mushroom Reef Marine Sanctuaries. of shallow seabed habitats, and to provide more Although the monitoring program will begin to detailed biological information on marine adequately reflect average trends and patterns protected areas to support assessment of as the surveys continue over longer periods such management performance. as multiple years to decades (Edmunds et al.

Temperate reefs literature review 7

Ecosystem services

Ecosystem services are the direct and indirect (Port of Melbourne Corporation 2007a; b; benefits supplied to human societies by natural Connell and Irving 2009). The south of the Bay, ecosystems (Daily et al. 1997) including, for together with the Entrance, is popular for example, key fishery species in the reef recreational diving because the water is community, or productivity values associated generally clear and the area contains high with the reef. quality diving sites associated with the deep canyon in the Entrance, marine national parks Temperate reefs are known for their high and shipwrecks. Key dive sites across the south biological complexity, species diversity, species of the Bay include Lonsdale Wall, which extends richness, level of endemism and productivity to depths of 45 m, and Popes Eye, which is a (Keough and Butler 1996; Edmunds et al. 2003). renowned location for trainee divers, snorkellers Temperate reef habitats have social and cultural and for bird watching and general sightseeing values including indigenous, aesthetic, (Port of Melbourne Corporation 2007a). recreational and historical aspects (Keough et al. 1990; Edmunds et al. 2006a). They also hold An example of the importance of reefs in Port significant economic value by supporting two of Phillip Bay in terms of ecosystem services is the the most valuable commercial fisheries in recent State Government initiative to create Australia, in abalone and rock lobster, plus other artificial reefs for recreational angling in the Bay. valuable activities such as recreational fishing, This indicates that natural reefs are considered diving and other tourism activities to be an important and limited resource (P. (Environment Conservation Council 2000; Hamer, pers comm.) Edmunds et al. 2003; Department of Primary Other examples of the ecosystem services Industries 2009b). Keough and Butler (1996) add provided by reefs in Port Phillip Bay and that the temperate reefs in Australia are elsewhere include protection from beach erosion important for commercial and recreational by acting as a wave break, and also associated fisheries and for recreational diving, and they algae act as a nutrient sink and site of detritus are potential sources of natural products for the production that underpins the detrital food pharmaceutical industry chain in soft bottom habitats. The subtidal and deep reefs (including the canyon) throughout Port Phillip Bay are described as ecological assets of Port Phillip Bay

Temperate reefs literature review 8

Physical habitats and biological communities

Intertidal reefs Intertidal reefs vary in structure from steep between sites, some of them were commonly sloping rock faces to relatively flat or gently found. For example: sloping boulder fields and rock platforms, • Upper eulittoral zone: species include with a variety of features including cobble Enteromorpha spp. fields, vertical steps, undulations in the reef, crevices, patches of sand and rock pools • Mid eulittoral zone: species include caused by a variety of processes such as Porphyra spp, Ulva spp, Gelidium pusillum weathering (Edmunds et al. 2004). • Lower eulittoral zone: species include Bennett and Pope (1952) surveyed 16 sites on Codium sp., Caulerpa sp., Polysiphonia sp. exposed intertidal reefs along the coast of More recent studies (OʹHara et al. in press) Victoria and in spite of differences in localities, five major zones and subsequent community have collected data on 65 intertidal reefs across assemblages were identified: Victoria as part of an effort to detect impacts on assemblages, and there are ongoing • Melaraphe‐lichen zone: species present qualitative surveys being conducted at Barwon include herbivorous molluscs (Nodilittorina Heads by local school children. spp., previously called Melaraphe spp.), Several recent monitoring studies of Victoria’s lichens, crustaceans such as small crabs, amphipods and isopods, and occasionally Marine Protected Areas have described the predatory gastropods. dominant biota present on Victorian temperate reefs. One of the most common algal species • Barnacle‐mussel zone: species present on intertidal reefs is the perennial fucoid alga include barnacles and mussels. Neptune’s necklace, Hormosira banksii, which can form extensive monotypic stands at mid‐ • The mixed algal turf or Galeolari zone: tidal levels of rock platforms (Keough and species present include mixed algae in Quinn 1998). Other common algae species that exposed areas with the serpulid Galeolaria can form mats with or without the presence of caespitosa in sheltered areas. H. banksii include the green algae Ulva spp. • The Poneroplax or “Bare” zone: species and Enteromorpha spp, coralline algae and vary along the coast and with wave action. filamentous brown algal turfs (Edmunds et al. Chitons of the genus Poneroplax are 2004). Less conspicuous is a thin layer of always present, and on many shores east microscopic algae growing directly on the of Cape Otway ascidians are found. surface of the reef, which is an important food source for species of grazing molluscs • The large brown algae zone: species (Edmunds et al. 2004; Gilmour and Edmunds present include large fucoid kelp algae. 2007; Stewart et al. 2007). Such patterns of vertical distributions in The invertebrate fauna on intertidal reefs, organisms are well chronicled on rocky shores which tend to exhibit patterns of zonation in internationally, for example bare zones at the the same way as shown by algae (King et al. mid shore level (Mettam 1994; Kaehler and 1971), are dominated by herbivorous and Williams 1997). predatory molluscs. Common herbivorous Zonation of algae in Port Phillip Bay was species on Victoria’s shores include the top briefly reviewed by Spencer (1970), and has shell Austrocochlea porcata, the variegated been examined on basalt reefs (King et al. 1971; limpet Cellana tramoserica and conniwinks OʹBrien 1975; Brown et al. 1980). Clear vertical Bembicium spp. Less common species include zones were apparent on reefs in the Bay and the warrener Turbo undulatus, the black nerite while species present varied to some extent Nerita atramentosa and the predatory

Temperate reefs literature review 9

gastropods Cominella lineolata and Lepsiella Several authors have investigated specific vinosa (Edmunds et al. 2004; Gilmour and groups of species in Victoria. For example, a Edmunds 2007). review by Sanderson (1997) described algal communities in more depth and Light (1992) Sessile invertebrate species create encrusting reviewed literature on the benthic flora of Port mats on the surface of the reef such as the Phillip Bay, which included information from mussels Xenostrobus pulex and Brachidontes both soft and hard substrates. rostratus and tubeworms Galeolaria caespitose, whilst there are a variety of other mobile Surveys of Port Phillip Bay in the 1950‐60s invertebrates such as small crabs and fish described 173 species of subtidal algae, which species that are either present in the intertidal included numerous species attached to hard zone throughout the tidal cycle and refuge in reefs, particularly in the Port Phillip Heads rockpools, or move into the area at high tide region (Womersley 1966). Womersley (1966) (Edmunds et al. 2004; Gilmour and Edmunds noted that species richness was lower inside 2007; Stewart et al. 2007). than outside the Bay and suggested that this may be due to a variety of factors including As is common on shores elsewhere, both in differences in water depth and temperature. Australia and worldwide (Little et al. 2009), He also mentioned the comparable lack of differences exist between biota present on rocky reefs within Port Phillip Bay. Hope Black exposed intertidal reefs along the Victorian (1971) used this data to examine distributions coastline and sheltered intertidal reefs within with substrate, in particular concentrating on Port Phillip Bay. Gilmour and Edmunds (2007) the importance of reefs in Port Phillip Bay as surveyed intertidal reef biota of Central habitat and summarised the distribution of Victoria’s Marine Protected Areas and found reefs in Port Phillip Bay as 4 main groups in species richness of algae and invertebrates, and respect to rock type: algal cover, to be higher on the exposed intertidal reefs along the coastline than on the 1. Dune limestone: in and adjacent to Port sheltered intertidal reefs inside Port Phillip Phillip Heads, including Popes Eye Bay. Stewart et al. (2007) reaffirmed their (artificial basalt structure) findings and also found that mat forming 2. Oligocene basalt: from Corio Bay to mussels were components of more intertidal Williamstown reef communities outside Port Phillip Bay than inside the Bay. 3. Tertiary ironstone of the Miocene clays and sandstones: north and east shores Intertidal reefs in Victoria are known to show the same general patterns as those in eastern 4. Granites: extending from Martha Pont Australia (Bennett and Pope 1952). seawards. Form off‐shore reefs. Underwood and Kennelly (1990) stated that “kelps are represented by Durvillaea potatorum, Light and Woelkerling (1992) summarised descriptions previously made of algae in the Ecklonia radiata and Phyllospora comosa; Macrocystis angustifolium is present in some intertidal and subtidal zones of Corio Bay places. Cystophora intermedia are found in (Womersley 1966; Hope Black 1971), the Werribee region (Womersley 1966; Spencer eastern Victoria and reappear in South Australia. Tunicates, such as the cunjevoi 1970; Hope Black 1971; Brown et al. 1980), Pyura stolonifera, are only found in some places Altona Bay – Hobsons Bay (Spencer 1970), Carrum and Portsea, and discussed in Victoria and low‐shore regions are occupied by large chitons and encrusting calcareous unpublished data for Werribee (Brown et al. algae. Above the regions dominated by algae 1980), Gloucester Reserve (OʹBrien 1975), Williamstown and Portarlington (Lewis 1975). are areas occupied by barnacles. Conspicuous amongst these barnacles are bands of foliose algae (e.g. Splachnidium rugosum and Ileafascia in summer).”

Temperate reefs literature review 10

Subtidal reefs Subtidal reefs are defined here as reef that is On exposed subtidal reefs at the entrance to Port never exposed to the air from tidal influences Phillip Bay, high vertically‐structured brown and generally covering depths of 2.5‐20 metres. algae (kelps) such as Macrocystis angustifolia, They can be split into two categories: Ecklonia radiata and Phyllospora comosa are often dominant. The green alga Caulerpa is also

1. Exposed subtidal reefs usually present plus a wide variety of low 2. Sheltered subtidal reefs structured, understorey red algae species including Plocamium, Pterocladia, Melanthalia and Exposed subtidal reefs are physically Coralina (Port of Melbourne Corporation 2007b). characterised by a high degree of exposure to wave and current energy. Vegetation has been surveyed at a number of subtidal reef sites along the coast of Victoria Exposed subtidal reefs exist along the majority resulting in the identification of two distinct of the Victorian coastline and include the reefs at vegetation groups together with the following the entrance of Port Phillip Bay, due to their observations recorded by OʹHara (2000b; 2001): high degree of exposure to ocean swells and tidal energy (McShane et al. 1986; Port of • Ecklonia/Phyllospora: Form dominant Melbourne Corporation 2007a). Certain taxa canopies in many exposed open‐coast have been described in some detail off the coast localities across Victoria. Phyllospora comosa of Victoria yet gaps still remain in our forms a dense canopy on high relief, shallow knowledge. For example, a review of (3 to 8 m), exposed or semi‐exposed reefs opisthobranch molluscs (Burn 2006) in Victoria but is often absent from low‐relief reef. described the range of species that occur in Ecklonia radiata often occurs in combination habitats such as the rocky intertidal zone and with Phyllospora or in combination with subtidal rocky reefs from Cape Otway to Macrocystis, Cystophora and other brown Wilsons Promontory, but noted that little is algae when Phyllospora is absent and is the known of species in shallow waters off eastern dominant species on deeper areas of reef Victoria (Wilsons Promontory to Cape Howe). (Ball et al. In prep). Algae • Cystophora/Sargassum: A diverse mixed‐algal In Victoria, subtidal reef communities are assemblage occurs in some Victorian typified by their prominent biota of algae subtidal reefs where the usual (Keough and Butler 1996; Edmunds et al. 2006a; Phyllospora/Ecklonia canopy is absent. These Connell 2007). Sanderson (1997) described how sites are visually characterised by the fucoid reefs show broad patterns of zonation along the algae Cystophora, Sargassum, Seirococcus and depth gradient: Hormosira banksii is the Acrocarpia, with many other brown, red and dominant species observed on intertidal rock green algae interspersed (including Ecklonia platforms; Durvillaea potatorum with mixed and Macrocystis). brown and green algae inhabits the seaward Invertebrates edge of intertidal rock platforms; Phyllospora Exposed subtidal reefs in Victoria typically have comosa occurs in large beds at depths of ~3–5 m; high abundances of large‐mobile predatory and at exposed sites, Ecklonia radiata is typically grazing invertebrates (Edmunds et al. 2006a). observed at depths >7 m and often growing with Predatory mobile invertebrates include: rock P. comosa; and giant kelp Macrocystis angustifolia lobster Jasus edwardsii, red bait crab Plagusia occurs at Port Phillip Heads MNP ‐ Point chabrus, dogwhelk Dicanthais orbita, octopus Lonsdale and at Point Nepean. Octopus maorum and seastars Coscinasterias Other research on subtidal algae on exposed muricata. Grazing mobile invertebrates include: subtidal reefs in Victoria is thoroughly reviewed abalone Haliotis rubra and H. laevigata, warrener by Light and Woelkerling (1992) and Sanderson Turbo undulatus and sea urchins Centrostephanus (1997). These also include reports on subtidal rogersii, Heliocidaris erythrogramma, Holopneustes reef algae at Black Rock between Ocean Grove and Amblypneustes (Edmunds et al. 2000; and Torquay (Rollings et al. 1993; Chidgey and Australian Government 2005; Port of Melbourne Marshall 1994) and other areas throughout Corporation 2007b; c). Victoria and the region (Cheshire and Hallum The low abundance of the grazing urchin 1989; Land Conservation Council 1993). Centrostephanus rodgersii on exposed reefs

Temperate reefs literature review 11

throughout the majority of Victoria results in with depth and habitat, with juveniles feeding in urchin barren habitat being restricted to the far‐ shallow areas of fringing habitat and adults in east where it is present in high abundance deeper turf and barrens habitats, reflecting the (Keough and Butler 1996; OʹHara 2000b; Ferns distribution of the species with depth. 2003; Department of the Environment and Some reef‐related fish species show regular Heritage 2005). Several studies have been patterns of seasonal movement of adults on and conducted on the creation and maintenance of off reefs, such as Hypoplectrodes maccullochi at urchin barrens elsewhere in southern Australia Cape Banks NSW, possibly due to changes in and New Zealand (Andrew and MacDiarmid prey abundance or because adults move to other 1991; Andrew 1993; Andrew and OʹNeill 2000). areas to spawn (Webb and Kingsford 1992; In Victoria, urchin barrens have been described Holbrook et al. 1994) at Cape Howe Marine National Park (Ball and Blake 2007b). There are also various small Sheltered subtidal reefs are physically species of crustaceans and molluscs that occupy characterised by a low degree of exposure to niches as grazers, predators or foragers wave and current energy. (Edmunds et al. 2006a). Sheltered subtidal reefs occupy a relatively Sessile invertebrates present on exposed small part of Port Phillip Bay, about 8 km2, or subtidal reefs can be found in several body less than 0.5%, of the seafloor (McShane et al. forms: 1986; Port of Melbourne Corporation 2007c). These reefs are generally within 1 km of shore in • Prominent colonial or modular sessile fauna shallow water depths less than 4 m (Port of such as sponges, ascidians, soft corals, Melbourne Corporation 2007c). Port of hydroids and bryozoans are abundant on Melbourne Corporation (2007c) described the subtidal reefs, usually in high abundances distribution and lithology of Port Phillip Bay within well‐shaded rock faces, overhangs reefs. Basalt reefs exist along the northern and caves, and on the underside of boulders shoreline at Williamstown extending west to (Keough and Butler 1996; Keough 1999) Point Lillias and sandstone reefs exist along the • Solitary or unitary forms of sessile fauna north‐eastern shoreline from Ricketts Point to include barnacles, some ascidians (eg. Point Ormond. There are also patches of reefs on Pyura), bivalve molluscs and polychaetes the south‐eastern shoreline from Dromana to (Keough and Butler 1996). Frankston and on the Bellarine Peninsula from Clifton Springs to St Leonards (Port of Fish Melbourne Corporation 2007a). Fish are a dominant biotic component of exposed subtidal reef ecosystems in Victoria Several artificial reefs exist within Port Phillip with wrasse (Labridae), morwong Bay, including newly deployed reefs for (Cheilodactylidae) and leatherjacket recreational fishing in the north of the Bay. (Monacanthidae) making up the majority of Previous studies such that carried out by Lewis species (Edmunds et al. 2000; Edmunds et al. (1983) have noted that algae on artificial 2006a). Wrasse are a roaming predatory species structures in Port Phillip Bay usually includes that feed on small molluscs and crustaceans, several introduced species. while morwongs are herbivorous or omnivorous Algae and leather jackets are generally omnivorous or Research on algae in Port Phillip Bay is carnivorous picker‐type species (Edmunds et al. reviewed in Light and Woelkerling (1992) and 2000). Exposed subtidal reef fish species also Sanderson (1997), and includes reports on commonly include herring cale Odax cyanomelas, subtidal reef algae in: the Werribee region sea sweep and scaly fin (Port of Melbourne (Brown et al. 1980); Williamstown, St Leonards, Corporation 2007c). Corio Bay (King et al. 1971; Lewis 1975); Altona Reef fish tend to include algavores, carnivores and Portarlington (Spencer 1972); and Hobsons and omnivorous species. Russell (1983) noted Bay (OʹBrien 1975). that “most rocky reef fishes have broadly The surfaces of sheltered subtidal reefs in Port generalised feeding habits, and foods taken Phillip Bay are typically patchier near the mainly reflect those organisms of suitable size exposed entrance, with various red and brown that are abundant and most readily available”. algae and the green algae species Caulerpa and Gillanders (1995) has shown that the diet of Ulva, while other areas are characterised by the rocky reef fish of different size classes can vary kelp Ecklonia radiata or the introduced species

Temperate reefs literature review 12

Undaria pinnatifida (Campbell 1999; Port of macroalgal cover, and possibly the effects of Melbourne Corporation 2007c). spear fishing (Jenkins et al. 1996) Invertebrates Fish often display complex relationships with Research on invertebrates on subtidal reefs their surroundings. A whole suite of factors are within Port Phillip Bay is sparse, although some known to affect temperate reef fish assemblage research is available that has examined structure and populations. For example, habitat relationships between invertebrates in the bay, type and movement patterns can influence the such as studies by Day et al. (1995) and McShane size range and age classes found at different and Smith (1986) on starfish predation. sites (Wheatley 2000). Fish Wheatley (2000) examined fish assemblage Sheltered reef fish species commonly include structure, species richness and density on southern hulafish Trachinops caudimaculatus, sheltered reefs in Port Phillip Bay in relation to weed fish Heteroclinus perpicillatus, old wives macro‐algae, depth, substrate type etc., as well Enoplosus armatus, toadfish (Aracanidae), as how habitat mediates recruitment, leatherjackets (Monacanthidae), globe fish competition and predation, with an emphasis on (Diodontidae), zebra fish Girella zebra, blennies the leatherjackets Meiischenia freycineti and (Blennidae) and seahorses Hippocampus sp.. Meiischenia hippocrepis. This study found that fish assemblages were most similar on reefs that Coleman (1972) collected fish from sheltered were closer together than distant reefs, and rocky reefs at Williamstown, Sandringham, suggested that these patterns were due to Rickett’s Point, Mornington, Mt. Martha, Safety similarities in larval supply, wave action and Beach and Sorrento Bay. Fish from 31 families tidal movement as well as to differences in were recorded and observations of basic ecology macroalgal assemblage structure. M. hippocrepis and biology were made including habitat use were only recorded on reefs, while M. freycineti and feeding behaviour. This study briefly were mainly found on reefs as adults following discussed how food availability, substrate type recruitment to seagrass beds. Mean growth rates and exposure may influence the distribution of differed between adults of the two species on these species. different reefs, and adults appeared to be Sheltered subtidal reefs are also important to permanent residents on individual reefs, with snapper Pagrus auratus and King George whiting no evidence of movement between reefs being Sillaginodes punctata at different stages of their found. While M. freycineti juveniles and sub‐ life cycles (Port of Melbourne Corporation adults moved between coastal seagrass beds and 2007c). offshore reefs over sand patches, the same sand patches appeared to restrict movement of adults, The structure of fish communities inhabiting a pattern of movement also described for this reef‐algal and unvegetated sandy areas at six and other Monacanthid species in NSW (Bell et sites has been studied by underwater visual al. 1978). census over 18 months in Port Phillip Bay (Jenkins et al. 1996). A total of 75 species Such patterns of ontogenetic movement between representing 36 families were recorded. Species habitats as individuals grow has been reported richness and total abundance varied both for other species in the Bay such as Sillaginodes spatially and temporally but were always punctatus (that moves between seagrass greater on the reefs (Jenkins et al. 1996). In beds/reef‐algae and sand areas ) (Jenkins et al. general, the northern bay sites were 1996; Jenkins and Wheatley 1998), as well as characterised by small cryptic species with an elsewhere in the region, e.g., Pseudolabrus increase in conspicuous water column species in celidotus (Jones 1984) in New Zealand and the south of the Bay (Jenkins et al. 1996). Achoerodus viridis (Gillanders 1997b; Gillanders Differences in community structure between 1997a) in NSW. these sites may be related to reef topography,

Temperate reefs literature review 13

Deep reefs Deep reef habitat is defined here as rocky predominantly of encrusting algae and, where habitat at depths greater than 20 m (Ball and urchins are low in number, many sessile Blake 2007a; Port of Melbourne Corporation invertebrates such as sponges and seawhips. 2007b). In western Victoria, recognised deep reef Edmunds et al. (2006b) states that few studies sites include Discovery Bay Deep, offshore Cape have been done on deep reef biology due to the Bridgewater and Cape Nelson, Port Fairy Deep, logistical difficulties associated with working at offshore Moonlight Head, Cape Otway, Apollo these depths. While some deep reef invertebrate Bay and Nine Mile Reef (Edmunds et al. 2006b; species have been identified, most remain Ball and Blake 2007a; Ball et al. in prep). Other unidentified due to the paucity of collected features include a submarine scarp between specimens. Consequently, our ecological Barwon Heads and Cape Otway on the Otway understanding of deep reef assemblages is Shelf (Jennings 1958) and a cliff at ~45 m depth limited, especially with respect to patterns and that extends for ~20 km between Point factors that influence the diversity and Roadnight and Sugarloaf Creek (Gill et al. 1980). abundance of deep reef species. In central Victoria, deep reef sites include Port In general, worldwide research on deep reefs Phillip Heads, including The Canyon, Point remains sparse in comparison with that on Addis and Wilson’s Promontory (Edmunds et al. shallow reefs. 2006b; Ball and Blake 2007a). Deep reefs habitats are also located in Port Phillip Bay itself at Invertebrates Schnapper Deep, Portsea Hole, Spectacular Reef Deep reef biota is typified by invertebrate and Far Side Reef, and The Rip (Edmunds et al. animals rather than algae, usually in the form of 2006b; Port of Melbourne Corporation 2007a). In sessile, filter feeding fauna (Tissot et al. 2006; eastern Victoria, smaller areas of deep reef exist Sanchez et al. 2009). Organisms such as sponges, near Point Hicks and Cape Howe (Edmunds et octocorals, bryozoans and ascidians usually al. 2006b). Mapping has been performed using dominate rock faces on deep reefs (Keough and video transects and side‐scan sonar to provide Butler 1996; OʹHara et al. 1999; Edmunds et al. quantitative descriptions of reef biota on sites 2006b). For example, the rocky wall within including: granite reefs such as “Point Hicks Portsea Hole is characterised by an abundance Reef”and“New Zealand Star Bank”; low relief of sponges, ascidians and bryozoans (Elias et al. sandstone/limestone reefs such as “Broken 2004; Edmunds et al. 2006b). This is partly due to Reef”; and high/low relief limestone reefs such the ability of species such as sponges to survive as the ”Howe/Gabo complex” (Bax and Williams in low light conditions that algae is unable to 2001). Broader‐scale surveys have also been survive in (Sorokin et al. 2008). conducted of substrate type and benthic organisms throughout the Bass Strait which Communities of sessile invertebrate animals are have included reefs such as “New Zealand Star sometimes collectively known as a ‘sponge bed’ Bank” (OʹHara 2002; Passlow et al. 2006). (Butler et al. 2002a). Sponge bed species can be encrusting or grow in a variety of forms whilst At New Zealand Bank, Beaman et al. (2005) attached to the substratum (Edmunds et al. described the biota that occurred on broadly 2006b). The most common algae present on deep categorised habitats. In this particular study, reefs are encrusting coralline red algae which is “high relief granite” outcrops at ~30‐45 m were able to tolerate low levels of penetrating light described as closely resembling those of similar (Edmunds et al. 2006b). Sponge bed habitats along the coast of NSW, where communities are the typical deep reef biota at communities include large sponges, ascidians, sites across Victoria but there are differences in cnidarians, bryozoans and reduced algal cover assemblages between deep reef sites (Edmunds (Underwood et al. 1991; Andrew 1999; Beaman et et al. 2006b; Ball and Blake 2007a; Ball et al. in al. 2005). prep). Butler et al. (2002a) have surveyed “Deep reef/urchin barrens” described at this site sponges throughout the Bass Strait. at ~40‐50 m (Beaman et al. 2005) closely resemble Recent surveys have concentrated on the area of those described in NSW and elsewhere reef known as The Rip, in Port Phillip Heads, (Underwood et al. 1991), with large concentrated which is more complex than other reefs within patches of the urchin Centrostephanus rodgersii on the Bay and includes “a variety of substrate deep reef, inhabiting areas consisting structures including vertical walls, caves, ledges,

Temperate reefs literature review 14

reef slopes, reef flats and steep‐sided chasms” Phillip Heads are unknown from any other area (Edmunds et al. 2006b). These diverse (Flora and fauna guarantee ‐ scientific advisory microhabitat types may result in a high diversity committee 2009). However, detailed taxonomic of species and (Edmunds et al. 2006b). studies are still incomplete on these species in Port Phillip Heads and as sponges are known to Edmunds et al. (2006b) found assemblages of exhibit variable growth patterns in relation to benthic fauna were different between all deep currents, wave action, predation, etc. (Palumbi reefs within Central Victoria and Port Phillip 1986; Kaandorp 1999; Bell and Barnes 2000; Hill Bay collectively. The Port Phillip Bay deep reef and Hill 2002), and species can adapt their gross assemblages were dominated by sponges, morphology to changes in their environment occupying 70 to 90% of the rocky substratum. within weeks (Palumbi 1984; Kaandorp and The Point Addis assemblage was dominated by Kluijver 1992), more in depth taxonomic studies upright sponges (arborescent, massive and are required to confirm these records. flabellate growth forms), but cnidarians including hydroids were entirely absent. Similarly, this area also exhibits a high diversity Wilson’s Promontory had a low coverage of of Bryozoans compared to other areas (Ponder et encrusting sponges and hydroids, with high al. 2002), has been described as an area abundances of red and brown algae and the containing highly species rich hydroid fauna gorgonian fan Pteronisis sp.. The Port Phillip (Watson 1982), and contains at least one ascidian Heads assemblage was dominated by encrusting species known only from Port Phillip Heads sponges, hydroids, ascidians and bryozoans, (Flora and fauna guarantee ‐ scientific advisory many of which are considered rare, and, committee 2009). according to Edmunds et al. (2006c) there are While studies of organisms on deep reefs in Port many identifiably different assemblage types Phillip Heads remain sparse, work has been present. conducted elsewhere on species such as sponges Within Port Phillip Heads, further differences in that are predominant on this type of reef assemblage structure were apparent between (Roberts and Davis 1996; Roberts 1996). areas (Edmunds et al. 2006b): While recent surveys of Port Phillip Heads have • Catacombs Ridge, the Plateau and Nepean begun to identify those species that make up Bank contained a high abundance of sessile communities, little is known about the encrusting sponges and hydroids mobile invertebrates that occur on deep reefs in Port Phillip Bay. This is partly due to sampling • Deep cobble habitats, such as Uelmans Deep strategies that have been used, with video were characterised by low abundances of transects unable to record species that are often sessile organisms cryptic in nature and shelter in cracks and • Reef walls at ~25 m were dominated by crevices in the substrate as well as within cryptic encrusting osculated sponges and other microhabitats created by sessile organisms. In sessile species, e.g. Portsea Hole addition, technical difficulties involved in surveying deep reefs also make this problematic • Reef slopes in the area were characterised by (Edmunds et al. 2006b). Edmunds et al. (2006b) dominant assemblages of “massive ruffled suggests that these organisms play an sponges, rambling grey encrusting sponge ecologically significant role, providing food for and other encrusting sponges”. carnivorous fishes on deep reefs in Port Phillip Other sessile species that occur in the reef Bay, and are likely to include a variety of assemblages of Port Phillip Heads include crustaceans and molluscs. hydroid fans, soft corals, gorgonian corals, crustose and arborescent bryozoans, colonial Fish ascidians, and solitary ascidians (Edmunds et al. Deep reef fish fauna include common subtidal 2006b). It has been reported that over 271 reef fish species, but other species that are rare validated species of sponges have been collected on shallow reef may also be present including from Port Phillip Heads, which is a large boarfishes Pentacerotidae), splendid perch proportion of the 523 species identified to date Callanthias australis, butterfly perch Caesioperca from Victoria, and the 1416 identified to date Lepidoptera and banded seaperch Hypoplectrodes throughout Australia (Flora and fauna nigroruber (Edmunds et al. 2006b). Fish guarantee ‐ scientific advisory committee 2009). assemblages typically begin to change at depths Notably, 115 of the species recorded in Port greater than 20 m, with the loss of the kelp‐

Temperate reefs literature review 15

associated wrasses and leatherjackets, and the of > 60 m over sediment areas and some appearance of deeper water species (OʹHara et reef‐and‐sediment areas, and in relation to al. 1999). On deep reefs within Port Phillip Bay, algae and invertebrates fish assemblages are reasonably diverse and • The draughtboard shark Cephaloscyllium include a variety of planktivores, roaming laticeps was present across all substrata in carnivores and omnivore/herbivores that occur depths of ~ 60 m, and was predicted to be in moderately high abundances (Edmunds et al. present out to the deepest regions of the 2006b). park at ~110 m The relationships between fish distributions and Surveys of habitat structure and fish community reef habitat in Victoria have not been examined structure on deep reefs from 25‐200 m from to a large extent, apart from recent studies on Gippsland Lakes – Cape Howe and southern reef down to ~60 m at Cape Howe Marine NSW found a correlation between communities National Park (Moore 2008; Moore et al. 2009) and depth, latitude and seabed type (Williams using stereo‐Baited Remote Underwater Video and Bax 2001). For example, 61% of fish species Systems (stereo‐BRUVS). This study used surveyed were associated with either reef or soft habitat suitability modelling to successfully link substrates, and the remainder were associated the distribution of fish species with with both. Species that were associated only environmental characteristics including depth, with reefs in the study included: butterfly perch substrate type and reef complexity (Moore et al. Caesioperca lepidoptera, eastern orange perch 2009). This allowed an examination of subtle Lepidoperca pulchella, bearded rock cod differences in biological and topographic Pseudophycis barbata, chinaman leatherjacket complexity and their importance in structuring Nelusetta ayraudi, barber perch Caesioperca razor, species distributions. For example: splendid perch Callanthias australis, striped • The eastern blue grouper Achoerodus viridis, trumpeter Latris lineate, mado Atypichthys a carnivore which feeds on a variety of prey, strigatus, bastard trumpeter Latridopsis forsteri, was distributed in relation to the presence of common bullseye Pempheris multiradiata, maori solid reef and boulders wrasse Ophthalmolepis lineolata, longfin pike Dinolestes lewini, largetooth beardie Lotella • The green moray Gymnothorax prasinus was rhacinus, bluethroat wrasse Notolabrus tetricus, linked positively to reef and broad‐scale southern conger Conger verreauxi, sergeant baker topographic complexity Aulopus purpurissatus, swallowtail Centroberyx • The eastern blue‐spotted flathead lineatus, pigfish Bodianus sp., silver sweep Scorpis Platycephalus caeruleopunctatus, was closely lineolata, and thresher shark Alopias vulpinus. affiliated with sand (Hutchins and Swainston 2002) and was present in depths

Temperate reefs literature review 16

Canyon reefs Assemblages within canyons vary with anemones and ascidians (Port of Melbourne substrate depth, size, and complexity (Harris Corporation 2007d). Sponges make up 67% of 2007; Williams et al. 2009b) and these habitats the biological groups in the canyon, hydroids may be particularly sensitive to anthropogenic 14% and all other groups less than 2% each (Port disturbance in the form of commercial fishing of Melbourne Corporation 2007d). Edmunds et which is concentrated at ~50‐1300 m depth al. (2006b) also found encrusting sponges and (Larcombe et al. 2002; Williams et al. 2009b). hydroids to dominate these assemblages. Port Phillip Heads Other canyons The entrance of Port Phillip Bay contains a key Little is known about abyssal reefs found deep geomorphological feature known as “The on the continental slope (>200‐400 m), such as Canyon” which meanders more than 3 km from the “Cascade” off east Gippsland, which is 1 km south‐west of Point Nepean through the thought to be dominated by cold water corals Entrance and 1 km north‐west of Point Nepean that form a habitat for a variety of invertebrate inside the Entrance. It covers an area of ~100‐120 species (OʹHara et al. 1999). ha, with a depth range to ~100 m, but also Recent mapping of geomorphic features and includes two shallow banks, Nepean Bank and assemblages from 200‐2000 m has, however, Rip Bank, which lie in the shipping channel been conducted in south‐east Australia (Harris through the Entrance (Port of Melbourne et al. 2005) and has been used in the design of Corporation 2007d). The canyon contains a deep water Marine Protected Areas (Harris distinctive ecological environment unlike other 2007), although mapping is still incomplete at environments in the Bay or elsewhere in the current time (Williams et al. 2009b). As such, Victorian waters. Reef communities within the relatively little is known about organisms that Canyon are present on mixed substrates of inhabit deep reefs and rocky canyons in the Aeolian calcarenite and basaltic rock and region, with surveys of similar habitats experience large volumes of water movement, elsewhere in Australia often finding a high with the tidal flow between the heads reaching percentage of un‐described species (Poore et al. speeds of up to 5 ms‐1 (Edmunds et al. 2006b). 2008). For example, recent surveys in 2009 are The water passing through Port Phillip Heads the first to collect samples of invertebrate carries high volumes of suspended particles megafauna from deeper than 1800 m around such as sand on the flood tide and sediments Australia (Williams et al. 2009a)). from the Bay on the ebbing tide which reduce light levels, but increase nutrient levels Some work has been conducted off southeast (Edmunds et al. 2006b). Australia. Surveys were recently undertaken in deep‐water marine reserves within the “South‐ Invertebrate communities are common deep reef east Commonwealth Marine Reserve Network” biota, but are difficult to study because of the (Department of the Environment 2008) that were strong tidal currents, ocean waves and seabed gazetted in 2007 as part of the “National depths that are beyond the normal range of Representative System of Marine Protected depth for scuba divers. Consequently, the Areas” (Williams et al. 2009b). Off East Canyon’s habitats and associated biota have Gippsland, areas of rocky reef are exposed from only been examined in detail by using remotely muddy sediments on the steep slopes of “Big operated vehicles (ROVs) and, to a lesser extent, Horseshoe Canyon”, part of the Bass Canyon divers using underwater video and still system. The area is the largest canyon that has photography (Port of Melbourne Corporation been sampled in the south‐east for benthic 2007d). These ecological studies confirmed that biodiversity (Williams et al. 2009b). This canyon much of the rocky seabed beyond 20 m in the system, at a depth of ~1500 m, has a total area of canyon consists of highly sculptured calcarenite ~319 km2 (Williams et al. 2009b), and the reef (including vertical walls, pinnacles, crevices majority of the diverse, abundant, sessile etc) with sandy and rubble patches on the flatter megafauna in the canyon is associated with regions and in the deep basins. The permanent these exposed hard surfaces (Kloser et al. 2001). rocky habitat is totally covered with a range of Percentage cover of “rich fauna” as determined sessile invertebrates, particularly encrusting from underwater video peaked at 200‐300 m sponge communities, with a variety of (Williams et al. 2009b). Organisms include component biota including hydroids, bryozoans, diverse, abundant, filter‐feeding species, such as

Temperate reefs literature review 17

dense beds of large sponges and the stalked Several canyons in south‐east Australia are the crinoid Metacrinus cyaneus, and numerous locations of the largest known aggregations of species of octocoral (especially gold corals). This feeding and spawning fishes in the South‐East site is the type locality for M. cyaneus and it is Fishery region (Williams and Kloser 2004). For the only known location of the species off south‐ example, the Zeehan Canyon complex provides eastern Australia (Kloser et al. 2001; Williams et “areas for high‐order predator foraging and blue al. 2009b). Above 600 m fisheries are important grenadier spawning” (Harris 2007). Elsewhere, in this area (Harris 2007). plankton and nekton have been found to be elevated in and around canyons, in addition to In contrast, the Zeehan canyon complex to the high densities of megafauna (Beaman et al. south‐west of Victoria consists of mostly soft 2005). sediment substrates, with few exposed rock surfaces (Williams et al. 2007). Canyons in this The use of abiotic classification of habitats to area exist every ~7 km and include fisheries for infer levels of biodiversity in these deep systems several species including blue grenadier, crab, is a contentious issue (Harris et al. 2009; Williams ling and rock lobster (Harris 2007). According to et al. 2009a; Williams et al. 2009b), which Harris (2007) “conservation values include links indicates how little is currently understood between canyons, ocean currents, upwelling about assemblages in these systems. processes and flows through Bass Strait”.

Temperate reefs literature review 18

Ecological and physical environmental drivers

Major environmental factors influence reef roughness and complexity, and shading communities in Victoria. Womersley and King (Womersley and King 1990; Underwood and (1990) split these factors into four key groups: Chapman 1995; Little et al. 2009). Dynamic factors: Three features of the tides affect intertidal reef communities: the rise and fall of the tide, • Tide ‐ period and amplitude, cycles variation between neap and spring tides and • Water movement – currents, upwelling, surf daily progression of the tides (Underwood and and wave action, storms Chapman 1995; Little et al. 2009). • Wind – effect on tide, water movement, and Waves cause major variation in assemblage humidity structure of intertidal reef communities from exposed to sheltered areas (Underwood and Physical factors Chapman 1995). The importance of the • Light – quality, quantity, periodicity magnitude of wave exposure in shaping community structure has long been recognised • Sea temperature – variation, range, (Lewis 1964; Stephenson and Stephenson 1972), stratification with comparisons and contrasts made between • Air temperature (in conjunction with exposed and sheltered intertidal reefs (e.g. emersion)– variation, range Seapy and Litter 1978). • Relative humidity A diverse range of other factors and processes influence assemblage structure and a variety of • Rainfall work has been carried out worldwide that • Substratum quantifies how these interact with each other. For example, while molluscan grazers may Chemical factors impact algal cover and shape sessile assemblage • Salinity structure at local scales, the availability and supply of algal propagules is also important and • Nutrients may in turn be partially driven by processes at

• Availability of gases (O2 and CO2) broader spatial scales such as benthic‐pelagic coupling and oceanic currents (Schiel 2004; • pH Underwood and Chapman 2007; Little et al. • Pollution 2009). Biotic factors At local scales, gradients can be seen in the relative importance of physical and biological • Competition for space, light, nutrients etc factors on intertidal reefs. Physical factors, such • Grazing/predation as desiccation stress, generally increase in importance up the shore, while biological factors • Epiphytism such as competition and predation increase in • Symbiotic relationships importance down the shore. Towards the top of the shore where physical stress is high, algal and sessile invertebrate cover is low, while towards Intertidal reefs the bottom of the shore where physical stress is Tides are, perhaps, the most important low, percentage cover of algae and sessile environmental factor causing gradients across invertebrates is high. In the mid shore, where intertidal reefs. The direct effects will be physical and biological stress levels may be of modified by factors such as wave action, air equal importance, a bare zone is often found. In temperature, humidity, freshwater run‐off, this zone, there is typically a low cover of algae desiccation stress, rock type, aspect, surface due to a mixture of desiccation stress and

Temperate reefs literature review 19

grazing; competition for free space is therefore several other authors describe the effects of very usually low (Connell and Gillanders 2007; Little hot days combined with afternoon low tides on et al. 2009). this species (Keough and Quinn 2000; Bellgrove et al. 2004) and mobile gastropods (Parry 1982). There is a large body of research that focuses on Parry (1982) also described predation on the importance of disturbance in the structuring intertidal limpets by oystercatchers and wrasse. of intertidal reef assemblages. Disturbance is important, as free space is a limiting factor at The majority of disturbance studies in Victoria some tidal heights on intertidal reefs and the have, however, been focused on anthropogenic creation of free space can lead to changes in the disturbance events, such as the recreational use structure of assemblages (Little et al. 2009). of reefs and the effects of trampling and the Initially this research concentrated on predation harvesting of invertebrates for food or bait as a key driver (Paine 1966) but this was (Addison et al. 2008) or the effects of pollution followed by a general recognition that any (Bellgrove et al. 1997; Hindell and Quinn 2000). disturbance that created space was fulfilling the In a study that has collected data from 65 same function (Connell and Gillanders 2007; intertidal reefs across Victoria, a number of Little et al. 2009). bioassessment methods have been tested to determine their ability to detect impacts on reef The magnitude and timing of disturbance events assemblages (OʹHara et al. in press). such as storms, ice scour and boulders overturning can create patches of space that Human impacts on rocky shore communities allow new individuals to recruit and may lead to have been chronicled in Victoria, and appear to a complex mosaic of patches at various states of take two main forms: the collection of seafood succession (Connell and Gillanders 2007; Little et from the intertidal zone; and trampling of al. 2009). On some shores, the impact of organisms by visitors walking on the shore disturbance events may be relatively (Povey and Keough 1991; King 1992; Keough et predictable, for example low on shores that have al. 1993; Keough and Quinn 1998; Keough and high algal cover (Connell and Gillanders 2007). Quinn 2000; Addison et al. 2008). Such impacts are well known and have been shown elsewhere Another key factor that affects the ecology of in Australia and internationally (Underwood intertidal reefs is the arrival of propagules or 1993; Fletcher and Frid 1996). “supply side ecology” (Underwood and Chapman 2007). Planktonic dispersal and Human predation (collecting) survival of propagules is highly variable, and Local studies within Port Phillip Bay, focusing consequently, spatial and temporal variability in on the collection of gastropods from the the number of propagules arriving is also highly intertidal zone, have demonstrated that the variable. The interactions between these new mean size and abundance (one species only) of recruits and the existing assemblage will vary target species were reduced at an impacted site greatly depending on this “patchiness” in larval compared to protected sites nearby (Keough et supply (Underwood and Chapman 2007). Apart al. 1993; Keough and Quinn 2000). The indirect from supply of propagules, other bottom up effects of this type of human predation have processes relate to the interaction of coastal been found to be subtle and related mainly to oceanography with intertidal communities, for the abundance of microalgae. For example, example the effect of coastal upwelling on the frequent removal of cellanid limpets can result supply of phytoplankton, particulate matter and in an increase in microalgal densities while nutrients to intertidal assemblages (Menge removal of nerites results in a decrease in 2000). Top down and bottom up processes can microalgae (Sharpe and Keough 1998). interact to influence the dynamics of Such removals may have more complex effects communities on intertidal reefs (Menge 2000). than currently appreciated, and a more in depth The following sections examine research that examination is required. For example, it has has been conducted locally. been suggested that removing the largest individuals from a population of the limpet Top‐down / disturbance processes Cellana tramoserica may eliminate the bulk of the In Victoria, several studies have been conducted reproductive effort of this species (Parry 1982), that examine natural disturbance on intertidal which may in turn impact community structure reef communities. For example, Bennett (1990) on the targeted shore as well as nearby areas. examined disturbance within beds of the There is almost no ecological information commonly occurring alga Hormosira banksii, and available about another main target species in

Temperate reefs literature review 20

Victoria, Turbo undulatus, and so it is impossible cover of microalgae ‐ the main food source for a to speculate what the effect of its removal might number of gastropod grazers. The mobile be (Keough and Quinn 2000). herbivores emigrate in response to increasing cover of Hormosira and when Hormosira cover is Other studies undertaken on the Victorian coast reduced, microalgal abundances increase at shores visited less frequently have found little resulting in increased densities of grazers. The evidence to suggest there is an impact of authors of this study were unable to determine harvesting (Keough and King 1991; King 1992), why one site showed no recovery over the six‐ although Addison et al. (2008) suggest that year study but they discuss the potential shellfish collections at Sorrento may have a ramifications of sites having different levels of broader impact on intertidal assemblages. resilience and the management options There have been no studies on the harvesting of associated with this. A management program other taxa for bait in Victoria, although in New within the Marine National Park system will be South Wales there is some evidence that the targeting trampling as a hazard and this may be removal of other taxa such as crabs and the able to provide data on which shores are more, tunicate Pyura stolonifera is unsustainable or less, resilient to trampling (Carey et al. 2007). (Fairweather 1991; Underwood 1993). This may Pollution also hold true in Victoria, where fertilisation The release of pollutants is another major type of success in isolated spawning individuals (>2 m disturbance event that impacts assemblages on apart) of P. stolonifera at Barwon Heads has been intertidal reefs in Victoria. Reefs within Port shown to be limited by a scarcity of sperm Phillip Bay are more likely to be impacted by a (Marshall 2002). Removal of individuals may range of toxicants due to their proximity to therefore directly reduce reproductive capacity urban and industrial areas, harbours, ports and within local populations. shipping channels. There have been numerous Fisheries Victoria is currently liaising with local studies documenting the superimposition of communities to determine which species they male sexual characteristics on female gastropods preferentially target on intertidal reefs; this following exposure to TBT (tributyltin) ‐based information could be used to direct future antifouling paint since this was first research examining this type of disturbance. demonstrated (Bryan et al. 1987; Gibbs et al. 1987). Foale (1993) described the incidence of Trampling imposex in the whelk Thais orbita at sites around The other main disturbance caused by the Port Phillip Bay and found that the incidence of recreational use of reefs is trampling. This has imposex corresponded strongly to the proximity been recognised as an issue of concern in to harbours or marinas although mean body Victoria (Carey et al. 2007). There is evidence burdens of TBT were not particularly high. The that trampling can impact intertidal reef reduction in reproductive potential of intertidal assemblages both in Victoria (Povey and predators such as whelks has the potential to Keough 1991; Keough and Quinn 1998) and in impact the structure of intertidal reef other parts of the world (Schiel and Taylor 1999; assemblages (Spence et al. 1990). Benedetti‐Cecchi et al. 2001). Studies undertaken within Port Phillip Heads Marine National Park Studies of intertidal reef assemblages affected by have found that trampling produced marked TBT have not been undertaken in Port Phillip effects in two major habitats. In beds of coralline Bay, although Parry (1982) considered predation algae, the effects were short lived, but in beds of by whelks to be a minor cause of mortality in the Hormosira, algal cover was greatly reduced and four species of limpet he studied at a San Remo the number of grazing molluscs was increased shore. A recent study (Rees et al. 2001) found in trampled areas and recovery was still not that the severity and extent of imposex has been complete >400 days later (Povey and Keough reduced except at locations that were adjacent to 1991). This pattern was also evident in a major ports or certain harbours. It is possible separate, longer‐term study, where two of three that in some areas sediments are providing a sites were able to recover between trampling source of TBT although no data exists on this in events whilst a third site did not recover Port Phillip Bay. (Keough and Quinn 1998). Keough and Quinn Other toxicants, such as copper, have also been (1998) propose a conceptual model where shown to cause imposex in certain species (Nias Hormosira can be likened to a keystone species et al. 1993). No specific research on the effects of (Paine 1995) whereby they provide damp, shady other toxicants on intertidal reef assemblages refuges for some species but also reduce the

Temperate reefs literature review 21

within Port Phillip Bay or coastal Victoria have It is likely that the small dispersal shadow of been conducted to our knowledge. Hormosira, combined with potential impacts on establishing zygotes, will limit the re‐ Bottom‐up / supply side processes establishment of this species in areas adjacent to Pollution sewage discharges (Bellgrove et al. 1997) A form of pollution that primarily has a bottom‐ up effect through the elevation of nutrients is Another study undertaken at Boags Rock has the discharge of sewage effluent. The majority of found that the recruitment of the intertidal studies considering the effects of sewage mussel Brachiodontes rostratus was facilitated by effluent on intertidal reef assemblages in the secondarily‐treated effluent while shell Victoria have been undertaken around Boags growth was reduced and mortality of larger Rock. However the Western Treatment Plant individuals was increased (Hindell and Quinn also discharges secondarily treated sewage 2000). This study also discussed the implications effluent from Melbourne into Port Phillip Bay. for intertidal fauna that use the habitat created Most of the studies considering the impacts of by mussel clumps. this discharge have been focused on the Larval supply / recruitment predominantly soft sediment environment in the It is well recognised that a vital consideration in vicinity of these discharges. Axelrad et al. (1981) rocky shore ecology is variability in recruitment sampled the macrophyte assemblages at three in both space and time. Recruitment depends on basalt reefs within the Bay and found that the larval supply, local hydrodynamics, larval intertidal zone at Werribee was characterized by behaviour, predation / herbivory and the Centroceras clavulatum throughout the year and availability of adequate resources to allow Ulva lactuca and Enteromorpha compressa in settlement and survival and so recruitment to a summer / autumn. Blooms of the blue green alga population. Quinn (1988) undertook an Cladophora sp. were also observed. We are not experimental study to investigate the aware of more recent studies specifically aimed importance of conspecific adults, macroalgae at the impacts of sewage effluents within Port and height on the shore to recruitment of the Phillip Bay. intertidal limpet, Siphonaria diemensis. In this Long‐term monitoring of the macroalgal study there was no effect of the density of adults assemblage around the Boags Rock discharge on the density of recruits or height on the shore found that fewer species were recorded at sites but there was an effect of macroalgal cover; with closer to the outfall, as well as a loss or significantly greater recruitment to areas with reduction of Hormosira coupled with an increase encrusting macroalgae. in algal turfs and the polychaete Boccardia Studies of intertidal macroalgal species in proboscidea adjacent to the discharge (Brown et al. Victoria have concluded that while recruitment 1990). These patterns are considered typical of cannot be predicted directly from the supply of those that have occurred around sewage propagules, the two processes are linked discharges throughout the world (Littler and (Bellgrove et al. 2004). Results indicate that while Murray 1975; Fairweather 1990). There is no pre‐ and post‐settlement processes are likely to clear consensus to explain the loss of H. Banksii influence macroalgal distribution and (or other dominant brown algae around the abundance, the temporal and spatial variability world) following exposure to sewage effluent in the supply and recruitment of propagules can (Bellgrove et al. 1997). At Boags Rock there was explain much of the patchiness in macroalgal no evidence that the sewage effluent assemblages. A study on the effects of the detrimentally affected the availability of grazing gastropod Bembicium nanum on the propagules or macroalgal recruitment (Bellgrove recolonization of algae at Aireys Inlet found that et al. 1997). There were, however, very high B. nanum significantly reduced recolonization of densities of propagules of opportunistic taxa the ephemeral brown alga Scytisiphon lomentaria such as Ulva and Enteromorpha and high but had no effect on recolonization of Hormosira recruitment of these taxa at polluted sites. Other or the green alga Enteromorpha intestinalis (Braley studies have found that high concentrations of et al. 1991). A separate study has found that treated sewage effluent inhibit zygote micrograzing copepods have the potential to germination and embryo growth of Hormosira greatly influence the density of various (Doblin and Clayton 1995) and so propagule macroalgal taxa, while a littorinid mesograzer supply and recruitment may still be important may reduce the both the density and number of in the loss of Hormosira in sewage affected areas. macroalgal taxa (Bellgrove 1998). This study also

Temperate reefs literature review 22

found that two limpets studied (Patelloida biogeographic significance for Australia’s latistrigata and Cellana tramoserica) did not have southern temperate region (OʹHara and Poore any significant effects on the densities of 2000). macroalgal taxa recruiting (Bellgrove 1998). This An ongoing study looking into the connectivity contrasts with studies at other locations that of intertidal gastropod molluscs with varying have shown rapid colonisation of foliose algae dispersal potentials within marine national following the exclusion of patellid limpets parks is currently comparing recruitment (Hawkins 1981; Underwood and Jernakoff 1981). patterns of gastropods in Marine Protected There have also been a number of studies Areas (MPA) and non MPA sites in Port Phillip specifically focused on Hormosira. While this Bay and the central coast of Victoria (Bathgate species has a broad distribution throughout pers. comm.) south‐eastern Australia, dispersal of propagules Nutrients is thought to be limited (Bellgrove et al. 1997; The supply of nutrients is considered another 2004). However, investigations into the important bottom‐up process and to date there occurrence of ‘outbreeding depression’ at a has been very little attention in Victoria to the regional scale led researchers to speculate that impacts of nutrients on rocky shore ecology. Hormosira may be capable of longer distance There have been studies that consider the dispersal than previously thought (McKenzie impacts of sewage discharges on intertidal reef and Bellgrove 2006). Detached fronds of assemblages (see discussion above) but it is not Hormosira have been shown to be capable of always easy to separate the effects of increased releasing gametes for up to 8 weeks following nutrients from other aspects of the discharge detachment and floating fertile fronds may be (freshwater, suspended solids, toxicants etc.). A an important mechanism for facilitating long‐ manipulative study has been undertaken at distance dispersal in this species (McKenzie and Point Nepean and found no effect of adding Bellgrove 2008). Further studies investigating nutrients or removing grazers (separately or genetic diversity over the broad‐scale together) on the algal assemblage monitored distribution of Hormosira using genetic markers (Baker 2006). This finding is in stark contrast to may give valuable insight into gene flow and work in other parts of the world (Thompson et long distance dispersal and are already al. 2000; Bokn et al. 2003) and other parts of underway. Australia (Underwood 1984; Gorgula 2004) and In a study that quantified species richness of may relate to the time of year the experiments invertebrates on 11 rocky intertidal shores were undertaken (summer) when propagule separated by a biogeographical barrier (Ninety supply was likely to be low (Clayton 1990; Mile Beach), it was revealed that species Bellgrove et al. 2004) and physical stress (heat) richness and species composition did differ on was high. A manipulative study undertaken in each side of the barrier and that the distribution the shallow subtidal in south Australia found of species was not related to their potential for that increasing nutrients had no effect on algal dispersal (Hidas et al. 2007). The three species assemblages in the presence of canopies and, in studied with direct development were found on the absence of canopies, only had an effect on both sides of the barrier, while seven of the eight algal assemblages in the presence of grazers species restricted to one or other side of the (Russell and Connell 2005). They attributed barrier had planktonic larvae. All species these complex interactions to the fact that the present on Red Bluff, an isolated rock platform, area of coast studied had few grazers (weak top‐ did, however, have planktonic larval stages. In down control by grazers) and was relatively contrast, a study looking at the mitochondrial oligotrophic. There is some evidence that the DNA of the highly‐dispersive intertidal coastal regions of Victoria are also under weak gastropod Nerita atramensota found a consumer control compared to eastern Australia biogeographical disjunction that was unrelated (Beovich and Quinn 1992; Bellgrove 1998; to either the Coorong or Ninety Mile Beach; Sharpe and Keough 1998; Burton 1999) and this instead, Wilsons Promontory was the point of may affect the response of assemblages to disjunction (Waters 2005). The authors elevated nutrients. Ambient nutrient levels concluded that this sharp biogeographical measured at Cheviot Beach (Parry and Restall disjunction was in marked contrast to the 2007) were very similar to those cited in the species’ high dispersal abilities and supports South Australian study and considerably less other studies that have noted that Wilsons than nutrient concentrations in New South Promontory may have considerable Wales (Russell and Connell 2005). Further

Temperate reefs literature review 23

studies are required to investigate how nutrient pulmonate, spihonariad limpet at the exposed supply might affect recruitment of Hormosira rocky shore of Point Nepean (Burton 1999), in and other algal species, grazer control, contrast to a previous study undertaken at San competitive interactions and responses to Remo (Beovich and Quinn 1992). In the Burton anthropogenic disturbances such as trampling. (1999) study and that of Keough et al. (1997) it was shown that while patterns of cellanid Competition growth varied in response to competitive Studies of competition on intertidal reefs in pressures, microalgal abundance did not. This is Victoria have primarily focused on exploitative in contrast to findings from other parts of intra and interspecific competition of Australia (Underwood 1984) and other parts of herbivorous gastropods. Studies undertaken at the world (Little et al. 2009). Further San Remo have found that densities of investigation concluded that feeding behaviour Austrocochlea constricta and Bembicium nanum was not important to limpet growth and were not restricted by interspecific competition mortality, and that the reasons for the observed for food, although intraspecific effects did occur effect of increased densities on growth and in summer and autumn due to a reduction in mortality at Cheviot Beach (Point Nepean) food supply (Quinn and Ryan 1989). Quinn and remain unresolved (Burton 1999). Ryan (1989) also found that growth was not a fixed characteristic in Siphonaria diemensis and There is evidence that the outcomes of can change rapidly in response to variations in exploitative competition in Victoria can depend food supply; growth decreased with increased on rock type and seasonal effects of food supply, densities of conspecifics, and shell growth and and appear to differ in some respects from tissue weight were reduced in an experimental similar studies undertaken in New South Wales. treatment with reduced food compared to a While there is evidence of competition for food normal food treatment. Beovich and Quinn in Victorian populations, it does not appear to (1992) found no evidence that Siphonaria be driving distributions as in New South Wales. lomentaria were food limited by Cellana While in some instances removal or reduction in tramoserica in winter and spring at this site. grazer densities on Victorian shores did cause an increase in algal growth, the magnitude of Studies on basalt rock in Port Phillip Bay have effects was much smaller than observed in New found that Cellana tramoserica individuals are South Wales and other parts of the world. strong exploitative competitors for food resources and when exposed to high densities of conspecifics experience reduced growth and increased mortality (Wright 1989; Marshall and Keough 1994; Merory 1997). These results are consistent with studies from other parts of Victoria (Parry 1982; Burton 1999) and New South Wales (Creese and Underwood 1982). Marshall and Keough (1994) also found an asymmetry in the competitive ability of cellanid limpets, with smaller individuals able to out compete larger individuals. They speculated that smaller limpets were able to access a food supply within the rough rock surface that larger limpets with their larger radulae were not able to access. This hypothesis was later tested by repeating the experiment on basalt rock at Williamstown and limestone rock on the exposed Point Nepean shore (Keough et al. 1997). This study confirmed predictions that asymmetry in competitive abilities of limpets would not be apparent on a smoother substratum and was further supported from results from another study undertaken at Point Nepean (Burton 1999). Cellanid limpets were also shown to be competitively superior to a

Temperate reefs literature review 24

Subtidal reef A wide range of factors and processes are In contrast, Edmunds et al. (2000) specifically set responsible for the distribution and structure of out to establish which physical variables assemblages on subtidal reefs. These have influence the distribution and composition of recently been reviewed in some depth (Connell reef communities. The study involved surveying 2007; Connell and Irving 2009; Wahl 2009), and seven subtidal (8 – 18 m) sites between Cape the descriptions that follow below cover work Schank and Wilsons Promontory to provide a that has been conducted in Victoria, with variety of reef substratum types, recording relevant examples from elsewhere also included biological (density of macroinvertebrates, to provide context. canopy forming plants, cover and biomass of understorey macroalgae) and physical Physical drivers (substratum lithology, relief, interstitial space, and complexity, depth, exposure, aspect, Biogeographical provinces or regions have been distance from shore, slope, longitude and demonstrated to influence the distribution and sediment cover) variables. Results of the study composition of subtidal reef communities in found that many reef inhabiting biota were Victoria. Waters et al. (in press) recently closely associated with particular physical provided an a priori test for the existence of variables. Invertebrates were closely associated Bennett and Pope’s (1952) Maugean (south‐ with combinations of substratum structure (i.e. eastern), Flindersian (western) and Peronian interstitial space, complexity, slope and relief), (eastern) biogeographical provinces across depth and longitude whilst aspect and exposure southern Australia. The study quantitatively were also of some importance. analysed distributional data from 1,500 algal species and identified the three distinct The slope of rock has been described as the most biogeographical assemblages, consistent with striking feature influencing the composition of traditional qualitative provinces. Connell and assemblages of rocky subtidal systems by Irving (2008) quantified the frequency and size Connell (2007). The position of rock affects key of patches of major benthic habitat on across the physical processes such as light, flow and southern coast of Australia and went on to show sedimentation, as well as biological processes that biogeography had a fundamental influence including consumer foraging, competition, on the patterns of abundance and composition facilitation and recruitment. Edmunds et al. of subtidal assemblages across regional scales. (2000) found algae had less correspondence with The most fundamental patterns related to (1) the physical data, but exposure, depth and reef proportion of rock covered by kelp forests, as slope were reasonably good explanatory related to particular functional groups of variables. Substratum type lithology as a single herbivores, and (2) the small‐scale heterogeneity variable was not found to be a major that characterises these forests. determinant, although some species occurred predominantly on one substratum type. The Prior to this, OʹHara (2001) tested the authors go on to state that the relationships assumption that habitat defined by various between variables measured do not necessarily biological and environmental variables are imply causality, but the physical‐biological surrogates for biodiversity. The study collected relationships described are similar to those and analysed benthic floral and faunal samples found in studies of temperate reef assemblages from subtidal reefs at 23 sites along the coast of in New Zealand (Choat and Schiel 1982; Choat Victoria, and determined that habitats defined and Ayling 1987). by dominant vegetation, and to a lesser extent region, supported consistent floral and faunal In New Zealand, depth and exposure have been assemblages. For each sample, habitat shown to play an important role in algal and parameters were recorded including dominant echinoid distribution (Choat and Schiel 1982), vegetation, geographic region, depth, rock type and echinoid and algal habitat have been shown and exposure. Although physical variables were to play an important role in determining determined to have little emphasis as drivers, associated fish fauna (Choat and Ayling 1987). the author acknowledges that the experimental These findings have been reiterated in design was probably not an appropriate test for Australian studies with depth and wave the effect of depth range, rock type and exposure shown to influence the distribution exposure on biodiversity. and composition of subtidal temperate reef communities in southern Australia. Edgar (1984)

Temperate reefs literature review 25

described benthic floral and faunal assemblages comosa occurs in large beds at depths of ~3–5 m; along the eastern, southern and western at exposed sites, Ecklonia radiata is typically Tasmanian coasts and related them to a subtidal observed at depths >7 m and often growing with zonation pattern of wave exposure and depth. P. comosa; and, giant kelp Macrocystis angustifolia Results of the study found that major (an indicator species for the Maugean assemblages of benthic organisms within the biogeographical province) occurs at Port Phillip same cool‐temperate biogeographical provinces Heads MNP ‐ Point Lonsdale and at Point (Maugean and Flindersian), can be predicted Nepean. reasonably accurately by reference to wave In South Australia, Connell (2003a; b; 2005) has exposure and depth. Coleman et al. (2007) found investigated the importance of physical depth to be a strong driver of patterns of mobile processes such as light penetration and invertebrates in kelp forests on the temperate sedimentation in structuring benthic coast of Western Australia. Their study found a communities, and a number of studies greater abundance and richness of common taxa elsewhere have also shown that subtidal in holdfasts from shallow relative to deep assemblage distributions vary due to a variety of waters. physical factors including light availability, Such differences in the distribution of species wave action and storm disturbance (Dayton et al. with depth can also be seen for a variety of reef 1984; Schiel and Foster 1986). Connell (2003a) fish. For example, the reef fish Achoerodus viridis tested the hypothesis that different temperate has been shown to decrease from shallow to reef‐algal habitat types will converge to become deep areas of reef and from inner to outer areas like those under Ecklonia radiata if subjected to of estuaries, although large individuals the same low light and accumulation of increased in numbers on more exposed coastal sediment without the presence of E. radiata. The reefs (Gillanders 1997a; Gillanders 1997b). Fish study found habitats did not converge under found on rocky reefs in New South Wales, in treatments. The author concludes that canopies particular labrids, have been found to show place strong constraints on the presence and distinct patterns in diversity and abundance in abundance of many taxa, but not encrusting‐ relation to wave exposure and depth (Fulton algal habitats which beneficially coexist as and Bellwood 2004). Few species were found to understorey. Connell (2003b) then went on to be abundant in exposed shallow habitats, while investigate why many sessile invertebrates are several species were restricted to sheltered anomalously absent from understorey habitats (Fulton and Bellwood 2004). Seasonal communities. A series of experiments were fluctuations in water temperature may also applied to partition both positive and negative result in changes in the abundance of fishes on habitat modifying effects by kelp for sessile temperate reefs (Parker Jr 1990). invertebrate recruitment. The key finding of the study was that a reduction of light intensity and Studies describing marine biodiversity in removal of sediment by canopies acted to Victoria have found depth and geography to facilitate recruitment, but physical abrasion by have the strongest influence on the composition the canopy acted as a negative force to of communities. Ferns et al. (2000) described overpower these positive effects for recruitment temperate reef biodiversity through mapping of sessile invertebrates. Connell (2005) and analysis of biological data and concluded experimentally separated the positive and that depth is an important factor in the negative effect of light penetration and distribution of dominant biota because of sedimentation on the assembly and maintenance localized conditions such as substratum of three subtidal habitats that characterise much topography/complexity and wave exposure. of the world’s temperate coastline: encrusting Victorian temperate reef community Marine coralline algae, articulate coralline algae and Habiat Class (MHC) attributes generally differ filamentous turf‐forming algae. The study found between shallow (0 ‐ 2.5 m), moderate (2.5 – 20 shade to cause a positive effect for encrusting m) and deeper (>20 m) subtidal depths. Broad coralline algae by facilitating the retention of patterns of algal species zonation along the space without overgrowth; however, it caused a depth gradient have also been shown in Victoria negative effect for articulate coralline and turf‐ (Sanderson 1997): Hormosira banksii is the forming algae by restricting growth and space dominant species observed on intertidal rock persistence. Sediment deposition caused a platforms; Durvillaea potatorum with mixed negative effect on encrusting coralline algae, a brown and green algae inhabits the seaward positive effect on articulated coralline algae and edge of intertidal rock platforms; Phyllospora

Temperate reefs literature review 26

a neutral effect on turf‐forming algae. This community compared with Cystophora and finding explains the presence of articulated Sargassum species. However, Ecklonia and coralline and turf‐forming algae on human‐ Macrocystis had large branching holdfasts that dominated coasts following the loss of canopy provided shelter to many larger cryptic animals, forming algae on reefs with heavy and provided stable substratum for many sessile sedimentation. The studies demonstrate the key invertebrates and smaller algae. role of physical factors associated with habitat‐ Algae can influence the presence of other marine forming canopy algae, particularly in relation to biota such as fish and invertebrates (Andrew human‐dominated coasts with heavy 1993; Edmunds et al. 2006a). Variation in algal sedimentation. cover and other biotic factors can show Another physical driver of subtidal reef considerable variation spatially and temporally communities is the presence of oceanographic (Dayton et al. 1984; Schiel and Foster 1986), and features such as upwelling that can alter regimes this can subsequently be seen in the distribution of variables such as nutrients and temperature. and abundance of associated invertebrate and For example, Butler et al. (2002b) states that the fish species (Russell 1977; Bodkin 1988; Bonney upwelling area contains “distinct colder Holbrook et al. 1990a, b; Schmitt and Holbrook water flora; rich assemblages of sessile filter 1990a; Anderson 1994). feeders such as sponges, bryozoans and corals; A large body of work has been conducted in feeding grounds for seabirds, fishes, whales and California, USA on temperate reef systems. other higher order predators such as fur seals Canopy‐forming kelps such as Macrocystis and penguins; and a productive fishing ground pyrifera can directly affect the densities of fish for rock lobster, sustaining a relatively large species that use the kelp as a nursery area fishing industry”. Butler et al. (2002b) described and/or adult habitat (Ebeling and Laur 1985; how limestone reefs in the area are often Bodkin 1988; Holbrook et al. 1990a; Carr covered by dense assemblages of molluscs, 1994).The effects of increases or decreases in sponges, bryozoans and red algae, with different types of algal community have been upwelling related assemblages of bryozoans, found to be strongly related to the resources sponges and axoozanthellate coral on the shelf required by different life history stages of fishes edge and upper slope, and off Portland, diverse (Holbrook et al. 1990a), as well as to the differing cyclostome bryozoans are found on the deep needs of individual species of fish (Holbrook et shelf. al. 1990b). For example, positive effects have Ecological drivers been chronicled for species that use kelp as a Habitat structure nursery ground or adult habitat; whereas Ecological components of temperate reefs have negative effects can be seen for fish that rely on been shown to influence the distribution and understorey species that are impacted by composition of subtidal reef communities in shading effects and which may serve as Victoria. Algae, in particular canopy forming important sources of food (Holbrook et al. 1990a; species such as kelps, act as foundations and Schmitt and Holbrook 1990a; b). strong ecological drivers to entire subtidal While work on temperate reefs in California, systems because they provide important food suggest that the distribution and abundance of and habitat structure for other organisms on the canopy and understorey algae may partially reef (Duggins 1989; Keough and Butler 1996). explain spatial variation in the species Variation in the configuration of subtidal algae composition of fish recruitment among in southern Australia and northern New temperate rocky reefs at the local level (Bodkin Zealand (e.g. monotypic or mixed stands of 1988; Carr 1989), heterogeneity of other habitat algae) may influence the composition and features, e.g. the presence of sand patches, is abundance of associated organisms (Goodsell et also likely to drive spatial variability in the al. 2004) such as understorey algae and sessile distribution of reef fishes, particularly at small invertebrates (Irving et al. 2004). spatial scales (Garcı´a‐Charton and Pe´rez‐ OʹHara (2000b; 2001) used multivariate analysis Ruzafa 2001). Macroalgal structure cannot, and determined that dominant vegetation is a therefore, necessarily be used as an indicator of primary ecological driver of subtidal reef recruitment strength for algae associated fish on habitats. The study concluded that larger kelps reefs (Anderson 1994). (e.g. Phyllospora, Ecklonia, and Macrocystis) Effects of habitat forming biota are not just supported a relatively species‐poor epiphytic limited to plants, e.g. sponge assemblages, have

Temperate reefs literature review 27

also been shown to directly influence the Flindersarian biogeographical provinces distribution of reef fish in New South Wales (Connell 2007) (Curley et al. 2002) as well as other areas, such as C. rodgersii and another barren forming urchin the Mediterranean (Sanchez‐Jerez et al. 2002). Evenchinus chloroticus appear to have a major Herbivory and Grazing impact on habitats, and patterns in the Herbivorous fish can make up to 47% of the fish abundance and foraging of other species. species present on some Victorian subtidal reefs Herbivorous fish species such as Odax and (Jones and Andrew 1990), and these species are Parma victoriae were found to be influenced by often associated with their preferred algal food the grazing of both of these urchin species, but (Port of Melbourne Corporation 2007c). For the authors conclude that it is unknown if this example, fish species such as herring cale Odax finding is the representative of all sea urchin‐ cyanomelas feed almost exclusively on patches of fish species interactions (Jones and Andrew Ecklonia radiata and are more abundant on the 1990). Andrew and Stocker (1986) studied the southern shallow reefs where these species are microhabitat, occupancy, dispersion and more dominant (Jones and Andrew 1990). The movement of E. chloroticus. The study found sea Victorian scalyfin Parma victoriae feeds in areas urchins were positively associated with where kelp is absent and red algal turfs are encrusting coralline algae but movement with present (Jones and Andrew 1990). Territorial regards to algae needs to be further investigated. herbivorous fish such as P. victoriae and O. Andrew (1993) investigated the effect of cyanomelas may affect algal distribution and availability of shelter on the foraging behaviour abundance by (1) direct feeding effect due to of C. rogersii, and on the abundance of consumption of algae, (2) weeding out of algae invertebrates and algae. The study found that to promote growth of preferred algae and (3) urchin recruitment was not restricted to high effects due to exclusion of other herbivorous shelter areas, but barren creation was heavily fish. reliant on shelter and urchin grazing caused Herbivorous fish are generally found to have a reductions in the density of foliose algae and localised impact on algae where as grazing limpets. Andrew and OʹNeill (2000) mapped urchins like Centrostephanus rodgersii appear to shallow subtidal habitats in New South Wales have a major effect on spatial patterns in the and estimated the coverage of C. rogersii barren distribution of macroalgae (Jones and Andrew habitat. The study found that the extensive 1990). coverage of the barren habitat in New South Wales is likely to limit the productivity of the Sea urchins are described throughout the abalone industry and the development of a sea literature as key components of temperate reef urchin fishery may have large impacts on ecosystems as they graze on algae and modify habitat representation on near shore reefs. A habitat, influencing the distribution and commercial fishery is currently developing for composition of subtidal reef communities sea urchins in Victoria with harvesting of the (Australian Government 2005). Several species white sea urchin Heliocidaris and C. rogersii of urchins exist in Victoria but only the black recording a catch valued at $191,199 in 2003/04 urchin Centrostephanus rogersii causes ‘urchin (Australian Government 2005). barren’ or ‘white rock’ habitat which is devoid of macroalgae (Australian Government 2005). In New South Wales, Gillanders and Kingsford Urchin barrens are restricted to the far‐east of (1998) found small Achoerodus viridis in greater Victoria where C. rogersii is present in high numbers in kelp beds than in adjacent urchin abundance (Keough and Butler 1996; OʹHara barrens, although the species appeared to be 2000b; Ferns 2003; Department of the flexible in its use of habitats on reefs, suggesting Environment and Heritage 2005). Several that populations would survive readily if more studies have been conducted on the creation, urchin barrens were created in an area . In maintenance and effect of urchin barrens north‐eastern New Zealand, some species of reef elsewhere in southern Australia and New fish have shown similar patterns, while others Zealand (Andrew and MacDiarmid 1991; were more closely linked to kelp or urchin Andrew 1993; Andrew and OʹNeill 2000). In barrens (Anderson and Millar 2004). Parma Victoria, urchin barrens have been described at microlepsis in NSW have been shown to exhibit Cape Howe MNP (Ball and Blake 2007b). The exactly the opposite pattern (Holbrook et al. presence of C. rogersii barrens represents one of 1994). the major differences between the Perionian and

Temperate reefs literature review 28

Larval supply/recruitment food is limiting as they can graze directly on Like intertidal habitats, larval supply, macroalgae and create barrens where abalone do connectivity and recruitment are key processes not occur (Andrew and Underwood 1992). structuring communities on sub‐tidal reefs Jenkins (2004) states that most work would (Keough and Swearer 2007). suggest abalone fluctuations may be affected by urchin abundances and the reverse is less likely. Recruitment processes in blacklip abalone, However, there are suggestions that when food Haliotis rubra, were related to regional is not limiting abalone are superior competitors hydrodynamics in eastern Victoria (McShane et for space, such as in crevices. al. 1988). The study suggested that dispersal of abalone larvae is primarily local. Results At Popes Eye in Port Phillip Bay, research on indicated that local reef topography could Parma victoriae found that territory size was sufficiently attenuate currents for larvae to stay related to intraspecific interactions, with the size on the parent reef for the full 3 ‐7 day pelagic of territories increasing considerably when period. neighbours were removed. No correlation existed between territory size and fish body size Hunt (2007) investigated the ecological or age, and no relationship was found between determinants for recruitment in a reef‐associated territory size and food abundance following planktivorous fish in Port Phillip Bay, the experimental manipulations of algal food southern hulafish Trachinops caudimaculatus. The abundance (Norman and Jones 1984). P. victoriae study surveyed the density of fish populations with larger territories do, however, have a wider and various microhabitat characteristics and variety and abundance of food types as larger analysed them together to detect relationships. territories typically include a wider range of Microhabitat characteristics explained 85% of microhabitats (Jones and Norman 1986). the spatial variation in recruit density, with food accessibility characteristics in the form of high Predation plankton supply and low suspended sediment Predation is a top‐down process that has been being the most important for recruitment. linked to trophic cascades in subtidal ecosystems. This occurs where removal of large Jenkins and Wheatley (1998) studied the predators from the reef ecosystem leads to an recruitment of fish in shallow sub‐tidal habitats increase in lower trophic levels that can have in Port Phillip Bay and found that while most profound effects on the ecosystem. An example emphasis in the past has been placed on of this occurs in New Zealand where removal of seagrass beds as nursery areas for juvenile fish, snapper (Pagrus auratus) and rock lobster (Jasus reef‐algal habitat showed similar levels of edwardsii) leads to a proliferation of urchins and recruitment to seagrass habitats for a number of subsequent barren formation (Shears and species such as King George whiting, Sillaginodes Babcock 2002). When marine protected areas punctata. Juveniles of most species commonly were declared, there was a subsequent increase thought to use seagrass as a nursery area were in lobsters and snapper, and a corresponding also found to recruit to shallow subtidal reef. growth of kelp forests (Shears and Babcock Exceptions were relatively specialised groups 2002). such as pipefish. Rock lobster are considered to be a keystone Although the number of studies to date in species on temperate reefs in Victoria because Victoria on recruitment to subtidal reefs is their feeding activities can have a significant limited, the are currently a number of studies effect on the structure of reef ecosystems underway addressing issues of larval supply, (Jenkins et al. 2005b). Adult rock lobsters are connectivity and recruitment of fish to subtidal carnivorous and feed mostly at night on a reefs in Port Port Phillip Bay (S.E. Swearer, P.A. variety of bottom dwelling invertebrates such as Hamer, pers. comm.). molluscs, crustaceans and echinoderms Competition (Department of Primary Industries 2009b). In In contrast to intertidal reefs, little research has Tasmania, the spread of Centrostephanus rodgersii been conducted on competition on subtidal reefs barrens may be related both to climate change in Victoria. Competitive relationships for food (facilitating a range extension) and heavy fishing and space are likely to exist between abalone of rock lobsters allowing urchin populations to and sea urchins as both co‐occur in reef increase and lead to barren formation (Connell ecosystems and feed on drift algae (Jenkins 2007). 2004). Urchins may be better competitors where

Temperate reefs literature review 29

The few studies of predation on subtidal reefs in Abalone Victoria have focussed on the 11 arm sea stars A number of studies have been conducted in Coscinasterias muricata. Day et al. (1995) found Victoria on abalone movement and dispersal, that C. muricata fed predominantly on mussels particularly in terms of implications for and to a lesser extent other molluscs and abundance and mortality estimates for stock invertebrates. Abalone were rarely eaten except assessment purposes. Abalone were found to where aggregations were found eating abalone move and re‐aggregate after removal by when other prey were scarce. Abalone were experimental fishing, potentially affecting found to have a number of behavioural estimates of abundance (Officer et al. 2001). responses that increased the likelihood of Another study followed dispersal of tagged escaping predation. McShane and Smith (1986) abalone from experimental plots (Dixon et al. recorded very high mortality of tagged abalone 1998). Dispersal contributed 40‐60% of tag as a result of predation by a dense aggregation disappearance and potentially has a significant of C. muricata on a subtidal reef in Port Phillip affect on mortality estimates. The magnitude of Bay. movements varied with habitat quality and is potentially affected by fishing (Dixon et al. 1998). Major commercial fisheries Subtidal reefs support the two most valuable Jenkins (2004) summarised the ecosystem effects commercial fisheries in Victoria: abalone and of abalone fishing by reviewing papers that rock lobster. The Victorian abalone fishery investigated interactions between abalone and commenced in 1962 and includes blacklip, the Victorian temperate reef ecosystem Haliotis rubra and greenlip, H. laevigata species. including feeding, competition, commensalism, Abalone are the most valuable commercial predation and parasitism. Abalone appear not to fishery in Victoria, worth currently about $28.5 have a structurally important role in the reef million (Department of Primary Industries ecosystem due to their passive feeding on drift 2009a). The rock lobster, J. edwardii fishery is the macroalgae (Shepherd and Clarkson 2001). second most valuable commercial fishery in Jenkins (2004) concluded that the literature Victoria after abalone. The 2008/09 catch was suggests a low effect of abalone fishing on the valued at about $14.3 million (Department of ecosystem in comparison to other fishing Primary Industries 2009b). activities, such as trawling and dredging. However, this should not circumvent rigorous After a planktonic larval stage, both abalone and experiments into the impacts of the fishery and rock lobster settle to a benthic rocky reef investigation into ecological interactions. existence on coastal reefs throughout Victoria (McShane 1999; Department of Primary Following this conclusion, Jenkins et al. (2005a) Industries 2009b). Abalone are found on analysed abalone/ecosystem monitoring data‐ Victorian reefs to depths of 60 m but they are sets from the Abalone Assessment Monitoring most commonly found in shallow water less program conducted by DPI and the Subtidal than 10 m deep (Harry Gorfine pers. comm, Reef Monitoring Program conducted by Parks McShane 1999). Greenlip abalone are patchily Victoria/DSE to identify ecological interactions distributed west of Wilsons Promontory whilst and potential indicator species for abalone. The blacklip abalone have a relatively consistent taxon that showed positive correlation over the distribution,, extending throughout Victoria broadest geographical area was encrusting algae (Harry Gorfine Pers. comm.). Southern rock or “pink rock”, which abalone larvae are lobster are found to depths of 150 metres, with dependent on for settlement (Daume et al. 1999). most of the commercial catch coming from Considering abalone undergo limited dispersal inshore water less than 100 metres deep (Prince 2003), Jenkins et al. (2005a) described the (Department of Primary Industries 2009b). The correlation of abalone and crustose coralline abundance of rock lobster decreases from west algae as a reasonable expectation. to east in Victoria reflecting a decreasing area of Rock lobster suitable rocky reef habitat (Department of A recent project by Ball et al. (in prep) used Primary Industries 2009b). The ecology of underwater video techniques to (1) describe abalone and rock lobster has been investigated critical habitat of rock lobsters and (2) identify in several studies revealing relationships with potential interactions between rock lobster and biotic and abiotic features of Victorian temperate other species. A total of twelve fixed sites were reef habitats. surveyed using underwater video in the western and eastern zones of the Victorian rock lobster

Temperate reefs literature review 30

fishery. The video habitat data was analysed with rock lobster catch data to assess interactions between rock lobsters, habitat and other species. Results for the analyses determined that distinct habitat assemblages could be linked with depth, and a number of habitat parameters were identified as being important in determining rock lobster distributions. These variables were depth, proportion of continuous rocky reef, percentage cover of P. comosa, percentage cover of understorey red algae and percentage cover of sessile invertebrates. A positive relationship was found between rock lobster and patchy reef, which may provide rock lobster with greater foraging opportunities and protection compared with continuous reef. The study concludes by stating that it only investigated the relationship between physical and biological habitat and rock lobster catches, but oceanographic influences such as wave energy and nutrient rich upwellings may also be linked to rock lobster distribution and abundance.

Temperate reefs literature review 31

Edmunds et al. (2006b) and several of these Deep reefs and canyons drivers are discussed below. The Port Phillip Heads region contains deep reef Physical drivers habitat and species that are unique within Port Phillip Bay (Edmunds et al. 2006b). These As light intensity diminishes with depth, habitats and the biota resident there were animals replace plants as the dominant life form surveyed prior to recent channel deepening (Keough and Butler 1996; OʹHara et al. 1999). activity, primarily using video from ROVs, as Algae, including encrusting red coralline algae were other deep reef habitats within Port Phillip that are often found on deep reefs, is typically Bay which included the Rip (between Point replaced by attached invertebrates such as Lonsdale and Point Nepean), Schnapper Deep, sponges, bryozoans, corals and ascidians Portsea Hole, Spectacular Reef and Far Side Reef (Edmunds et al. 2006b). (diver video), and at Wilson’s Promontory (drop Recent surveys carried out on a number of deep video) and Point Addis (towed video) on the reefs in Victoria have described how the open coast (Edmunds et al. 2006b). This study dominant biota shows zonation with depth (Ball described a variety of substrate types in the Rip et al. in prep). Phyllospora comosa (crayweed) was and on other deep reefs within Port Phillip Bay, observed to depths of ~29 m, and typically grew with deep areas of The Rip having more with the kelp Ecklonia radiate which was the complex surface complexity than shallow areas dominant species observed to depths of ~ 48 m. (Chidgey 2006). Deep reefs in Port Phillip Heads E. radiata was the dominant species at the contain a range of assemblage types, some of majority sites, while P. comosa alone or with E. which are different to all other reefs surveyed radiata was an important component of the biota within and outside Port Phillip Bay, and are at a range of sites at Portland, Warrnambool, mainly dominated by encrusting sponges and Warrnambool West, Port Fairy West and from hydroids (Edmunds et al. 2006b). Ocean Grove to Torquay. At 60–80 m, sessile Many of the factors and processes responsible invertebrates began to replace these dominant for shaping assemblages on deep reefs are the large brown macroalgae. same as those that occur on shallow subtidal Ryan et al. (2005) described how submarine and intertidal reefs (see previous discussion). canyon and shelf topography can influence For example, substrate angle can effect the physical–biological coupling. Considerable distribution of sponges on deep reefs, and amounts of water circulate through deep water sponge diversity also varies with depth canyons due to a range of factors including (Maldonado and Young 1996). temperature gradients, eddies, oceanic currents Edmunds et al. (2006b) discussed the biology of and upwelling (Breaker and Broenkow 1994). organisms on deep reefs in Victoria, with the Such movements of large bodies of water have assumption that this was broadly similar to been shown to drive the movement of relatively species studied on shallow reefs, and described large quantities of sediments and sand (Hume et a variety of physical and ecological drivers al. 2000), which has ramifications for organisms related to the ecology of deep reefs in Victoria, that live in these environments. For example, particularly those in and around Port Phillip high levels of organic matter in sediments may Heads. These processes often interact with each influence species richness (Curdia et al. 2004), other and can therefore exert a variable excess sediments may cover and destroy influence on species found on and around deep assemblages (Okey 2003), or nutrient transport reefs. Very little, if any, research has been may be affected as in Perth Canyon off Western conducted in Victoria on these patterns and Australia where interactions occur between the processes and that done elsewhere in deep Leeuwin Current and upwelling (Hume et al. water has tended to concentrate on more widely 2000; Rennie et al. 2009). distributed soft sediments (Levin et al. 2001) This Interactions between topography and currents is due in part to the perceived difficulties can also influence the distribution of deep reef associated with sampling and conducting fishes. On deep shelf areas where cold water is manipulative experiments on deep reefs. uplifted from slopes, areas can exist where A summary of the likely factors involved in waters are nutrient rich and key prey are shaping the structure of assemblages are laid out abundant (Bax and Williams 2000), for example, in Tables 5‐7 following a recent review by at the head of Horseshoe Canyon where productive fishing grounds are found (Bax and

Temperate reefs literature review 32

Williams 2001). Strong currents may effect (Hypoplectrodes nigroruber). Schools of barber certain species due to their physical structure, perch (Caesioperca razor) are replaced by the and at a smaller scale, cracks, crevices and holes related butterfly perch (Caesioperca Lepidoptera) of varying sizes can provide microhabitat and (OʹHara et al. 1999). While fish present on influence the distribution of species in relation shallow subtidal reefs include algavores, to water movement (Beaman et al. 2005). For omnivores and carnivores, those on deep reefs example, currents in Port Phillip Heads are are typically carnivorous as algae are typically likely to have a greater effect on erect sponge not present at depth. Although common on species than encrusting species, as has been seen rocky reefs, sponges, hydrozoans, anthozoans, elsewhere (Bell and Barnes 2000; Bell et al. 2002), bryozoans, and ascidians are thought to be and may result in certain sponge species being largely unpalatable to reef fish (Russell 1983); it found in encrusting rather than erect forms is therefore likely that fish at these depths are (Abdo et al. 2008). feeding on associated mobile invertebrate fauna. Sponge assemblages are more stable on solid Competition reef rather than boulder substrates, but are more Sponges in deep water have been shown to be diverse on boulders (Carballo and Nava 2007). important competitors for space (Suchanek et al. This may be due in part to the fact that sponges 1983) and may live for long periods (Ayling on boulders can occur on surfaces at a variety of 1981), which is likely to effect the distribution of angles which produces microhabitats with other sessile species on deep reefs/canyons such varying degrees of shading and water as hydroids and bryozoans. The competitive movement. Boulders may also be more prone to ability of sponges is also increased by their disturbance, and intermediate levels of ability to regrow swiftly after injury (Duckworth disturbance are generally thought to increase 2003), and the ability of some encrusting species diversity (Sousa 1979). to grow quickly when free space becomes available yet grow slowly when it is limited and Ecological drivers they are undisturbed (Roberts and Davis 1996). Herbivory and grazing Verges et al. (2009) found that herbivory differs While sessile species may compete for free with depth from shallow to deep reefs and has space, they can also have positive interactions an important effect of the vertical distribution of on each other. For example, Abdo et al. (2008) algae to ~40 m. found that neighbouring sponge species protected each other from environmental In deeper areas of reefs, sessile species such as impacts. sponges provide structure and diversity, and may provide either direct or indirect resources Larval supply/recruitment for fish (Tissot et al. 2006). Species richness and Sponges can reproduce asexually and spread fish densities vary from shallow to deep reefs through the water column or across substrates (Love et al. 2009), and heterogeneous habitats, or neighbouring individuals. They can also substrate type and complexity have been shown reproduce sexually, releasing larvae, propagules to influence the distribution of fish assemblages or gametes into the water column. While asexual on deep reefs (Yoklavich et al. 2000; Anderson et reproduction and growth may be of primary al. 2009). importance to sponges (Jackson 1986), dispersal and recruitment are also important in sustaining Habitat structure populations and shaping assemblage structure The distribution of fish fauna is governed by (Keough 1988; Underwood and Keough 2001). biologically formed habitat structure as well as by food, and begins to change with the loss of The presence of large sessile species may effect the kelp‐associated wrasses and leatherjackets, larval deposition and food availability of and the appearance of fishes such as boarfishes adjacent species by altering fluid dynamics in (family Pentacerotidae), splendid perch the immediate area (Nowell and Jumars 1984). (Callanthias australis) and banded seaperch

Temperate reefs literature review 33

Knowledge gaps Recent and current efforts to map reef biota in the physical and ecological processes affecting relation to substrate and habitat type are the system. commendable and are providing a wealth of In the following we outline knowledge gaps that information on local systems. However, the exist for each of the reef systems that we have majority of information on reefs in Victoria discussed in this review. provides only a “snapshot” of assemblage structure and the distribution of species at one Intertidal reefs particular time of year or sampling site. What is Much of the work on reefs in Victoria that has lacking are examinations of temporal and spatial examined patterns and processes such as variation in the structure of assemblages on competition and settlement has been conducted different reef types, and in many cases more on intertidal reefs. basic information on which species occur and their basic ecology and behaviour. While general There are, however, still a number of knowledge patterns that shape reef communities have been gaps that include: examined world wide, and to some extent • Basic information on the biology and ecology locally, knowledge of processes and species of a range of species interactions effecting local species are less well understood. This is problematic as this • Quantitative examinations of spatial and information is likely to be important in helping temporal variation of assemblages on many us to understand what is shaping many of these shores, both in regional Victoria and within communities. Port Phillip Bay While understanding what species are in • Potential impacts of sedimentation, pollution assemblages and how and why they vary is etc on assemblages important, we also need to conduct research that • Linkages with adjacent assemblages from examines marine ecosystems in a broader different habitats geographical context across southern Australia. Victoria’s placement at the convergence of - e.g. how highly mobile predators such several biogeographical provinces (i.e. as fish and birds utilise intertidal rocky Flindersian, Peronian and Maugean) make it the reef habitats ideal place to conduct studies on a variety of • The ecology and importance of species that questions at these broader scales. are becoming targets of food and bait The amount of research and level of collection, but which have not traditionally understanding has been greatest for intertidal been collected in Victoria reefs, is lower for subtidal reefs, and is very • Interactions between coastal oceanography limited for deep and canyon reefs. This is and intertidal communities, i.e. effects of probably a reflection of ease of accessibility and upwelling such as on the Bonney coast logistical constraints. • How water level rises will affect reef Research on subtidal reefs in Port Phillip Bay has assemblages been fragmentary, and there is a poor understanding of the drivers influencing the reef - e.g. are there low lying reefs that will be communities and how these differ from the open completely covered? coast. Further research on the physiological and ecological drivers affecting subtidal reefs in Port Subtidal reefs Phillip Bay is required. Plummer et al. (2003) summarised the habitat types and species found on shallow reefs within Of special interest are the deep reef and canyon marine national parks and sanctuaries in habitats of Port Phillip Heads. This area has a Victoria. For many sites, they noted that while unique combination of deep water, strong anecdotal or qualitative data existed, quantitative currents, and coastal sedimentary processes. The data were often lacking. sessile invertebrate communities are well developed but their uniqueness is uncertain. It has been suggested that on shallow reefs in Detailed studies of taxonomy and assemblage Victoria, surrogates such as dominant vegetation structure are required along with research into and region may be more accurate for predicting assemblage structure, at least for algae and

Temperate reefs literature review 34

invertebrates (OʹHara 2001), than substrate alone, • Determining sources of larval recruitment and indeed recent predictive models appear to be and causes of variability in recruitment satisfactory for linking substrate and depth with • Standardising commercial catch rates and macroalgae (Holmes et al. 2008). determining stock status Gaps in our knowledge about shallow reefs, • Investigating the effect of seawater including those in Port Phillip Bay and along temperature of rock lobster ecology Victoria’s open coastline include: including the effect of the Bonny upwelling • Basic information on what species are found nutrient rich intrusion into western Victoria. and assemblage structure Deep reefs and canyons - Algae Little is known about deep reefs in Victoria, or - Sessile invertebrates the biology and ecology of organisms that live on them, due in part to difficulties associated with - Mobile invertebrates conducting observational work or manipulative - Fish experiments in situ. Almost nothing is therefore known about how various biotic factors influence • Quantitative data examining patterns of the distribution, survival, etc. of species found on spatial and temporal variation deep reefs, except for those species such as rock • Relationships with assemblages from lobster and abalone, where some information is adjacent habitats, e.g. sand and seagrass available due to directed research on these patches valuable fisheries species (see previous discussion of these fisheries). • The impact of introduced species Without basic information on the life history of • Relationship with coastal oceanography such organisms and details of how they interact with as the Bonney upwelling each other and the environment, it may not be possible to determine to what degree potential • Processes driving the ecology of sheltered subtidal reefs in Port Phillip Bay compared to disturbance events have an impact on individual exposed reefs on the open coast species or assemblages of species. Gaps in our knowledge about deep reefs, • Very little research has been carried out on invertebrates on subtidal reefs of Port Phillip including those in Port Phillip Heads include: Bay ƒ Basic information on what species are found and assemblage structure; this is true for • Processes relating to the export of drift algae and detritus from subtidal reefs and the both sessile species and associated mobile subsidy to other habitats (Vanderklift and invertebrates Wernberg 2008; Crawley et al. 2009). ƒ Spatial and temporal patterns of distribution of species on deep reefs through Victoria Key knowledge gaps for commercial fisheries of ƒ Which species are ecologically important abalone and rock lobster exist and have been ƒ identified for the purposes of this literature Rarity of species and assemblages in a wider review. geographical sense ƒ Abalone research is required (Harry Gorfine Processes determining the structure of pers. comm.) into: communities in deep reefs and canyons, especially in Port Phillip Heads (current, • The quantification of stock‐recruitment sediment loads, plankton/seston dynamics of the fishery concentration) • Age validation of individual abalone ƒ Identification of species and assemblages that specimens and are vulnerable to natural and human disturbance/impacts • Modelling the fishery as an entire system including management performance ƒ The uniqueness of sessile invertebrate species measures. in Port Phillip Heads deep reef and Canyon compared to other deep reef and canyon Rock lobster research is required (David Reilly pers. comm.) into: habitats in Victoria

Temperate reefs literature review 35

ƒ Trophic linkages between deep reefs and ƒ How communities change on a temporal canyon communities in Victoria and other basis, whether that be seasonally or between marine and terrestrial communities. years Due to this knowledge gap, key questions that ƒ How assemblages may recover from pulse or we are currently unable to answer with press disturbance events confidence include: ƒ How climatic or oceanographic changes may ƒ How the removal, increase or introduction of influence the distribution and health of species may effect assemblage structure assemblages.

Temperate reefs literature review 36

References

Abdo, D. A., McDonald , J. I., Harvey, E. S., Andrew, N. L., and Stocker, L. J. (1986). Fromont, J., and Kendrick, G. A. (2008). Dispersion and phagokinesis in the Neighbour and environmental echinoid Evechinus chloroticus (Val.). influences on the growth patterns of two Journal of Experimental Marine Biology and temperate Haliclonid sponges. Marine Ecology 100, 11‐23. and Freshwater Research 59, 304‐312. Andrew, N. L., and Underwood, A. J. (1992). Addison, P. F. E., Koss, R. S., and OʹHara, T. D. Associations and abundance of sea (2008). Recreational use of a rocky urchins and abalone on shallow subtidal intertidal reef in Victoria: implications reefs in southern New South Wales. for ecological research and Australian Journal of Marine and management. Australasian Journal of Freshwater Research 43, 1547‐1559. Environmental Management 15, 169‐179. Australian Government (2005). Assessment of Anderson, M. J., and Millar, R. B. (2004). Spatial the Victorian Sea Urchin Fishery. variation and effects of habitat on Australian Government, Department of temperate reef fish assemblages in the Environment and Heritage. northeastern New Zealand. Journal of Axelrad, D. M., Poore, G. C. B., Arnott, G. H., Experimental Marine Biology and Ecology Bauld, J., Brown, V. E., R.R.C., and 305, 191‐221. Hickman, N. J. (1981). The effects of Anderson, T. J., Syms, C., Roberts, D. A., and treated sewage discharge on the biota of Howard, D. F. (2009). Multi‐scale fish‐ Port Phillip Bay, Victoria, Australia. In habitat associations and the use of ʹEstuaries and Nutrientsʹ. (Eds B. J. habitat surrogates to predict the Neilson and L. G. Cronin.). (The organisation and abundance of deep‐ Humana Press) water fish assemblages. Journal of Ayling, A. M. (1981). The role of biological Experimental Marine Biology and Ecology disturbance in temperate subtidal 379, 34‐42. encrusting communities. Ecology 62, 830‐ doi:10.1016/j.jembe.2009.07.033 847. Anderson, T. W. (1994). Role of macroalgal Baines, P. G., and Fandry, C. B. (1983). Annual structure in the distribution and cycle of the density field in Bass Strait. abundance of a temperate reef fish. Australian Journal of Marine and Marine Ecology Progress Series 113, 279‐ Freshwater Research 34, 143‐153. 290. Baker, K. (2006). Top‐down and Bottom‐up Andrew, N., and OʹNeill, A. L. (2000). Large‐ regulation of rocky intertidal shores of scale patterns in habitat structure on southeastern Victoria, Australia. subtidal rocky reefs in New South Honours Thesis, University of Wales. Marine and Freshwater Research Melbourne. 51, 255‐263. Ball, D., and Blake, S. (2007a). Shallow water Andrew, N. L. (1993). Spatial heterogeneity, sea habitat mapping at Victorian Marine urchins grazing, and habitat structure National Parks and Marine Sanctuaries, on reefs in temperate Australia. Ecology Volume 1: Western Victoria. Parks 74, 292‐302. Victoria Technical Series No.36. Parks Andrew, N. L. (Ed.) (1999). ʹUnder Southern Victoria, Melbourne. Seas.ʹ (University of New South Wales Ball, D., and Blake, S. (2007b). Shallow water Press: Sydney.) habitat mapping at Victorian Marine Andrew, N. L., and MacDiarmid, A. B. (1991). National Parks and Marine Sanctuaries, Interrelations between sea urchins and Volume 2: Eastern Victoria. Parks spiny lobsters in northeastern New Victoria Technical Series No.37. Parks Zealand. Marine Ecology Progress Series Victoria, Melbourne. 70, 211‐222.

Temperate reefs literature review 37

Ball, D., Blake, S., and Plummer, A. (2006). supply of propagules, recruitment and Review of Marine Habitat Classification assemblages of intertidal macroalgae on Systems No. 26. Parks Victoria, a wave‐exposed rocky coast, Victoria, Melbourne. Australia. Journal of Experimental Marine Ball, D., Morris, L., Womersley, B., Blake, S., and Biology and Ecology 310, 207‐225. Coots, A. (In prep). Habitat assessment doi:10.1016/j.jembe.2004.04.011 of rock lobster fixed site survey areas. Benedetti‐Cecchi, L., Pannacciulli, F., Bulleri, F., Department of primary Industries, Moschella, P. S., Airoldi, L., Relini, G., Queenscliff, Victoria. and Cinelli, F. (2001). Predicting the Bax, N. J., and Williams, A. (2001). Seabed consequences of anthropogenic habitat on the south‐eastern Australian disturbance: large scale effects of loss of continental shelf: context, vulnerability canopy algae on rocky shores. Marine and monitoring. Marine and Freshwater Ecology Progress Series 214, 137‐150. Research 52, 491‐512. Bennett, I., and Pope, E. C. (1952). Intertidal Bax, N. J., and Williams, A. E. (2000). Habitat zonation of the exposed rocky shores of and fisheries productivity in the South Victoria, together with a rearrangement East Fishery. Final report to FRDC of the biogeographical provinces of Project 94/040. Marine Research, Hobart, temperate Australian shores. Australian Tasmania, Australia. Journal of Marine and Freshwater Research Beaman, R. J., Daniell, J. J., and Harris, P. T. 4, 105‐159. (2005). Geology‐benthos relationships Bennett, M. (1990). The effect of grazing on a temperate rocky bank, eastern Bass gastropods on the recovery of a Strait, Australia. Marine and Freshwater disturbance within the Hormosira mat. Research 56, 943‐958. Honours Thesis, University of Bell, J. D., Burchmore, J. J., and Pollard, D. A. Melbourne. (1978). Feeding ecology of three Beovich, E. K., and Quinn, G. P. (1992). The sympatric species of leatherjackets grazing effects of limpets on a rocky (Pisces: Monacanthidae) from a intertidal shore. Australian Journal of Posidonia seagrass habitat in New Ecology 17, 75‐82. South Wales. Australian Journal of Marine Black, K. P. (1992). Evidence of the importance and Freshwater Research 29, 631‐643. of deposition and winnowing of Bell, J. J., and Barnes, D. K. A. (2000). The surficial sediments at a continental shelf influences of bathymetry and flow scale. . Journal of Coastal Research 8, 319‐ regime upon the morphology of 331. sublittoral sponge communities. Journal Black, K. P., Hatton, D., and Rosenberg, M. of the Marine Biological Association of the (1993). Locally and externally‐driven United Kingdom 80, 707‐718. dynamics of a large semi‐enclosed bay Bell, J. J., Barnes, D. K. A., and Turner, J. R. in southern Australia. Journal of Coastal (2002). The importance of micro and Research 9, 509‐538. macro morphological variation in the Blake, S., Young, P., Ball, D., and Coots, A. adaptation of a sublittoral demosponge (2009a). Corangamite Nearshore Marine to current extremes. Marine Biology 140, Habitat Mapping and Assessment, 75‐81. Fisheries Victoria Technical Report Bellgrove, A. (1998). Recruitment of intertidal Series. Department of Primary macroalgae on a wave exposed rocky Industries, Queenscliff, Victoria, coast. PhD Thesis, Monash University. Australia. Bellgrove, A., Clayton, M. N., and Quinn, G. P. Blake, S., Young, P., Ball, D., and Coots, A. (1997). Effects of secondarily treated (2009b). Nearshore Marine Habitat sewage effluent on intertidal macroalgal Mapping and Assessment. Fisheries recruitment processes. Marine and Victoria, Department of Primary Freshwater Research 48, 137‐146. Industries, Queenscliff, Victoria, Bellgrove, A., Clayton, M. N., and Quinn, G. P. Australia. (2004). An integrated study of the Bodkin, J. L. (1988). Effects of kelp forest temporal and spatial variation in the removal on associated fish assemblages

Temperate reefs literature review 38

in central California. Journal of conservation values of the Bass Strait Experimental Marine Biology and Ecology sponge beds area: a component of the 117, 227‐238. Commonwealth Marine Conservation Bokn, T. L., Duarte, C. M., Pedersen, M. F., Assessment Program 2002‐2004: report Marba, N., Moy, F. E., Barrón, C., to Environment Australia. Bjerkeng, B., Borum, J., Christie, H., Butler, A., Althaus, F., Furlani, D., and Ridgway, Engelbert, S., Fotel, F. L., Hoell, E. E., K. (2002b). Assessment of the Karez, R., Kersting, K., Kraufvelin, P., conservation values of the Bonney Lindblad, C., Olsen, M., Sanderud, K. upwelling area: a component of the A., Sommer, U., and Sørensen, K. (2003). Commonwealth Marine Conservation The response of experimental rocky Assessment Program 2002‐2004 : report shore communities to nutrient to Environment Australia CSIRO, additions. Ecosystems 6, 577‐594. Hobart, Tasmania, Australia. Braley, H., Anderson, T. A., and Quinn, G. P. Campbell, S. J. (1999). Occurrence of Codium (1991). The effect of the grazing fragile subsp Tomentosoides (Chlorophyta gastropod Bembicium nanum on : Bryopsidales) in marine embayments recolonization of algae on an intertidal of southeastern Australia. Journal of rock platform. Proceedings of the Royal Phycology 35, 938‐940. Society of Victoria 103, 13‐16. Carballo, J. L., and Nava, H. (2007). A Breaker, L. C., and Broenkow, W. W. (1994). The comparison of sponge assemblage circulation of monterey bay and related patterns in two adjacent rocky habitats processes. In ʹOceanography and Marine (tropical Pacific Ocean, Mexico). Biology, Vol 32ʹ pp. 1‐64) Écoscience Brown, V. B., Davies, S. A., and Synnot, R. N. Carey, J. M., Beilin, R., Boxshall, A., Burgman, (1990). Long‐term monitoring of the M. A., and Flander, L. (2007). Risk‐Based effects of treated sewage effluent on the Approaches to Deal with Uncertainty in intertidal macroalgal community near a Data‐Poor System: Stakeholder Cape Schanck, Victoria, Australia. Involvement in Hazard Identification Botanica Marina 33, 85‐98. for Marine National Parks and Marine Brown, V. B., Rowan, K. S., and Ducker, S. C. Sanctuaries in Victoria, Australia. Risk (1980). The Effects of Sewage Effluent on Analysis 27, 271‐281. the Macrophytes off Werribee, Port Carr, M. H. (1989). Effects of macroalgal Phillip Bay. Ministry of Conservation assemblages on the recruitment of Victoria, Environmental Studies temperate zone reef fishes. Journal of Program, Task Report No. 273. Experimental Marine Biology and Ecology Bryan, G. W., Gibbs, P. E., Burt, G. R., and 126, 59‐76. Hummerstone, L. G. (1987). The effects Cheshire, A. C., and Hallum, N. D. (1989). of tributyltin (TBT) accumulation on Biomass and density of native stands of adult dogwhelks, Nucella lapillus; long Durvillaea potatorum (southern bull‐kelp) term field and laboratory experiments. in south eastern Australia. Marine Journal of the Marine Biological Association Ecology Progress Series 8, 277‐283. of the United Kingdom 67, 525‐544. Chidgey, S. (2006). Basslink Project Marine Burn, R. (2006). A checklist and bibliography of Biological Monitoring: McGaurans the Opisthobranchia (Mollusca: Beach. CEE Consultants Pty Ltd, Gastropoda) of Victoria and the Bass Richmond, Victoria, Australia. Strait area, south‐eastern Australia. Chidgey, S. S., and Marshall, P. A. (1994). Museum Victoria Science Reports 10, 1‐ Progress report on ground‐truthing 106. survey, June 1994, Port Phillip Bay Burton, B. (1999). Competitive interactions Environmental Study. between and within the intertidal Choat, J. H., and Ayling, A. M. (1987). The gastropod genera Cellana and Siphonaria. relationship between habitat structure PhD Thesis, University of Melbourne. and fish faunas on New Zealand reefs. Butler, A., Althaus, F., Furlani, D., and Ridgway, Journal of Experimental Marine Biology and K. (2002a). Assessment of the Ecology 110, 257‐284.

Temperate reefs literature review 39

Choat, J. H., and Schiel, D. R. (1982). Patterns of continental Australia. Journal of distribution and abundance of large Biogeography 35, 1608‐1621. brown algae and invertebrate herbivores Connell, S. D., and Irving, A. D. (2009). The in subtidal regions of northern New subtidal ecology of rocky‐coasts: local‐ Zealand. Journal of Experimental Marine regional‐biogeographic patterns and Biology and Ecology 60, 129‐162. their experimental analysis. In ʹMarine Cirano, M., and Middleton, J. F. (2004). Aspects macroecologyʹ. (Eds J. D. Witman and R. of the mean wintertime circulation Kaustuv.) pp. 392‐417. (University of along Australiaʹs southern shelves. Chicago Press: Chicago.) Journal of Physical Oceanography 34, 668‐ Crawley, K. R., Hyndes, G. A., Vanderklift, M. 684. A., Revill, A. T., and Nichols, P. D. Clayton, M. N. (1990). The adaptive significance (2009). Allochthonous brown algae are of life history characters in selected the primary food source for consumers orders of marine brown macroalgae. in a temperate, coastal environment. Australian Journal of Ecology 15, 439‐452. Marine Ecology Progress Series 376, 33‐44. Coleman, M. A., Vytopil, E., Goodsell, P. J., doi:10.3354/meps07810 Gillanders, B. M., and Connell, S. D. Creese, R. G., and Underwood, A. J. (1982). (2007). Diversity and depth‐related Analysis of inter‐ and intra‐ specific patterns of mobile invertebrates competition amongst intertidal limpets associated with kelp forests. Marine and with different methods of feeding. Freshwater Research 58, 589‐595. Oecologia 53, 337‐346. Coleman, R. F. (1972). Observations on shallow Curdia, J., Carvalho, S., Ravara, A., Gage, J. D., water, rocky reef fishes of port Phillip Rodrigues, A. M., and Quintino, V. Bay, Victoria. B.Sc. Thesis. (2004). Deep macrobenthic communities Connell, S. D. (2003a). The monopolization of from Nazare submarine canyon (NW understorey habitat by subtidal Portugal). ʹ pp. 171‐180. (Inst Ciencias encrusting coralline algae: a test of the Mar Barcelona.) combined effects of canopy‐mediated Curley, B. G., Kingsford, M. J., and Gillanders, B. light and sedimentation. Marine Biology M. (2002). Spatial and habitat‐related 142, 1065‐1071. patterns of temperate reef fish Connell, S. D. (2003b). Negative effects assemblages: implications for the design overpower the positive of kelp to of Marine Protected Areas. Marine and exclude invertebrates from the Freshwater Research 53, 1197‐1210. understorey community. Oecologia 137, Daily, G. C., Alexander, S., Ehrlich, P. R., 97‐103. Goulder, L., Lubchenco, J., Matson, P. Connell, S. D. (2005). Assembly and A., Mooney, H. A., Postel, S., Schneider, maintenance of subtidal habitat S. H., Tilman, D., and Woodwell, G. M. heterogeneity: synergistic effects of light (1997). Ecosystem Services: Benefits penetration and sedimentation. Marine Supplied to Human Societies By Natural Ecology Progress Series 289, 53‐61. Ecosystems. Issues in Ecology 2, 1‐16. Connell, S. D. (2007). Subtidal temperate rocky Dartnall, A. J. (1974). Littoral biogeography. In habitats: Habitat heterogeneity at local ʹBiogeography and Ecology in to continental scales. In ʹMarine Tasmaniaʹ. (Ed. W. D. Williams.) pp. Ecologyʹ. (Eds S. D. Connell and B. M. 171‐194. (Dr. W. Junk b.v., Publishers: Gillanders.) pp. 378‐401. (Oxford The Hague.) University Press: South Melbourne.) Daume, S., Brand‐Gardner, S., and Woelkerling, Connell, S. D., and Gillanders, B. M. (2007). W. J. (1999). Preferential settlement of ʹMarine Ecology.ʹ (Oxford University abalone larvae: diatom films vs. non‐ Press: Oxford.) geniculate coralline red algae. Connell, S. D., and Irving, A. D. (2008). Aquaculture 174, 243‐254. Integrating ecology with biogeography Day, R., Dowell, A., Sant, G., Klemke, J., and using landscape characteristics: a case Shaw, C. (1995). Patchy predation: study of subtidal habitat across Foraging behaviour of Coscinasterias calamaria and escape responses for

Temperate reefs literature review 40

Haliotis rubra. Marine and Freshwater Edmunds, M., Hart, S., Elias, J., and Jenkins, S. Behaviour and Physiology 26, 11‐33. (2003). Victorian subtidal reef Dayton, P. K., Currie, V., Gerrodette, T., Keller, monitoring program: The reef biota at B. D., Rosenthal, R., and VenTresca, D. Port Phillip Heads Marine National (1984). Patch dynamics and stability of Park. Parks Victoria, Melbourne. some California kelp communities. Edmunds, M., Hart, S., Elias, J., and Power, B. Ecological Monographs 54, 253‐289. (2004). Victorian intertidal reef Department of Primary Industries (2009a). ʹThe monitoring program: The reef biota in Victorian Abalone Fishery.ʹ Available at Central Victoria and Port Phillip Bay http://www.dpi.vic.gov.au/DPI/nrenfaq. Marine Sanctuaries. Parks Victoria, nsf/LinkView/9F09A1B4418E935BCA256 Melbourne. C55001EB9A9F5F3C3DA915AFBE4CA2 Edmunds, M., Judd, A., Gilmour, P., Stewart, K., 56C6F0016CA60 [accessed 11/11/2009. Pickett, P., Monk, J., and Crozier, J. Department of Primary Industries (2009b). (2006a). Volume 8: Shallow Reefs. Victorian Rock Lobster Fishery Report to Maunsell. Australian Marine Management Plan. Fisheries Victoria Ecology Report 356, Melbourne. Management Report Series No. 70. Edmunds, M., Power, B., Pickett, P., Baker, K., Melbourne. Wassnig, M., Crozier, J., Monk, J., Department of the Environment and Heritage Gilmour, P., Shimeta, J., Sams, M., Judd, (2005). Assessment of the Victorian Sea A., Williams, J., and Stewart, K. (2006b). Urchin Fishery. Australian Government, Volume 9: Deep Reef Biota. Report to Canberra. Maunsell. Australian Marine Ecology Department of the Environment, W., Heritage Report 357, Melbourne. and the Arts (2008). ʹNational Edmunds, M., Roob, R., and Ferns, L. W. (2000). Representative System of Marine Chapter 6 Marine biogeography of Protected Areas (NRSMPA).ʹ Available central Victoria and Flinders bioregions at ‐ A preliminary analysis of reef flora http://www.environment.gov.au/coasts/ and fauna. In ʹEnvironmental inventory mpa/nrsmpa/index.html. of Victoriaʹs Marine Ecosystems Stage 3 Dixon, C. D., Gorfine, H. K., Officer, R. A., and (2nd Edition) ‐ Understanding Sporcic, M. (1998). Dispersal of tagged Biodiversity Representativeness of blacklip abalone, Haliotis rubra: Victoriaʹs Rocky Reefsʹ. (Eds L. W. Ferns Implications for stock assessment. and D. Hough.). (Parks, Flora and Fauna Journal of Shellfish Research 17, 881‐887. Division, Department of Natural Doblin, M., and Clayton, M. N. (1995). The Resources and Environment: East effects of secondarily treated sewage Melbourne.) effluent on the early life history stages of Elias, J., Edmunds, M., and Hart, S. (2004). Port two species of brown macroalgae: Phillip Bay channel deepening Hormosira banksii and Durvillea environmental effects statement ‐ potatorum. Marine Biology 122, 689‐698. marine ecology specialist studies. Duckworth, A. R. (2003). Effect of wound size on Volume 7: deep reef habitat study. Port the growth and regeneration of two of Melbourne Corporation, Melbourne. temperate subtidal sponges. Journal of Environment Conservation Council (2000). Experimental Marine Biology and Ecology Marine Coastal & Estuarine 287, 139‐153. Investigation Final Report. Environment Duggins, D. O. (1989). Magnification of Conservation Council, East Melbourne. secondary production by kelp detritus Fairweather, P. G. (1990). Sewage and the biota in coastal marine ecosystems. Science on seashores: assessment of impact in 245, 170‐173. relation to natural variability. Edgar, G. J. (1984). General features of the Environmental Maonitoring and ecology and biogeography of tasmanian Assessment 14, 197‐210. subtidal rocky shore communities. Fairweather, P. G. (1991). A conceptual Papers and Proceedings of the Royal Society framework for ecological studies of of Tasmania 118, 173‐186. coastal resources: an example of a

Temperate reefs literature review 41

tunicate collected for bait on Australian fish local assemblage. Marine Biology seashores. Ocean and shoreline 138, 917‐934. management 15, 125‐142. Gibbs, P. E., Bryan, G. W., Pascoe, P. L., and Ferns, L. (2003). Victoria’s system of marine G.R., B. (1987). The use of the dogwhelk, national parks and marine sanctuaries: Nucella lapillus as an indicator of management strategy 2003‐2010. tributyltin (TBT) contamination. Journal Melbourne, Australia. of the Marine Biological Association of the Ferns, L. W., and Hough, D. (2000). United Kingdom 67, 507‐523. Environmental inventory of Victoriaʹs Gill, E. D., Segnit, E. R., and Hunt, I. (1980). Marine Ecosystems Stage 3 (2nd Pleistocene submerged cliff off the Edition). Parks, Flora and Fauna Otway coast of Victoria. Proceeding of the Division, Department of Natural Royal Society of Victoria 91, 43‐51. Resources and Environment, East Gillanders, B. M. (1995). Feeding ecology of the Melbourne. temperate marine fish Achoerodus viridis Ferns, L. W., Hough, D., and Caitlin, J. (2000). (Labridae): size, seasonal and site‐ Chapter 1 Synthesis of stage 3. specific differences. Marine and Describing marine biodiversity through Freshwater Research 46, 1009‐1020. mapping and quantitative analysis of Gillanders, B. M. (1997a). Comparison of growth biological data: A classification system rates between estuarine and coastal reef for Victoriaʹs intertidal and nearshore populations of Achoerodus viridis (Pisces: sub‐tidal marine waters. In Labridae). Marine Ecology Progress Series ʹEnvironmental inventory of Victoriaʹs 146, 283‐287. Marine Ecosystems Stage 3 (2nd Gillanders, B. M. (1997b). Patterns of abundance Edition) ‐ Understanding Biodiversity and size structure in the blue groper, Representativeness of Victoriaʹs Rocky Achoerodus viridis (Pisces, Labridae): Reefsʹ. (Eds L. W. Ferns and D. Hough.). evidence of links between estuaries and (Parks, Flora and Fauna Division, coastal reefs. Environmental Biology of Department of Natural Resources and Fishes 49, 153‐173. Environment: East Melbourne.) Gillanders, B. M., and Kingsford, M. J. (1998). Fletcher, H., and Frid, C. L. J. (1996). Impact and Influence of habitat on abundance and management of visitor pressure on size structure of a large temperate reef rocky intertidal algal communities. fish, Achoerodus viridis (Pisces : Aquatic conservation: Marine and Labridae). Marine Biology 132, 503‐514. freshwater ecosystems 6, 287‐297. Gilmour, P., and Edmunds, M. (2007). Victorian Flora and fauna guarantee ‐ scientific advisory intertidal reef monitoring program: The committee (2009). Final intertidal reef biota of Central Victoriaʹs recommendation on a nomination for Marine Protected Areas (Volume 2). listing: Port Phillip Bay entrance deep Parks Victoria, Melbourne. canyon marine community. Nomination Goodsell, P. J., Fowler‐Walker, M. J., Gillanders, no. 794. B. M., and Connell, S. D. (2004). Foale, S. (1993). An evaluation of the potential of Variations in the configuration of algae gastropod imposex as a bioindicator of in subtidal forests: Implications for tributyltin pollution in Port‐Phillip Bay, invertebrate assemblages. Austral Victoria. Marine Pollution Bulletin 26, Ecology 29, 350‐357. 546‐552. Gorgula, S. C., S., (2004). Expansive covers of Fulton, C. J., and Bellwood, D. R. (2004). Wave turf‐forming algae on human dominated exposure, swimming performance, and coast: the relative effects of increasing the structure of tropical and temperate nutrient and sediment loads. Marine reef fish assemblages. Marine Biology Biology 145, 613‐619. 144, 429‐437. Harris, P. T. (2007). Applications of geophysical Garcı´a‐Charton, J. A., and Pe´rez‐Ruzafa, A. information to the design of a (2001). Spatial pattern and the habitat representative system of marine structure of a Mediterranean rocky reef protected areas in southeastern Australia. In ʹMapping the seafloor for

Temperate reefs literature review 42

habitat characterisation: Geological Holbrook, S. J., Kingsford, M. J., Schmitt, R. J., Association of Canada special paper 47ʹ. and Stephens Jr, J. S. (1994). Spatial and (Eds B. J. Todd and G. Greene.) pp. 449‐ temporal patterns in assemblages of 468: St Johns, NF, Canada.) temperate reef fish. American Zoologist Harris, P. T., Heap, A. D., Anderson, T. J., and 34, 463‐475. Brooke, B. (2009). Comment on: Holbrook, S. J., Schmitt, R. J., and Ambrose, R. F. Williams et al. (2009) ʺAustraliaʹs deep‐ (1990b). Biogenic habitat structure and water reserve network: implications of characteristics of temperate reef fish false homogeneity for classifying abiotic assemblages. Australian Journal of surrogates of biodiversityʺ ICES Journal Ecology 15, 489‐503. of Marine Science, 66: 214–224. ICES Holmes, K. W., Radford, B., Van Niel, K. P., Journal of Marine Science 2082‐2085 Kendrick, G. A., Grove, S. L., and Harris, P. T., Heap, A. D., Passlow, V., Sbaffi, L., Chatfield, B. (2007). Mapping the Fellows, M., Porter‐Smith, R., Buchanan, benthos in Victoria’s Marine National C., and Daniell, J. (2005). Geomorphic Parks, 1. Cape Howe Marine National features of the continental margin of Park. Parks Victoria, Melbourne. Australia: report to the National Oceans Holmes, K. W., Van Niel, K. P., Radford, B., Office on the production of a consistent, Kendrick, G. A., and Grove, S. L. (2008). high‐quality bathymetric data grid and Modelling distribution of marine definition and description of benthos from hydroacoustics and geomorphic units for part of Australia’s underwater video. Continental Shelf marine jurisdiction. Geoscience Research 28, 1800‐1810. Australia, Canberra. Hope Black, J. (1971). Benthic communities. Hawkins, S. J. (1981). The influence of season Memoirs of The National Museum of and barnacles on the algal colonization Victoria Melbourne 32, 129‐170. of Patella vulgata exclusion areas. Journal Hume, T. M., Oldman, J. W., and Black, K. P. of the Marine Biological Association of the (2000). Sediment facies and pathways of United Kingdom 61, 1‐15. sand transport about a large deep water Hidas, E. Z., Costa, T. L., Ayre, D. J., and headland, Cape Rodney, New Zealand. Minchinton, T. E. (2007). Is the species New Zealand Journal of Marine and composition of rocky intertidal Freshwater Research 34, 695‐717. invertebrates across a biogeographic Hunt, T. L. (2007). Ecological determinants of barrier in south‐eastern Australia recruitment in populations of the related to their potential for dispersal? southern hulafish, Trachinops Marine and Freshwater Research 58, 835‐ caudimaculatus. Bachelor of Science, 842. Degree with Honours Thesis Honours Hill, M. S., and Hill, A. L. (2002). Morphological Thesis Thesis, University of Melbourne. plasticity in the tropical sponge IMCRA (1998). Interim Marine and Coastal Anthosigmella varians: responses to Regionalisation for Australia: am predators and wave energy. The ecosystem‐based classification for Biological Bulletin 202, 86‐95. marine and coastal environments. Hindell, J. S., and Quinn, G. P. (2000). Effects of Version 3.3. Environment Australia, sewage effluent on the population Commonwealth Department of structure of Brachidontes rostratus Environment, Canberra, Australia. (Mytilidae) on a temperate intertidal Irving, A. D., Connell, S. D., and Gillanders, B. rocky shore. Marine and Freshwater M. (2004). Local complexity in patterns Research 51, 543‐551. of canopy‐benthos associations Holbrook, S. J., Carr, M. H., Schmitt, R. J., and produces regional patterns across Coyer, J. A. (1990a). Effect of giant kelp temperate Australasia. Marine Biology on local abundance of reef fishes: the 144, 361‐368. importance of ontogenetic resource Jackson, J. B. C. (1986). Modes of dispersal of requirements. Bulletin of Marine Science clonal benthic invertebrates: 47, 104‐114. consequences for species distributions and genetic structure of local

Temperate reefs literature review 43

populations. Bulletin of Marine Science organisms along environmental 39, 588‐606. gradients. Marine Biology 134, 295‐306. Jenkins, G. P. (2004). The ecosystem effects of Kaandorp, J. A., and Kluijver, M. J. d. (1992). abalone fishing: a review. Marine and Verification of fractal growth models of Freshwater Research 55, 545‐552. the sponge Haliclona oculata (Porifera) Jenkins, G. P., Gason, A. S. H., and Morris, L. with transplantation experiments. (2005a). Towards Ecosystem Based Marine Biology 113, 133‐143. Management of the Victorian Abalone Kaehler, S., and Williams, G. A. (1997). Do Fishery: Analysis of Existing Ecological factors influencing recruitment Monitoring Data. Department of ultimately determine the distribution Primary Industries, Victoria, and abundance of encrusting algae on Queenscliff. seasonal tropical shores? Marine Ecology Jenkins, G. P., Morris, L. C., and Blake, S. Progress Series 156, 87‐96. (2005b). Ecological Risk Assessment of Keough, M. J. (1988). Benthic Populations: is the Victorian Rock Lobster Fishery. recruitment limiting or just fashionable? Department of Primary Industries, In ʹProceedings of the 6th International Victoria, Queenscliff. Coral Reefs Symposium ʹ. pp. 141‐148. Jenkins, G. P., Watson, G. F., Hammond, L. S., Keough, M. J. (1999). Sessile Animals. In ʹUnder Black, K. P., Wheatley, M. J., and Shaw, Southern Seas, the ecology of Australiaʹs C. (1996). Importance of shallow water, Rocky Reefsʹ. (Ed. N. Andrew.). (UNSW: reef‐algal habitats as nursery areas for Sydney.) commercial fish from southeastern Keough, M. J., Black, K. P., Russell, J. S., and Australia. Fisheries Research and Craig, W. O. (1996). Predicting the Scale Development Corporation, 92/44. of Marine Impacts: Understanding Jenkins, G. P., and Wheatley, M. J. (1998). The Planktonic Links between Populations. influence of habitat structure on In pp. 199‐234. (Academic Press: San nearshore fish assemblages in a Diego.) southern Australian embayment: Keough, M. J., and Butler, A. J. (1996). Chapter Comparison of shallow seagrass, reef‐ 11. Temperate reefs. In ʹThe state of the algal and unvegetated sand habitats, marine environment report for with emphasis on their importance to Australiaʹ. (Ed. L. P. Zann.). (GBRMPA: recruitment. Journal of Experimental Townsville.) Marine Biology and Ecology 221, 147‐172. Keough, M. J., and King, A. (1991). Jennings, J. N. (1958). The submarine Recommendations for monitoring of topography of Bass Strait. Proceeding of marine plant and animal populations in the Royal Society of Victoria 71, 49‐71. Wilsons Promontory Marine National Jones, G. P. (1984). Population ecology of the Park and the Bunurong Marine Park. temperate reef fish Pseudolabrus celidotus Melbourne. Bloch and Schneider (Pisces: Labridae). Keough, M. J., and Quinn, G. P. (1998). Effects of I. Factors influencing recruitment. periodic disturbances from trampling on Journal of Experimental Marine Biology and rocky intertidal algal beds. Ecological Ecology 75, 257‐276. Applications 8, 141‐161. Jones, G. P., and Andrew, N. L. (1990). Keough, M. J., and Quinn, G. P. (2000). Herbivory and patch dynamics on rocky Legislative vs. practical protection of an reefs in temperate Australasia: The roles intertidal shoreline in southeastern of fish and sea urchins. Australian Australia. Ecological Applications 10, 871‐ Journal of Ecology 15, 505‐520. 881. Jones, G. P., and Norman, M. D. (1986). Feeding Keough, M. J., Quinn, G. P., and Bathgate, R. selectivity in relation to territory size in (1997). Geographic variation in a herbivorous reef fish. Oecologia 68, 549‐ interactions between size classes of the 556. limpet Cellana tramoserica. 215, 19‐34. Kaandorp, J. A. (1999). Morphological analysis Keough, M. J., Quinn, G. P., and King, A. (1990). of growth forms of branching sessile The ecology of temperate reefs. Australian Journal of Ecology 15, 361‐363.

Temperate reefs literature review 44

Keough, M. J., Quinn, G. P., and King, A. (1993). Lewis, J. R. (1964). ʹEcology of rocky shores.ʹ Correlations between human collecting (The English Universities Press: and intertidal mollusk populations on London.) rocky shores. Conservation Biology 7, 378‐ Light, B. R., and Woelkerling, W. J. (1992). 390. ʹLiterature and information review of Keough, M. J., and Swearer, S. E. (2007). the benthic flora of Port Phillip Bay, Fundamental concepts in marine Victoria, Australia / B.R. Light and Wm. ecology. In ʹMarine Ecologyʹ. (Eds S. D. J. Woelkerling.ʹ (CSIRO: Melbourne :.) Connell and B. M. Gillanders.) pp. 17‐46. Little, C., Williams, G. A., and Trowbridge, C. (Oxford University Press: South (2009). ʹThe Biology of Rocky Shores.ʹ Melbourne.) (Oxford University Press: Oxford.) King, A. (1992). Human activity and its effects Littler, M. M., and Murray, S. N. (1975). Impact on marine intertidal plant and animal of sewage on the distribution, populations: monitoring and abundance and community structure of management. B.Sc. Thesis, University of rocky intertidal macro‐organisms. Melbourne. Marine Biology 30, 277‐291. King, R. J., Hope Black, J., and Ducker, S. C. Love, M., Yoklavich, M., and Schroeder, D. (1971). Intertidal ecology of Port Phillip (2009). Demersal fish assemblages in the Bay with systematic list of plants and Southern California Bight based on animals. Memoirs of The National Museum visual surveys in deep water. of Victoria Melbourne 32, 93‐128. Environmental Biology of Fishes 84, 55‐68. Kloser, R. J., Williams, A., and Butler, A. (2001). doi:10.1007/s10641‐008‐9389‐8 Assessment of acoustic mapping of Maldonado, M., and Young, C. M. (1996). seabed habitats: marine biological and Bathymetric patterns of sponge resource surveys South‐East Region. distribution on the Bahamian slope. Cooperative Program, Report 2 to the Deep‐Sea Research Part I‐Oceanographic National Oceans Office. Research Papers 43, 897‐915. Land Conservation Council (1993). Marine and Marshall, D. (2002). In situ measures of coastal special investigation, Descriptive spawning synchrony and fertilization report, June 1993. success in an intertidal free spawning Larcombe, J., Brooks, K., Charalambou, C., invertebrate. Marine Ecology Progress Fenton, M., Fisher, M., Kinloch, M., and Series 236, 113‐119. Summerson, R. (2002). Marine Matters‐ Marshall, P. A., and Keough, M. J. (1994). Atlas of Marine Activities and Coastal Asymmetry in intraspecific competition Communities in Australia’s South‐East in the limpet Cellana tramoserica Marine Region. Bureau of Rural (Sowerby). Journal of Experimental Marine Sciences, Canberra. Biology and Ecology 177, 121‐138. Levin, L. A., Etter, R. J., Rex, M. A., Gooday, A. McKenzie, P., and Bellgrove, A. (2008). Dispersal J., Smith, C. R., Pineda, J., Stuart, C. T., of Hormosira banksii (phaeophycae) via Hessler, R. R., and Pawson, D. (2001). detached fragments: reproductive Environmental influences on regional viability and longevity. Journal of deep‐sea species diversity. Annual Phycology 44, 1108‐1115. Review of Ecology and Systematics 32, 51‐ McKenzie, P. F., and Bellgrove, A. (2006). No 93. outbreeding depression at a regional Lewis, J. A. (1975). The biology of Grateloupia scale for a habitat‐forming intertidal filicina (Lamouroux) C. Agardh in Port alga with limited dispersal. Marine and Phillip Bay, Victoria. BSc Thesis, Freshwater Research 57, 655‐663. University of Melbourne. doi:10.1071/mf05078 Lewis, J. A. (1983). Floristic composition and McShane, P., and Smith, M. (1986). Starfish vs periodicity of subtidal algae on an abalone in Port Philip bay. Australian artificial structure in port Phillip Bay Fisheries 148, 16‐18. (Victoria, Australia). Aquatic Botany 15, McShane, P. E. (1999). Blacklip Abalone. In 257‐274. ʹUnder Southern Seas, the ecology of

Temperate reefs literature review 45

Australiaʹs Rocky Reefsʹ. (Ed. N. OʹBrien, C. E. (1975). Standing crop, community Andrew.). (UNSW: Sydney.) composition and seasonal variations in McShane, P. E., Beinssen, K. H. H., and Foley, S. two contrasting benthic algal (1986). Abalone reefs in Victoria ‐ a communities in the Hobsons Bay area. resource atlas. Marine Science BSc Thesis, University of Melbourne. Laboratories, Queenscliff. OʹHara, T. (2000a). Chapter 3 Patterns of Menge, B. A. (2000). Top‐down and bottom‐up Temperate Marine Species Diversity at community regulation in marine rocky the Continental Scale. In ʹEnvironmental intertidal habitats. Journal of Experimental inventory of Victoriaʹs Marine Marine Biology and Ecology 250, 257‐289. Ecosystems Stage 3 (2nd Edition) ‐ Merory, M. (1997). Some influences on the Understanding Biodiversity feeding rate of the limpet Cellana Representativeness of Victoriaʹs Rocky tramoserica. Honours Thesis, University Reefsʹ. (Eds L. W. Ferns and D. Hough.). of Melbourne. (Parks, Flora and Fauna Division, Mettam, C. (1994). Intertidal zonation of animals Department of Natural Resources and and plants on rocky shores in the Bristol Environment: East Melbourne.) Channel and Severn Estuary‐the OʹHara, T. (2000b). Chapter 5 Habitats as northern shores. Biological Journal ofthe surrogates for faunal and floral Linnean Society 51, 123‐147. assemblages associated with rocky reef Middleton, J. F., and Black, K. P. (1994). The low along the Victorian coast. In frequency circulation in and around ʹEnvironmental inventory of Victoriaʹs Bass Strait: a numerical study. Marine Ecosystems Stage 3 (2nd Continental Shelf Research Edition) ‐ Understanding Biodiversity Monk, J., Ierodiaconou, D., Bellgrove, A., and Representativeness of Victoriaʹs Rocky Laurenson, L. (2008). Using Reefsʹ. (Eds L. W. Ferns and D. Hough.). Community‐Based Monitoring with GIS (Parks, Flora and Fauna Division, to Create Habitat Maps for a Marine Department of Natural Resources and Protected Area in Australia. Journal of Environment: East Melbourne.) the Marine Biological Association of the OʹHara, T. (2001). Consistency of faunal and United Kingdom 88, 865‐871. floral assemblages within temperate Moore, C. H. (2008). Defining and predicting subtidal rocky reef habitats. Marine and species‐environment relationships: Freshwater Research 52, 853‐863. understanding the spatial ecology of OʹHara, T., McShane, P. E., and Norman, M. demersal fish communities. PhD Thesis, (1999). Victoria. In ʹUnder Southern The University of Western Australia. Seas, the ecology of Australiaʹs Rocky Moore, C. H., Harvey, E. S., and Van Niel, K. P. Reefsʹ. (Ed. N. Andrew.). (UNSW: (2009). Spatial prediction of demersal Sydney.) fish distributions: enhancing our OʹHara, T. D. (2002). Benthic assemblages of understanding of species‐environment Bass Strait. Report to Geosciences relationships. ICES Journal of Marine Australia. Museum Victoria. Science 66, 2068‐2075. OʹHara, T. D., Addison, P. F. E., Gazzard, R., Nias, D. J., McKillup, S. C., and Edyvane, K. S. Costa, T. L., and Pocklington, J. B. (In (1993). Imposex in Lepsiella vinosa from Press). A rapid bioassessment Southern Australia. Marine Pollution methodology tested on intertidal rocky Bulletin 26, 380‐384. shores. Aquatic Conservation Norman, M., and Jones, G. P. (1984). OʹHara, T. D., and Poore, C. G. B. (2000). Determinants of territory size in the Patterns of distributions for southern pomacentrid reef fish, Parma victoriae. Australian marine echinoderms and Oecologia 61, 60‐69. decapods. Journal of Biogeography 27, Nowell, A. R. M., and Jumars, P. A. J. (1984). 1321‐1335. Fluid environments of aquatic benthos. Officer, R. A., Dixon, C. D., and Gorfine, H. K. Annual Review of Ecology and Systematics (2001). Movement and re‐aggregation of 15, 303‐328. the blacklip abalone, Haliotis rubra

Temperate reefs literature review 46

Leach, after fishing. Journal of Shellfish voyage SS10‐2005. Museum Victoria Research 20, 771‐779. Science Reports 11, 1‐106. Okey, T. A. (2003). Macrobenthic colonist guilds Port of Melbourne Corporation (2007a). 13 ‐ The and renegades in Monterey Canyon bay ‐ Project areas 2 and 3. Port of (USA) drift algae: Partitioning Melbourne Corporation, Melbourne. multidimensions. Ecological Monographs Port of Melbourne Corporation (2007b). 14 ‐ The 73, 415‐440. entrance ‐ Project area 4. Port of Paine, R. T. (1966). Food web complexity and Melbourne Corporation, Melbourne. species diversity. The American Naturalist Port of Melbourne Corporation (2007c). 100, 65‐75. Appendix 51 ‐ Overview Impact Paine, R. T. (1995). A conversation on refining Assessment ‐ Shallow Reef the concept of keystone species. Communities. Port of Melbourne Conservation Biology 9, 962‐964. Corporation, Melbourne. Palumbi, S. R. (1984). Tactics of acclimation: Port of Melbourne Corporation (2007d). morphological changes in sponges in an Appendix 52 ‐ Overview Impact unpredictable environment. Science 225, Assessment ‐ Deep Canyon. Port of 1478‐1480. Melbourne Corporation, Melbourne. Palumbi, S. R. (1986). How body plans limit Povey, A., and Keough, M. J. (1991). Effects of acclimation: responses of a demosponge trampling on plant and animal to wave force. Ecology 67, 208‐214. interactions on rocky shores. OIKOS 61, Parker Jr, R. O. (1990). Tagging Studies and 355‐368. Diver Observations of Fish Populations Prince, J. D. (2003). The barefoot ecologist goes on Live‐Bottom Reefs of the U.S. fishing. Fish and Fisheries 4, 359. Southeastern Coast. Bulletin of Marine Quinn, G. P. (1988). Effects of conspecific adults, Science 46, 749‐760. macroalgae and height on the shore on Parry, G. (1982). Reproductive effort in four recruitment of an intertidal limpet. species of intertidal limpets. Marine Marine Ecology Progress Series 48, 305‐ Biology 67, 267‐282. 308. Parry, G. D., and Restall, J. E. (2007). The effect Quinn, G. P., and Ryan, N. R. (1989). of Boags Rocks sewage discharge on Competitive interactions between two adjacent rocky reefs. Department of species of intertidal gastropod from Primary Industries No. 64. Victoria, Australia. Journal of Passlow, V., O’Hara, T. D., Daniell, T., Beaman, Experimental Marine Biology and Ecology R. J., and Twyford, L. M. (2006). 125, 1‐12. Sediments and benthic biota of Bass Rattray, A., Ierodiaconou, D., Laurenson, L., Strait: an approach to benthic habitat Burq, S., and Reston, M. (2009). Hydro‐ mapping. acoustic remote sensing of benthic Plummer, A., L., M., Blake, S., and Ball, D. biological communities on the shallow (2003). Marine natural values study: South East Australian continental shelf. Victorian marine national parks and Estuarine Coastal and Shelf Science 84, 237‐ sanctuaries. Parks Victoria, Melbourne. 245. Ponder, W., Hutchings, P., and Chapman, R. Rees, C. M., Brady, B. A., and Fabris, G. J. (2001). (2002). ʹOverview of the conservation of Incidence of imposex in Thais orbita from Australian marine invertebrates. A Port Phillip Bay (Victoria, Australia), report for Environment Australia.ʹ following 10 years of regulation on use Available at of TBT. Marine Pollution Bulletin 42, 873‐ http://malsocaus.org/marine_invert/cont 878. ents.html. Rennie, S., Hanson, C. E., McCauley, R. D., Poore, G. C. B., McCallum, A. W., and Taylor, J. Pattiaratchi, C., Burton, C., Bannister, J., (2008). Decapod Crustacea of the Jenner, C., and Jenner, M. N. (2009). continental margin of south‐western Physical properties and processes in the and central Western Australia: Perth Canyon, Western Australia: Links preliminary identifications of 524 to water column production and species from FRV Southern Surveyor seasonal pygmy blue whale abundance.

Temperate reefs literature review 47

Journal of Marine Systems 77, 21‐44. comparisons. Journal of Experimental doi:10.1016/j.jmarsys.2008.11.008 Marine Biology and Ecology 300, 309‐342. Roberts, D., and Davis, A. (1996). Patterns in Schiel, D. R., and Foster, M. S. (1986). The sponge assemblages on temperate structure of subtidal algal stands in coastal reefs off Sydney, Australia. temperate waters. Oceanography and Marine and Freshwater Research 47, 897‐ Marine Biology Annual Review 24, 265‐ 906. 307. Roberts, D. E. (1996). Patterns in subtidal marine Schiel, D. R., and Taylor, D. I. (1999). Effects of assemblages associated with a deep‐ trampling on a rocky intertidal algal water sewage outfall. Marine and assemblage in southern New Zealand. Freshwater Research 47, 1‐9. Journal of Experimental Marine Biology and Rollings, N., Light, B., Doblin, M., and Chiffings, Ecology 235, 213‐235. A. (1993). An evaluation of remote Schmitt, R. J., and Holbrook, S. J. (1990a). sensing and associated field techniques Contrasting effects of giant kelp on for mapping the distribution of benthic dynamics of surfperch populations. habitats in Port Phillip Bay, Oecologia 84, 419‐429. Unpublished final report, Port Phillip Schmitt, R. J., and Holbrook, S. J. (1990b). Bay Environmental Study Task G2.1. Population responses of surfperch Russell, B. C. (1983). The food and feeding habits released from competition. Ecology 71, of rocky reef fish of north‐eastern New 1653‐1665. Zealand. New Zealand Journal of Marine Seapy, R. R., and Litter, M. M. (1978). The and Freshwater Research 17, 121‐145. distribution, abundance, community Russell, B. D., and Connell, S. D. (2005). A novel structure, and primary productivity of interaction between nutrients and macroorganisms from two central grazers alters relative dominance of California rocky intertidal habitats. marine habitats. Marine Ecology Progress Pacific Science 32, 293‐314. Series 289, 5‐11. Sharpe, A. K., and Keough, M. J. (1998). An Ryan, J. P., Chavez, F. P., and Bellingham, J. G. investigation of the indirect effects of (2005). Physical–biological coupling in intertidal shellfish collection. Journal of Monterey Bay, California: topographic Experimental Marine Biology and Ecology influences on phytoplankton ecology. 223, 19‐38. Marine Ecology Progress Series 287, 23‐32. Shears, N. T., and Babcock, R. C. (2002). Marine Sanchez‐Jerez, P., Gillanders, B. M., Rodriguez‐ reserves demonstrate top‐down control Ruiz, S., and Ramos‐Espla, A. A. (2002). of community structure on temperate Effect of an artificial reef in Posidonia reefs. Oecologia 132, 131‐142. meadows on fish assemblage and diet of Shepherd, S. A., and Clarkson, P. S. (2001). Diet, Diplodus annularis. ICES Journal of Marine feeding behaviour, activity and Science 59, S59‐S68. predation of the temperate blue‐ doi:10.1006/jmsc.2002.1213 throated wrasse, Notolabrus tetricus. Sanchez, F., Serrano, A., and Ballesteros, M. G. Marine and Freshwater Research 52, 311‐ (2009). Photogrammetric quantitative 322. study of habitat and benthic Sorokin, S. J., Laperousaz, T. C. D., and Collings, communities of deep Cantabrian Sea G. J. (2008). Investigator group hard grounds. Continental Shelf Research expedition 2006: sponges (Porifera). 29, 1174‐1188. Transactions of the Royal Society of South doi:10.1016/j.csr.2009.01.004 Australia 132, 163‐172. Sanderson, J. C. (1997). Subtidal Macroalgal Sousa, W. P. (1979). Disturbance in marine Assemblages in Temperate Australian intertidal boulder fields: The Coastal Waters, Australia. Department nonequilibrium maintenance of species of the Environment, Canberra. diversity. Ecology 60, 1225‐1239. Schiel, D. R. (2004). The structure and Spence, S. K., Bryan, G. W., Gibbs, P. E., Masters, replenishment of rocky shore intertidal D., Morris, L., and Hawkins, S. J. (1990). communities and biogeographic Effects of TBT Contamination on

Temperate reefs literature review 48

Nucella Populations. Functional Ecology management. Ocean and Coastal 4, 425‐432. Management 20, 41‐62. Spencer, R. D. (1970). An ecological study of the Underwood, A. J., and Chapman, M. G. (1995). subtidal macrophytic vegetation of three Rocky Shores. In ʹCoastal Marine selected areas of Port Phillip Bay: Ecology of temperate Australiaʹ. (Eds A. Werribee, Altona and Carrum. MSc J. Underwood and M. G. Chapman.). Thesis, University of Melbourne. (UNSW Press: Sydney.) Spencer, R. D. (1972). Algal pollution and Underwood, A. J., and Chapman, M. G. (2007). marine fouling in Port Phillip Bay. PhD Intertidal temperate rocky shores. In Thesis, University of Melbourne. ʹMarine Ecologyʹ. (Eds S. D. Connell and Stephenson, T. A., and Stephenson, A. (1972). B. M. Gillanders.) pp. 402‐427. (Oxford ʹLife between tidemarks on rocky University Press: Oxford.) shores.ʹ (W. H. Freeman: San Francisco.) Underwood, A. J., and Jernakoff, P. (1981). Stewart, K., Judd, A., and Edmunds, M. (2007). Effects of interactions between algae Victorian intertidal reef monitoring and grazing gastropods on the structure program: The intertidal reef biota of of a low shore intertidal algal Victoriaʹs Marine Protected Areas. Parks community. Oecologia 48, 221‐233. Victoria, Melbourne. Underwood, A. J., and Kennelly, S. J. (1990). Suchanek, T. H., Carpenter, R. C., Witman, J. D., Ecology of marine‐algae on rocky shores and Harvell, C. D. (1983). Sponges as and subtidal reefs in temperate important space competitors in deep Australia. Hydrobiologia 192, 3‐20. Caribbean coral reef communities. In Underwood, A. J., and Keough, M. J. (2001). ʹThe ecology of deep and shallow coral Supply side ecology: the nature and reefsʹ. (Ed. M. L. Reaka.) pp. 55‐60: consequences of variations in the Washington, D.C.) recruitment of intertidal organisms. In The University of Queensland (2001). ʹTypes of ʹMarine Community Ecologyʹ. (Eds M. reefs.ʹ Available at D. Bertness, S. D. Gaines and M. Hay.) http://www.reef.edu.au/asp_pages/secc. pp. 183‐200. (Sinauer Associates: asp?formno=2. Massachusetts, USA.) Thomas, F. I. M., and Atkinson, M. J. (1997). Underwood, A. J., Kingsford, M. J., and Andrew, Ammonia uptake by coral reefs: effects N. L. (1991). Patterns in shallow subtidal of water velocity and surface roughness marine assemblages along the coast of on mass transfer. Limnology and New South Wales. Australian Journal of Oceanography 42, 81‐88. Ecology 6, 231‐249. Thompson, R., Roberts, M., Norton, T., and Vanderklift, M. A., and Wernberg, T. (2008). Hawkins, S. (2000). Feast or famine for Detached kelps from distant sources are intertidal grazing molluscs: a mis‐match a food subsidy for sea urchins. Oecologia between seasonal varitations in grazing 157, 327‐335. doi:10.1007/s00442‐008‐ intensity and the abundance of 1061‐7 microbial resources. Hydrobiologia 484, Verges, A., Alcoverro, T., and Ballesteros, E. 167‐175. (2009). Role of fish herbivory in Tissot, B. N., Yoklavich, M. M., Love, M. S., structuring the vertical distribution of York, K., and Amend, M. (2006). Benthic canopy algae Cystoseira spp. in the invertebrates that form habitat on deep Mediterranean Sea. Marine Ecology‐ banks off southern California, with Progress Series 375, 1‐11. special reference to deep sea coral. doi:10.3354/meps07778 Fishery Bulletin 104, 167‐181. Wahl, M. e. (2009). ʹMarine hard bottom Underwood, A. (1984). Vertical and seasonal communities: patterns, dynamics, patterns in competition for microalgae diversity, and change.ʹ (Springer: between intertidal gastropods. Oecologia Heidelberg, Germany.) 64, 211‐222. Waters, J. M., Wernberg, T., Connell, S. D., Underwood, A. J. (1993). Exploitation of species Thomsen, M. S., Zuccarello, G. C., Kraft, on the rocky coast of New South Wales G. T., Sanderson, C., West, J. A., and (Australia) and options for its Gurgel, C. F. D. (In Press). Australia’s

Temperate reefs literature review 49

marine biogeography revisited: back to homogeneity for classifying abiotic the future? Austral Ecology surrogates of biodiversity, ICES Journal Waters, J. M. K., T.M.; OʹLoughlin, M.; Spencer, of Marine Science, 66: 214‐224ʺ by Peter H.G. (2005). Phylogeographical T. Harris, Andrew D. Heap, Tara J. disjunction in abundant high dispersal Anderson, and Brendan Brooke. 66, littoral gastropods. Molecular Ecology 14, 2086‐2088. 2789‐2802. Williams, A., Bax, N. J., Kloser, R. J., Althaus, F., Watson, J. E. (1982). Hydroids (Class Hydrozoa). Barker, B., and G., K. (2009b). Australia’s In ʹMarine invertebrates of southern deep‐water reserve network: Australia. Part I. Handbook of the flora implications of false homogeneity for and fauna of South Australiaʹ. (Eds S. A. classifying abiotic surrogates of Shepherd and F. I. M. Thomas.). biodiversity. ICES Journal of Marine (Government Printer: South Australia.) Science 66, 214‐224. Webb, R. O., and Kingsford, M. J. (1992). Williams, A., and Kloser, R. J. (2004). Voyage Protogynous hermaphroditism in the plan, RV Southern Surveyor, SS04/2004. half‐banded sea perch, Hypoplectrodes CSIRO Marine Research, Hobart. maccullochi (Serranidae). Journal of Fish Womersley, H. B. S. (1966). Port Phillip survey Biology 40, 951‐961. 1957‐1963. Algae. Memoirs of The Wheatley, M. J. (2000). Ecology of populations National Museum of Victoria Melbourne and assemblages of temperate reef fish 27, 133‐156. in Port Phillip Bay, Australia. PhD Womersley, H. B. S. (1984). ʹThe marine benthic Thesis, Monash University. flora of southern Australia. Part 1.ʹ Williams, A., Althaus, F., Barker, B., Kloser, R., (Government Printer: South Australia.) and Keith, G. (2007). Using data from Womersley, H. B. S., and King, R. J. (1990). the Zeehan candidate MPA to provide Ecology of Temperate Rocky Shores. In an inventory of benthic habitats and ʹBiology of Marine Plantsʹ. (Eds M. N. biodiversity, and evaluate prospective Clayton and R. J. King.) pp. 267‐295. indicators for monitoring and (Longmire Cheshire: Melbourne.) performance assessment. Final Report to Wright, J. (1989). An investigation of the Department of Environment and competition between Cellana tramoserica Water Resources. (Sowerby) and Patiriella exigua (Lamark). Williams, A., and Bax, N. J. (2001). Delineating Honours Thesis, University of fish–habitat associations for spatially Melbourne. based management: an example from Yoklavich, M. M., Greene, H. G., Cailliet, G. M., the south‐eastern Australian continental Sullivan, D. E., Lea, R. N., and Love, M. shelf. Marine and Freshwater Research 52, S. (2000). Habitat associations of deep‐ 513‐536. water rockfishes in a submarine canyon: Williams, A., Bax, N. J., and Kloser, R. J. (2009a). an example of a natural refuge. Fishery Remarks on ʺComment on: Williams et Bulletin 98, 625‐641. al. (2009) Australiaʹs deep‐water reserve network: implications of false

Temperate reefs literature review 50

Appendix 1 Tables

Table 1. Six bioregions relevant to Victoria as presented in Interim Marine Coastal Regionalisation of Australia Technical Group, IMCRA (2006)

• Otway Location: Cape Jaffa to slightly north of Apollo Bay and including King Island Very steep to moderate offshore gradients. High wave energy. Currents generally slow, but moderately strong through entrance to Bass Strait. Cold temperate waters subject to nutrient rich upwellings. • Central Victoria Location: Cape Otway to west of Wilsons Promontory to Flinders Is. Very steep to steep offshore gradients dominated by cliffed shorelines. Sea‐surface temperature is representative of Bass Strait waters. Moderate wave energy. • Flinders Location: Eastern Entrance to Bass Strait and including Wilsons Promontory, Rapid changes in offshore gradient. Granitic coastline exposed to submaximal swells on east‐facing shores of Flinders Island and moderate to low swells elsewhere. Sandy beaches of moderate length with seagrass beds prevalent in shallow water. High tidal range » 3 m and strong tidal currents. Sea‐surface temperature is representative of Bass Strait waters. Waves highly variable. • Twofold Shelf Location: East of Wilsons Promontory and north to Tathra (36°48’S), Submaximally exposed coastline with long sandy beaches broken by rocky headlands and numerous coastal lagoons. Moderate tidal range ~ 2 m. Mean annual sea‐surface temperature reflects the influence of warmer waters brought into Bass Strait by the East Australian Current. Variable wave energy. • Victorian Embayments Location: Victorian bays, inlets and estuaries e.g., Port Phillip Bay

Confined bodies of water that total in excess of 3000 km2 and individually vary in size from 1950 km2 to less than 1 km2. They are generally basin‐shaped, less than 25 m deep, have limited fetch and are dominated by depositional environments. • Central Bass Strait Location: Central offshore region of Bass Strait

The region is about 60,000 km2 in size and lies in the central area of Bass Strait. The sea floor is shaped like an irregular saucer with water depth varying from about 80 m at its centre to 50 m around the margins. The substrate of central area is mainly mud. Tidal velocities vary from <0.05 ms–1 in the central area to as high as 0.5 ms–1 at the margins where the islands and promontories form the western and eastern entrances to Bass Strait. Water mass characteristics are complex and vary seasonally representing the mixing of the different water masses present on western and eastern side of the Strait.

Temperate reefs literature review 51

Table 2. Interim intertidal marine habitat (MHC) categories for Victoria, Ferns et al. (2000).

Table 3. Interim shallow subtidal (0 – 2.5 m) marine habitat (MHC) categories for Victoria, Ferns et al. (2000).

Temperate reefs literature review 52

Table 4. Primary shallow habitat classification scheme as presented in Ball et al. (2000).

Temperate reefs literature review 53

Table 5. Potential physical drivers responsible for shaping deep reef assemblages in Victoria. Summarised from Edmunds et al. (2006b)

o Sedimentation ƒ Sediments may naturally settle and cover rock ƒ Strong wave action and currents may expose rocky reefs and keep them free of sediments ƒ With increasing depth, wave action decreases and sedimentation may increase ƒ Sediment transport from adjacent habitats may be such that reefs are heavily sediment effected even in the presence of strong currents ƒ Reef steepness and relief can influence sediment build‐up, i.e., more vertical surfaces are less likely to accumulate sediment o Geological structure ƒ The type of rock and geological history can influence the size and structure of reefs ƒ Surface roughness can effect settlement, increase surface area and influence water movement over the rock surface and therefore the transport of food, oxygen, nutrients etc (Thomas and Atkinson 1997) ƒ Reef structure may influence how sediments and loose rocks smother or scour reef surface and sessile organisms o Water movement, including waves and currents ƒ May erode reefs ƒ Can impact sediment deposition and transport ƒ Influence the type and distribution of organisms on the reef o Light climate ƒ High levels of sedimentation and increasing depth can influence light levels ƒ Reef aspect and shading at a variety of scales influence light availability ƒ Where light levels are sufficient, algae out compete sessile invertebrates on rocky reefs, e.g., sponges and corals o Depth ƒ Interacts with factors listed above ƒ Deep reefs tend to be dominated by sessile invertebrate assemblages, e.g., sponge gardens

Temperate reefs literature review 54

Table 6. Potential ecological drivers responsible for shaping deep reef assemblages in Victoria. Summarised from Edmunds et al. (2006b) • Sessile invertebrates spend their adult life attached to the substratum o Species such as sponges, may exhibit different physical characteristics depending on environmental conditions o Sponges require suitable seabed for them to attach and resist the actions of currents and waves and are often found in underwater tunnels and notches that are surrounded by kelps (Keough 1999) o Sponges, cnidarians, bryozoans, and colonial ascidians dominate deep reef assemblages o The age of individuals and colonies on deep reefs in Victoria cannot be assumed to be correlated with size o There may be complex interactions which will not be known without study of the basic ecology of species, o Sessile clonal species such as sponges often release actively swimming larvae which travel relatively short distances before recruitment, even in high currents , while some species produce crawling larvae o Larvae can react to a range of stimuli such as light levels and gravity (Keough et al. 1996) • Food availability effects the distribution of species, and while mobile invertebrates and fish can move to areas where food is available, sessile species are predominantly suspension feeders that require food in the form of plankton that is available in the water column. • Little is known about the small crustaceans, molluscs etc that are associated with sessile communities on Victoria’s deep rocky reefs. o Therefore their role in shaping assemblage structure is not understood. • Little is known about the behaviour and diet of predatory fish on Victoria’s deep reefs, or their impact on assemblage structure

Temperate reefs literature review 55

Appendix 2 Conceptual Models

Temperate reefs literature review 56

Temperate

reefs

literature

review

57 Figure 1. Key relationships and drivers on intertidal reefs in Victoria

58 Temperate

reefs

literature

review

Figure 2. Key relationships and drivers on subtidal reefs in Victoria

Temperate

reefs

literature

review

59 Figure 3. Key relationships between invertebrates on subtidal reefs in eastern and western Victoria

60 Temperate

reefs

literature

review

Figure 4. Key relationships and drivers on deep reefs in Victoria

Temperate

reefs

literature

review 61 Figure 5. Key relationships and drivers on canyon reefs in Victoria