Nudibranchs of the Central Western Australian Coast
Justine M. Arnold
This thesis is presented as part of the requirements for the Degree of Bachelor of Science
in Marine Science with Honours at Murdoch University.
October 2014
DECLARATION
I declare that the work presented here is my own research conducted from March to
October 2014, and has not been submitted for the award of any other degree at another
tertiary institution.
Justine Arnold
October 2014
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ABSTRACT
Nudibranchs are a diverse group of gastropod molluscs that are distributed around the world found inhabiting coral reef ecosystems. Baseline data on nudibranchs is lacking in the mid west region of Western Australia. Four sub-regions across the Midwest;
Geraldton and the three groups at the Abrolhos Islands, the Easter Group, the Wallabi
Group and the Pelsaert Group were the focus of nudibranch diversity surveys. Collection of quantitative information to establish a biogeographical baseline for the nudibranchs of this region was one of the main aims of this study.
In total 89 dives were made over the duration of this study, with an average dive time of
30 minutes. A total of 296 individual nudibranchs were observed. The most abundant family found was Chromodorididae and Chromodoris westraliensis was the dominant species. Equal numbers of nudibranchs were found at shallow and deep sites, with depth found to not have a significant difference on nudibranch abundance or species abundance. Sub-region was suggested to be the predominant influence in nudibranch abundance and species richness. The probable cause for this is the influence from the
Leeuwin Current and its effects on the habitat composition. The Leeuwin Current is believed to strongly influence recruitment of planktonic larvae along the Western
Australian coast. Suggesting that larval recruitment of all marine species including nudibranchs, nudibranch prey items and benthic flora nudibranchs inhabit is influenced by the Leeuwin Current.
Investigations into key nudibranch prey items and their seasonal occurrence may help in predicting abundance of sub-annual nudibranch species in an area. Benthic habitat differences and nudibranch prey items could be distributed at different rate over each sub- region due to local hydrology effects from the Leeuwin Current. Geraldton was found to be clearly different to the three Abrolhos Island groups, with sub-region being a determining factor for abundance and species abundance. Greater sampling effort into
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destructive day-time and night-time sampling is also predicted to increase the number of species and abundance of nudibranchs found in the Midwest region.
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ACKNOWLEDGEMENTS
There are several people that deserve honorable mention for their assistance throughout the duration of this study.
I was lucky enough to be the recipient of the Calver Family Scholarship for 2014. Thank you for allowing me to be the recipient of such a highly regarded award. With the assistance of the scholarship I was able to expand my research to areas that at first seemed impossible.
I would like to thank my parents, Charlie and Lorraine Arnold, without their love, support and encouragement I would not have been able to make it through the past 5 years at university, especially this last year where they have bent over backwards and became fully involved in my honours research. It was such an honor to spend so much time with such giving people. Thank you.
I would like to extend my gratitude to my volunteer dive buddies for donating their precious time to my research, Peter Howie, Rowan Kleindienst, Claire Cocking, Brenda
Arnold and Ellen Boylen, Thank you.
Thank you to Laura Bradshaw for always knowing the right thing to say and for last minute technical assistance.
And to my supervisor Mike Van Keulen, Thank you; for taking me on-board, your endless wealth of knowledge and advice and for allowing me the opportunity to apply the numerous skills I have learnt in my undergraduate degree in this project.
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TABLE OF CONTENTS
DECLARATION ...... i ABSTRACT ...... ii ACKNOWLEDGEMENTS ...... iv TABLE OF CONTENTS ...... v 1.0 INTRODUCTION ...... 1 1.1 Nudibranchs ...... 2 1.1.1 Family Characteristics ...... 2 1.1.2 Distribution ...... 2 1.1.3 Habitat and Feeding ...... 3 1.1.4 Life History ...... 4 1.1.5 The Leeuwin Current ...... 5 1.2 Climate Change ...... 7 1.2.1 Known Climate Change Impacts ...... 8 1.2.2 Postulated Climate Change Impacts ...... 9 1.3 Worldwide Nudibranch Diversity ...... 9 1.4 Western Australian Nudibranch Diversity ...... 11 1.5 Aims of This Study ...... 12 2.0 METHODS...... 14 2.1 Area Description ...... 14 2.2 Environmental Description ...... 16 2.2.1 Wind ...... 16 2.2.2 Swell ...... 16 2.2.3 Current ...... 17 2.2.4 Water Temperatures ...... 17 2.2.5 Salinity ...... 18 2.3 Habitat Description ...... 18 2.4 Site Selection ...... 18 2.5 Survey Methods ...... 19 2.6 Species Identification ...... 20 2.7 Statistical Analysis ...... 21 2.7.1 Species and Abundance ...... 21
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2.7.2 Species Diversity and Evenness ...... 22 2.7.3 Connectivity ...... 23 3.0 RESULTS ...... 24 3.1 Species and Abundance ...... 24 3.2 Family Level Analyses ...... 27 3.3 Total Abundance Analyses ...... 29 3.4 Total Species Analyses ...... 30 3.5 Interactions ...... 32 3.6 Species Diversity and Evenness Indices ...... 33 3.7 Connectivity ...... 35 3.8 Substrate Preference and Activity ...... 38 4.0 DISCUSSION ...... 40 4.1 Estimating and Comparing Diversity ...... 40 4.2 Family Level Analysis ...... 42 4.3 Total Species and Abundance ...... 44 4.4 Species Diversity and Evenness ...... 47 4.5 Distribution ...... 49 4.6 Substrate Preference and Activity ...... 50 4.7 General Discussion ...... 50 5.0 CONCLUSION ...... 52 5.1. Future Implications ...... 53 6.0 REFERENCE LIST ...... 54 7.0 APPENDIX ...... 65 Appendice 1: ...... 65 Appendice 2: ...... 67
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1.0 INTRODUCTION
Members of the sub-class Opisthobranchia are defined as mollusc gastropods that have, over the course of evolution reduced their external shells, or have no shell (Martin et al.
2006). There are seven orders in the Opisthobranchia, one of these being Nudibranchia.
Individuals from Nudibranchia are defined as shell-less marine gastropods, commonly referred to as sea-slugs (Hoover et al., 2012; Cheney et al., 2014). They have been recorded in a wide range of habitats, from intertidal reef platforms in the tropics to temperate areas in the deep sea (Chavanich et al., 2013). Due to nudibranchs being cryptic, highly camouflaged, and therefore relatively hard to find, it has been difficult to assess their diversity, species richness and abundance (Domenech et al. 2002;
Chavanich et al. 2013).
The local hydrology of a region and its impacts on nudibranch larval distribution are not well known. Like all benthic marine invertebrates, nudibranchs have a planktonic larval stage in their life cycle (Pechenik 1999; Todd et al. 1998). Attempts have been made to identify trace elements in larvae carbonate structures, once they have settled, in an effort to assess where larvae originated (Levin, 2006). This technique requires larvae to retain the larval structure when settling out of the plankton, with gastropods required to retain statoliths and prodissoconch (larval shell) (Levin, 2006). The majority of nudibranchs, lose their shell on settling out of the plankton so it is near impossible to use this method (Levin,
2006).
Nudibranchs can be separated into three groups based on life cycles; sub-annual, annual and biannual. Sub-annual nudibranchs are ephemeral species that undergo several generations in one year (Todd, 1981). Annual species are nudibranchs that undergo a single generation in one year; and biannual species have a post-larvae life of up to two years in which they spawn once and then die (Todd, 1981). The distribution of short-lived nudibranch species, with sub-annual life cycles, has been found to be strongly dependent
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on seasonal peaks of temperature and dietary resources available in an area.
Nudibranchs that are long-lived, with annual or biannual life cycles, have food available year round, leading to the assumption that they are not limited by food resources (Aerts,
1994). This suggests that the distribution of long-lived nudibranchs is dependent on abiotic and other biotic factors. Larval supply is thought to be the key to determining adult population dynamics of marine organisms (Levin, 2006). Marine protected areas (MPAs) have provided a means of assessing ecosystem function, larval dispersal, connectivity and resilience in a number of marine ecosystems (Babcock et al., 1999; Levin, 2006).
Understanding the dispersal mechanisms of organisms assists scientists in placement of
MPAs (Levin, 2006).
1.1 Nudibranchs
1.1.1 Family Characteristics
There are over 120 different families of nudibranchs, with new species being either sighted or described monthly (“World Register of Marine Species,” 2014). Each family is defined by unique characteristics relating to defence mechanisms, methods of dispersal, life history stages, food specialisation, habitat preference, regionality and colouration. For example, nudibranchs from the Suborder Aeolidacea have developed a defence mechanism that is derived from the food they eat. After feeding on cnidarians aeolid nudibranchs accumulate the ingested nematocysts into their own tissues for defence as they lack the protective shells of other gastropods (Fogg-Matarese, 2009; Hoover et al.,
2012).
1.1.2 Distribution
Nudibranchs are important components of rocky intertidal and sub-tidal communities
(Todd, 1981). Biotic and abiotic factors both play a role in the dispersal and distribution of nudibranch species. The majority of nudibranchs are benthic invertebrates relying on
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abiotic conditions in their environment for geographic dispersal (Garcia and Bertsch,
2009). Biotic factors that influence nudibranchs include but are not limited to: presence of settlement hosts, chemical cues from prey items and abundance of food; abiotic factors that influence nudibranchs include temperature and current (McCuller, 2012).
Nudibranchs are found in marine habitats all around the world and are generally well represented from equatorial to polar regions (Garcia and Bertsch, 2009). Biological diversity tends to increase from polar to tropical regions, a typical characteristic of marine organisms (Garcia and Bertsch, 2009)
1.1.3 Habitat and Feeding
Nudibranchs have been principally found in habitats consisting of loose rocks and coral rubble, shoreward of fringing reefs (Kay and Young, 1969). Generally nudibranchs exist in habitats where there are ample prey items (Lambert, 1991). Nudibranchs feed on a range of marine organisms including ascidians, sponges, bryozoans, tunicates, corals, hydroids or sea anemones (Todd, 1981; Martin et al., 2006). Studies of feeding behavior exhibited by nudibranchs have revealed that segregation does occur when more than one species is found in the same area. Lambert (1991a) showed that food availability was the main cause for segregation between species; the spread of food in an area was the determining factor as to where the different species of nudibranch could be found.
Stability of nudibranch populations has been linked to the stability of prey organisms. Prey types such as soft corals and sponges have been determined to be available more consistently over the year compared to bryozoans and hydroids that are seasonally variable. Nudibranchs with sub-annual life cycles are more likely to feed on seasonally variable prey items, with annual and biannual species of nudibranch more likely to feed on temporally stable, encrusting prey organisms (Todd, 1981). Aeolid nudibranchs, including
Hermissenda crassicornis (Hoover et al., 2012), Cratena pilata (Fogg-Matarese, 2009) and Cratena peregrine (Aguado and Marin, 2007) are known to be associated with
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cnidarians (such as scyphozoan polyps) and have developed a chemical in their mucus that inhibits the discharge of the stinging nematocysts, incorporating these cells into their own tissues as a defense mechanism (Fahey and Garson, 2002; Martin et al., 2006;
Aguado and Marin, 2007; Hoover et al., 2012).Hoover et al. (2012) suggested that nudibranch species that consume cnidarians, polyps and hydroid species have the potential to control jellyfish blooms, though further studies are necessary.
1.1.4 Life History
The three main ecological life cycle groupings of nudibranchs; sub-annual, annual and biannual, were identified by (Todd, 1981). Sub-annual species are generally small, cryptically coloured and characterised by unstable populations that fluctuate in abundance over short periods of time (Todd, 1981). Morphology and temporal stability of nudibranch life cycles has been linked to the stability of prey organisms of each species. Annual species complete only a single generation over the period of one year, often exhibiting striking colourations compared to the substrate they are found on. A large majority of nudibranchs fall into the annual life cycle category and tend to feed on stable encrusting prey types such as corals, bryozoans and hydroids. Nudibranchs with an annual lifecycle usually survive three to four months post-spawning before mortality occurs (Todd, 1981).
The prey of biennial nudibranch species largely consists of, but is not limited to, stable colonial organisms such as octocorals and sponges (Todd, 1981; García-Matucheski and
Muniain, 2011). Access to stable food sources year round is thought to be linked to extended life periods and larger sizes of individual species.
A wide range of larval forms exist within the Nudibranchia, ranging from direct development to short or long term plankton; namely planktotrophic or lecithotrophic development (Todd, 1981; Hadfield, 1987). Larvae with direct development have eliminated the need for free-living larval forms compared to planktotrophic larvae that have an extended pelagic feeding phase lasting for several weeks (Todd, 1981).
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Lecithotrophic larvae are only in the pelagic phase for a few hours to days and do not feed (Todd, 1981). Thompson (1958) discovered that larvae of the nudibranch, Adalaria proxima metamorphose only in the presence of living bryozoans of the species Electra pilosa, when the larvae can ‘smell’ the live bryozoans even though adults of this species have been recorded feeding on at least three other species of bryozoans. Metamorphose of larvae occurs during the substrate searching phase, with larvae being able to search for up to two weeks for suitable substrate to settle upon (Thompson, 1958). General flattening of the body, casting of shell, casting of operculum and the inversion and spread of the mantle fold are main external changes that occur during metamorphosis. As with many other marine planktonic larvae, nudibranchs respond to a number of chemical and physical cues from their prey items to metamorphose, settle and complete their life cycle.
Studies have shown that nudibranch larvae post hatching have an upwards swimming stage that is quite rapid, occurring regardless of the light source (Hadfield, 1987).
Investigations into the effect this has on distribution of larvae via currents in an area have yet to be carried out. In the majority of nudibranch species, one mating provides enough sperm for several spawnings (Hadfield, 1987). Individuals that are isolated after mating may continue to lay eggs, though fertilisation may not occur for up to 3-4 egg masses
(Hadfield, 1987).
1.1.5 The Leeuwin Current
The Western Australian marine environment is diverse and unique, with the world’s only southern flowing eastern boundary current, the Leeuwin Current. The Leeuwin Current is responsible for the majority of larval dispersal and planktonic movement along the west
Australian coastline (Hutchins and Pearce, 1994; Waite et al., 2007). The Leeuwin
Current extends from the Northwest Shelf and continues along the continental shelf around Cape Leeuwin, and eastward across the Great Australian Bight (Figure 1.1.5)
(Cresswell 1991; 1996). This current supplies the high latitudes of western and southern
Australia with warm water. In contrast, other eastern boundary currents in the southern
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hemisphere (such as the Humboldt Current and the Benguela Current) carry cool, nutrient rich waters northwards (Morgan and Wells, 1991; Pearce, 1991; Caputi et al., 1996). The warm waters of the Leeuwin Current allow tropical species of marine life to venture and settle further south and survive in temperate waters (Pearce et al. 2011). Eddies and gyres, varying in size from 10 km to 100 km wide, bud off from the Leeuwin Current and have been found to enhance planktonic biota abundance and diversity in regions where eddies are formed (Feng et al., 2010; Holliday et al., 2012) .
The Abrolhos Islands, located on the edge of the continental shelf, lie directly in the path of the Leeuwin Current. It is believed that large eddies have a major influence on the flora and fauna inhabiting this region (Phillips and Huisman, 2009). Geraldton is inshore, not on the edge of the continental shelf, and therefore the Leeuwin Current does not have a direct impact in this area (Wells and Bryce, 1993). During the winter months the Leeuwin
Current tends to flow closer to the coastline and in the summer months the flow moves offshore, onto the edge of the continental shelf (Feng et al., 2009). The Capes Current, an equator-ward current is the dominant current inshore along the Western Australian coastline during these summer months (Gersbach et al. 1999; Pearce and Pattiaratchi
1999; Pattiaratchi and Woo 2009). The Capes Current is a cool, higher salinity, seasonal, wind driven flow of relatively nutrient rich water originating in the Cape Leeuwin region extending to the Abrolhos Islands (Gersbach et al., 1999; Pattiaratchi and Woo, 2009). It is believed that the Capes Current, like the Leeuwin Current has a significant influence on seasonal migration and spawning patterns of numerous fish species (Gersbach et al.,
1999).
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Figure 1.1.5: The surface currents off southwestern Australia. The Leeuwin Current flows year round, being the strongest in winter and is marked by the broad grey arrow. The Capes Current is marked by the long black arrow along the continental shelf and is driven by summer southerly winds. There are two eddies that have separated from the Leeuwin Current. The Abrolhos Islands are located within the path of the Leeuwin Current, compared to Geraldton which receives waters from the Capes Current. Adapted from Cresswell and Domingues (2009)
1.2 Climate Change
Ocean acidification and global warming are altering the marine environment, with sea surface temperatures slowly increasing and estimated to reach between 1°C and 4°C higher than the current maximum by the end of the century (IPCC, 2007). With climate change effects forecast to drive organisms towards the polar regions, away from the equator (Perry et al., 2005). Strong evidence of this has already been documented, with
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the sea urchin Centrostephanus rodgersii expanding its natural range pole-ward from
New South Wales to Tasmania (Johnson et al., 2011). Marine ecosystems and the physical environment of Western Australia are considered to be sensitive environments, susceptible to climate variability (Feng et al., 2009). Regional projections show the
Leeuwin Current will experience low to medium effects from climate change, with experts now suggesting focus be turned to conservation responses to increase resilience of marine ecosystems (Feng et al., 2009).
1.2.1 Known Climate Change Impacts
The effects of climate change are visible today, with climate driven phenomena resulting in large changes in marine ecosystems. Chavez (2012) discussed dramatic shifts in fish abundance along the coast of Peru, which can be linked to an event involving the polar ice caps. The ice caps expanded causing the InterTropical Convergence Zone (ITCZ)
(sometimes referred to as the meteorological equator) to shift southwards. This halted the main driver of nutrients in the Pacific Ocean, (the Walker Circulation) causing the now abundant fish populations to be barely evident. When the conditions in the Pacific Ocean became warmer again, the wealth of fish populations returned. Research has shown the
East Australian Current has extended its range southwards along the eastern coast of
Australia with effects of the current now seen in Tasmania. Johnson et al. (2011) discussed how a better understanding of climate change effects between individual taxa and interactions between species is critical for managing future climate change projections.
A warm water event occurred along the west Australian coast in the austral summer of
2010/2011 (Pearce and Feng, 2013; Caputi et al., 2014). This event was associated with one of the strongest La Nina events on record, with temperatures of the Leeuwin Current reaching 5°C higher than equivalent latitudes of other southern hemisphere eastern boundary currents (Feng et al., 2013; Pearce and Feng, 2013). Benthic invertebrates that
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were affected by this heat wave included abalone (Haliotis roei), with a complete mortality of stocks north of the Murchison River (Kalbarri), and lobster (Panulirus cygnus) mortalities at the Abrolhos Islands.
1.2.2 Postulated Climate Change Impacts
Species of marine invertebrates endemic to an area are under the greatest threat from climate change (Hughes, 2003). O’Hara (2002) suggests that a portion of species that are endemic to a region may become locally extinct with temperature increases. O’Hara’s study focused on marine invertebrates and their distribution along the Victorian coastline predicting extinctions of echinoderms, gastropods and decapods with 1-2 °C rises in seawater temperatures.
Researchers are predicting jellyfish will take-over our marine environments in the future.
Effects from climate change enable jellyfish to grow faster, increasing population size whilst jellyfish predators are being overfished, leaving the populations to flourish
(Richardson et al., 2009).
1.3 Worldwide Nudibranch Diversity
Limited studies have been conducted on nudibranchs, making them relatively mysterious organisms. Although comprehensive studies have examined the chemical aspects of nudibranchs and their ecology, there is limited literature on depth associations of different nudibranch families, species abundance in specific regions, factors that affect distribution and abundance, or habitat and food preferences. Worldwide studies on nudibranchs are equally limited, although Bennett (2013) compiled a list of opisthobranch species identified in different regions around the world (Table 1.3).
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Table 1.3: Total number of opisthobranchs found at various locations around the world, in both northern and southern hemispheres (Bennett, 2013).
Total Sampling Average No. Locality Period Latitude Species
Eastern Arctic Unknown 71°N 5
Great Britain Unknown 53°N 133
Western Arctic Unknown 51°N 37
California 40 years 34°N 212
Caribbean 25 years 22°N 329
Hawaii Unknown 20°N 430
Guam Several years 13°N 474
Philippines Unknown 12°N 563
Panama Unknown 10°N 218
Tanzania Unknown 7°S 258
Papua New Guinea >6 years 10°S 646 Northern Great Barrier Reef (Aust.) 5 years 14°S 158
Madagascar Unknown 20°S 168 Southern Great Barrier Reef (Aust.) 32 years 23°S 261
Sunshine Coast (Aust.) 8 years 26°S 501 Victoria (Aust.) 52 years 39°S 336
Temp (South Africa) Unknown - 124 New Zealand 50 years 41°S 162
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1.4 Western Australian Nudibranch Diversity
There is a gap in the knowledge of opisthobranchs, including nudibranchs, not only in
Western Australia but Australia wide (Table 1.4). Studies which have been completed on nudibranchs in Australia include assessment of rarity in Queensland (Benkendorff and
Przeslawski, 2008), chemical associations by (Garson and Chem, 2004) and (Yong,
Salim, and Garson, 2008). Bennett (2013) focused on the diversity, distribution, abundance and feeding ecology of opisthobranchs at Coral Bay, Ningaloo Reef, Western
Australia and compiled diversity estimates from localities in Western Australia and their relative survey duration (Table 1.4). It was noted that the survey duration for studies carried out before the year 2000 were not specifically opisthobranch targeted surveys.
These studies were carried out by the Western Australian Museum and focused on collecting all molluscan species, not specifically nudibranchs. The Western Australian
Museum is currently in the process of collecting samples of opisthobranchs from the
Kimberley region, Rowley Shoals and the Abrolhos Islands to ascertain accurate species identifications, taxonomic information and genomics of species. The results from this study will not be available in time to be included in this paper (pers. comm. Nerida Wilson,
2014). An Honours project is currently in progress focusing on the south west of Western
Australia looking at the abundance and diversity of nudibranch species at the Busselton
Jetty; the results from this study are not available for inclusion in this paper. The Midwest of Western Australia is lacking in published literature on nudibranchs; their behaviors, abundance, species richness, depth associations and benthic habitats with which they are associated.
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Table 1.4: Comparison of diversity estimates of opisthobranchs for surveys this survey and surveys undertaken in similar localities. Adapted from Bennett (2013)
Location Year Survey Duration No. Species Surveyed
Dampier 1998 156 hours 90 Archipelago 1999
Montebello Islands 1993 135 hours 63
Murion Islands & 1996 72 hours 54 Exmouth Gulf
Coral Bay 2013 60 hours 56
Bernier and Dorre 1995 66 hours 55 Islands
Abrolhos Islands** 2014 26 hours 16
Geraldton** 2014 8 hours 7
**Results from this study
1.5 Aims of This Study
The Abrolhos Islands is a unique area located in the Midwest of Western Australia, supporting a mixture of tropical and temperate organisms (Phillips and Huisman, 2009;
Scheffers et al., 2012). There has been limited research carried out in the Midwest region on nudibranchs, which includes Geraldton and the Abrolhos Islands; this has provided the motivation for this study. Four main areas were the focus of this study: inshore Geraldton and offshore at the Abrolhos Islands across the three island groups: Wallabi, Easter and
Pelsaert.
The overarching aim of this research is to collect quantitative information from a range of locations within the Midwest region of Western Australia and establish a biogeographical baseline for the nudibranchs of this region. Specifically, the ecosystems they inhabit, species diversity, overall abundance and ecological processes that influence their
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distribution and the direction of future research. The Midwest region is a transition zone with critical overlap between tropical and temperate climate conditions; climate change- induced shifts are expected to occur in this region and the collection of baseline data can be used to monitor these shifts overtime.
The major aim of this study is to document baseline data for future long term monitoring programs, accounting for temporal and spatial variation in species abundance. The main focus is on diversity, species richness and abundance of nudibranchs at the Abrolhos
Islands and Geraldton. Investigations into habitat substrate, depth preference and connectivity will be explored. Site specific data will be recorded for each site including depth, water temperature, habitat use and activity undertaken by the individual nudibranch.
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2.0 METHODS
2.1 Area Description
Surveys for nudibranchs were conducted at Geraldton (28°45.5399 S; 114°37.0820 E) located in the Midwest of the Western Australian coastline; and the Houtman Abrolhos
Islands located on the edge of the continental shelf, 65-70 km to the north-west of
Geraldton (Figure 2.1.1) (Phillips and Huisman 2009; Scheffers et al. 2012). The Houtman
Abrolhos Islands (for the purpose of this paper referred to as the Abrolhos Islands) are comprised of 122 islands in three distinct groups: Wallabi Group, Easter Group and
Pelsaert Group (Scheffers et al., 2012) (Figure 2.1.2). These islands form one of the most complex high latitude coral reef systems in the world (Phillips and Huisman 2009).
Sample sites were randomly spread across the three groups, Easter Group (28°42 S;
113°47 E), Pelsaert Group (28°52 S; 113°57 E) and Wallabi Group (28°27 S; 113°43 E)
(Figure 2.1.2; a detailed layout of the sampling sites at each group is included in Appendix
2).The Leeuwin Current has noticeable impact on environmental parameters across the
Abrolhos Island groups and distinguishing the Islands from inshore habitats at Geraldton
(Phillips and Huisman 2009). Geraldton is inshore, not on the edge of the continental shelf therefore the Leeuwin Current does not have an impact in this area.
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Figure 2.1.1: The location of study sites, Geraldton and the Abrolhos Islands, in relation to Western Australia Adapted from (Caputi et al., 1996).
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Figure 2.1.2: Geraldton and the three Abrolhos Islands study sites, showing their location relative to each other (Google Earth, 2014)
2.2 Environmental Description
2.2.1 Wind
The winds at both Geraldton and the Abrolhos Islands have a similar seasonal wind pattern throughout the year. The Abrolhos Islands experience greater wind strengths with a mean wind speed in winter of 23.4 km h-1 and summer 31 km h-1 compared to Geraldton wind strengths of 15.8 km h-1 and 24.8 km h-1 respectively (Pearce, 1997; Phillips and
Huisman, 2009).
2.2.2 Swell
Geraldton has a persistent, low to moderate wave energy regime with dominant swell from the south to south-west (Hegge et al., 1996). Persistent swell waves are present at
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the Abrolhos Islands generated by prevailing south-westerly winds from the Southern
Ocean (Scheffers et al., 2012). Swell has a mean wave height of 1.2 m approaching from the south and west for the majority of the time (Collins et al., 1996; Scheffers et al., 2012).
The south-westerly reef margins absorb the full force of wave impacts, with the south- easterly reef edge attracting refracted swell and effects from wind waves (Collins et al.,
1996).
2.2.3 Current
The Leeuwin Current is the dominant current that runs along the Western Australian coastline and is summarised by Hatcher (1991) as being a narrow (<200 km), shallow
(<200 m) stream of water of tropical origin which flows southwards at relatively high velocities (0.1-0.4m s-1) along the western continental slope of Australia. Studies have shown that there is little direct influence of the Leeuwin Current near the coast (Phillips and Huisman 2009); however being situated of the edge of the continental shelf, the
Abrolhos Islands are directly in the path of the Leeuwin Current. Large eddies have been known to form between the islands groups creating small northward flowing currents
(Phillips and Huisman 2009).
2.2.4 Water Temperatures
The Western Australian Department of Fisheries have collected long-term time-series sea temperature data for the Abrolhos Islands. Mean temperatures measured at Rat Island
(Easter Group) ranged from 19.5°C in August to 23.3°C in March. Mean sea temperatures at Dongara, located on the coast 65 km south of Geraldton ranged from17.5°C in July to
23.9°C in February (Pearce 1997; Pearce et al. 1999; Phillips and Huisman 2009). The effect of the Leeuwin Current is particularly evident at the Abrolhos Islands during the winter months, maintaining ocean temperatures 2°C warmer than near the coast.
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2.2.5 Salinity
Salinity at the Abrolhos Islands ranged from 35.37ppm in July to 35.74ppm in January.
Dongara salinities ranged from 35.40ppm in July to 36.34ppm in February; Dongara salinities are similar to those found in Geraldton waters (Phillips and Huisman 2009). High salinity levels inshore can be attributed to evaporation in summer months whilst offshore the low salinity levels during winter months are caused by the Leeuwin Current (Phillips and Huisman 2009).
2.3 Habitat Description
In March 2014 pilot surveys were conducted at the Abrolhos Islands and Geraldton to determine the occurrence of nudibranch species on different habitat substrates.
Nudibranchs were found mainly in habitats that consisted of coral rubble overgrown with seaweeds; research efforts were therefore focused on sites that consisted of this habitat type. Sampling methods were designed to focus on benthic nudibranchs in both shallow and deep water habitats to gain information on the diversity and distribution of nudibranchs at Geraldton and the Abrolhos Islands.
2.4 Site Selection
Sites were randomly selected by looking at a nautical chart of the Abrolhos Islands. For each of the four sub-regions sampled 30 shallow sites were selected at random and 30 deep sites were selected at random; these sites matched the habitat description criteria as closely as possible. The sites were numbered from 1 to 30 and placed into a random number generator. The first four numbers were then chosen as sampling sites. The numbers were regenerated each time when choosing sampling sites for each sub-region.
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2.5 Survey Methods
Sampling was undertaken seasonally, to obtain a quantitative measure of nudibranch abundance at deep and shallow sites in the months of April, June and August. 15 m transects were set up using rope, ballast, sinkers and floats. The floats and ballast were positioned at 0 m, 7 m and 15 m along the transect line. The transect line was deployed at each of the sample sites; researchers then proceeded to swim along each side of the transect using SCUBA (Figure 2.5.1), covering an area of 60 m2 (2 m either side of the transect line). When a nudibranch was found several photographs were taken in situ, both macro and at a distance, to be able to accurately identify each individual. These images were also used to identify the substrate the nudibranch was observed on; habitats were recorded as one of the following eight categories, adapted from Bennett (2013): rocky reef
(R), crustose coralline algae (CA), macroalgae (MA), sessile organisms including spongers (S), Corals (C), sand/coral rubble (S/R), limestone (L) and unidentified (U). The activity of each individual nudibranch was determined using the images captured. Two depth categories were examined in this study: shallow sites were in the range of 1–2 m in depth and deep sites ranged from 5 m to 8 m. Four activity categories were identified: mating, stationary, moving and laying eggs. Nudibranch individuals that were in contact with another nudibranch were deemed to be mating. It was assumed that nudibranchs that were stationary were feeding. Each of the sample sites was given a unique site name corresponding to which location it can be found, for example site E14 represents a site that is in the Easter Group that is shallow sample site number 4 or W52 represents a site that is in the Wallabi Group that is a deep sample site number 2 (See Appendix 2).
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Figure2.5.1: Divers in the field searching for nudibranchs along the transect line
2.6 Species Identification
Nudibranchs were identified from photographs taken in- situ using Wells and Bryce
(1993), Coleman (2001) and Debelius and Kuiter (2007) as well as using information on online forums such as the Australian Museum’s Online Seaslug Forum (Rudman, 2010) and Nudibranchs of the Sunshine Coast, Queensland and Tasmania, Australia (Cobb and
Mullins, 2014). Several Chromodoris species individuals of the blue, black, orange and white colouration look quite similar and hard to accurately identify with certainty to species level. Species exhibit characteristics that constantly overlap. After consultation with taxonomic experts it was decided that if the individual had a punctuate pattern with either white pigments on the mantle flap it belonged to Chromodoris annae but if it was found to have blue on the mantle flap it belonged to Chromodoris westraliensis. If there was no punctate pattern at all it most likely belonged to Chromodoris sp. 24.
Gary Cobb, a nudibranch expert and creator of the webpage Nudibranchs of the Sunshine
Coast, Queensland and Tasmania, Australia, was consulted for his opinion on several of
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the Chromodoris species that were similar. Nerida Wilson, Senior Research Scientist of the Molecular Systematic Unit at the Western Australian Museum was also consulted, confirming all of the nudibranch identifications and recommended that gene sequencing take place for accurate species level identifications for the individuals that cannot be confidently identified. This information is, at this stage being processed and is currently still unpublished. Due to a lack of resources, individuals that could not be identified to species level were identified as near as possible to a particular species and labeled accordingly; e.g. Chromodoris cf. annae.
2.7 Statistical Analysis
2.7.1 Species and Abundance
Basic statistical analysis of data was performed using Microsoft Excel 2007 and IBM
SPSS v. 21. Comparison of abundance and species abundance was performed using
IBM SPSS v 21. All assumptions required for undertaking the statistical tests were assessed and met.
Species are considered rare if they persist in low abundances and are restricted to a few specialised sites (Benkendorff and Przeslawski, 2008). The use of the quartile cut-off provides a standardised method to asses rarity in rocky shore invertebrates (Benkendorff and Przeslawski, 2008) Use of the rarity scale helps target species with lower than average abundances for more in-depth studies (Benkendorff and Przeslawski, 2008). A scale of rarity was derived from Benkendorff & Przeslawski (2008) based on one of the three assessment measures, numerical rarity (Table 2.7.1). The proportion of nudibranchs was used to rank occurrence into quartiles
21
Table 2.7.1: Rarity scale used to determine occurrence of nudibranchs at the Abrolhos Islands and Geraldton. Adapted from Benkendorff & Przeslawski (2008).
Abundant ≥ 30 individuals observed over the survey sites
Common 8-29 individuals observed over the survey period
Uncommon 2-7 individuals observed over the survey sites
Rare Single observation of an individual with unpredictable occurrence across survey sites
2.7.2 Species Diversity and Evenness
The Shannon-Weaver index of diversity (H’) was used to explore differences in species richness between sites and depth of sites.
Where pi is the proportion of individuals of each species to the total number of individuals
(Shannon and Weaver, 1963).
Species evenness was determined using Pielou’s Evenness Index:
22
H’ is the Shannon Weaver diversity index and H’max can be determined by ln(S), where S is the total number of species. H’max is the theoretical maximum values for H’ if all species were equally abundant (Pielou, 1966).
2.7.3 Connectivity
Species connectivity was determined using PRIMER v 6.1 (Primer-E Pty Ltd).
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3.0 RESULTS
In total, 89 dives were made over the duration of this study, with an average dive time of
30 minutes and an accumulated overall bottom time of 23 hours and 14 minutes. Two of the deepest dives of the study took place in the Wallabi Group, reaching 8.7 m and 8.5 m at sites W51 and W54 respectively (See Appendix 2.4). The shallowest average dive was to 1.5 m occurring at 11 of the sample sites at two of the shallow sites in each sampling location; a summary of depth and other site details can be found in Appendix 1.
3.1 Species and Abundance
A total of 296 individual nudibranchs were visually observed and photographed across 89 separate dive surveys over the study period from April to August 2014. 148 individuals were identified from both shallow and deep sample sites across the four different sub- regions. A total of 17 different species of nudibranch were found at the shallow sites across all four sub-regions and 12 different species across the deep sites. Of the total species found six were present at both shallow and deep sampling sites. Geraldton had
11 individuals of six species found at the shallow sites and five individuals of two species at the deep sites (Figures 3.1.1 and 3.1.2). The Easter Group had 71 individuals of 12 species found at the shallow sites and 65 individuals of six species at the deep sites. The
Wallabi Group had 36 individuals of five species over the shallow sites and 38 individuals of six species over the deep sites. The Pelsaert Group had 30 individuals of ten species across the four shallow sites and 40 individuals of seven species found across the four deep sample sites.
24
80
70
60
50
40 Shallow
30 Deep
Number of Individuals of Number 20
10
0 Geraldton Easter Wallabi Pelsaert
Figure 3.1.1: Total number of individual nudibranchs found in each of the survey sub-regions at two depths over an area totaling over 5 km2
14
12
10
8
6 Shallow
Deep Number of Species of Number 4
2
0 Geraldton Easter Wallabi Pelsaert
Figure 3.1.2: Total number of species of nudibranchs found in each of the survey sub-regions at two depths over an area totaling over 5 km2
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Of the three sampling trips the first trip was the most successful with researchers locating a total of 111 nudibranchs, 52 individuals over the 17 shallows sites and 59 individuals over the 14 deep sites. The second and third sampling trips resulted in 82 and 103 individual nudibranchs respectively being located and photographed. Each sampling trip was carried out in a different season; the first trip in autumn, the second trip in winter and the third trip in spring. A total of 19 different species were identified; Table 3.1.3 is a complete list of nudibranch species that were identified during the study, their respective families, authority and occurrence according to the rarity scale (see Table 2.7.1).
Table 3.1.3: Complete list of nudibranch species found over the duration of the study at Geraldton and the Abrolhos Islands, 2014
Family Species Name Authority Occurrence Aegiridae Notodoris citrina Bergh, 1875 Common Chromodorididae Chromodoris annae Bergh, 1877 Common Chromodoris cf. annae Common
Chromodoris cf. sp. 24 Common
Chromodoris cf. westraliensis Common
Chromodoris westraliensis O'Donoghue, 1924 Abundant
Chromodoris sp. 24 Abundant
Glossodoris atromarginata Cuvier, 1804 Rare
Glossodoris hikuerensis Pruvot-Fol, 1954 Rare
Mexichromis cf. mariei Rare Dendrodorididae Dendrodoris fumata Ruppell & Leuckart, 1831 Rare Discodorididae Atagema intecta Kelaart, 1858b Uncommon Jorunna funebris Kelaart, 1858 Uncommon Gymnodorididae Gymnodoris citrina Bergh, 1875 Uncommon Gymnodoris sp. Rare Phyllidiidae Phyllidiella pustulosa Cuvier, 1804 Uncommon Polyceridae Crimora lutea Baba, 1949 Rare Tritoniidae Marionopsis dakini O'Donoghue, 1924 Uncommon Tritoniopsis elegans Andouin, 1826 Uncommon
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3.2 Family Level Analyses
The 19 species of nudibranch found during the study came from 13 different genera in eight families (Table 3.1.3). The family Chromodorididae was the dominant family, with a total of 268 individuals in three genera; Aegiridae had 8 individuals, Tritoniidae and
Discodorididae had 5 and 6 individuals respectively from two different genera.
One species of nudibranch could only be identified to genus level as it is currently not described, and is not in any published identification book; additional information is required for taxonomic placement (Figure 3.2.1). The most abundant species found overall was Chromodoris westraliensis (n=155). The second most abundant species across the study regions was Chromodoris sp. 24 (n=48). Several variations of
Chromodoris sp. 24 were found during the study, with varied colouration and patterns; hence the decision to identify 11 individuals as Chromodoris cf. sp. 24. (Figure 3.2.2).
Chromodoris cf. annae (n=27), Chromodoris cf. westraliensis (n=17), Chromodoris cf. sp.
24 (n=10) concluded the top five nudibranch species found during the study. Chromodoris annae and Notodoris citrina both had 8 individuals found.
27
Figure 3.2.1: Unidentified species found during this study, Gymnodoris sp.
Figure 3.2.2: Two alternative versions of Chromodoris cf. sp. 24 that were found over the duration of this study.
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3.3 Total Abundance Analyses
A T-test was performed to investigate whether there was a difference in the mean number of individuals in the shallow and deep sampling sites. No significant difference was found between the mean number of individuals per transect at shallow (mean = 2.90, SE = 1.23) and deep sites (mean = 3.58, SE = 1.34) (α = 0.05, t29 = 2.05, p-value = 0.48), the number of nudibranchs at deep and shallow sites were the same. The largest number of individuals per transect was found at the Easter Group (mean = 22.5, ± 0.77 SE) followed by the Wallabi Group (mean = 12.33, ± 0.73) and the Pelsaert Group (mean = 11.8, ±
0.79 SE), with the lowest recorded number of individuals per transect at Geraldton (mean
= 3.2, ± 0.32 SE).
There was a significant difference in the mean number of individuals per transect at the four sites (ANOVA: α=0.05, F(3,89)=5.21, p-value=0.002). To investigate if Geraldton was the determining factor for the significant difference in the initial ANOVA analysis, the analysis was run again; although this time Geraldton was excluded. The second ANOVA resulted in a significant difference (α=0.05, F(2,71)=3.83, p-value=0.026). The mean (± SE) number of nudibranchs per transect found across each sub-region varied markedly
(Figure 3.3.1), with a mean of 0.9 (± 0.25) for the shallow sites and a mean of 1.25 (±
0.25) for the deep sites at Geraldton. At the Abrolhos Islands, the Easter Group sites had the highest mean number of nudibranchs per transect over the duration of the study at both shallow and deep study sites, with a mean of 5.8 (± 0.33) and 5.4 (± 0.76) respectively. The Wallabi Group had a mean of 3.0 (± 0.09) nudibranchs across the shallow sites and a mean of 3.2 (± 1.04) nudibranchs across the deep sites per transect.
The Pelsaert Group had a mean of 2.6 (± 0.28) nudibranchs across the shallow sites and a mean of 3.3 (± 0.96) individuals across the deep sites per transect. The deep sample sites at the Easter Group, Wallabi Group and Pelsaert Group showed a large variation in numbers per transect over the three sampling trips, resulting in a greater standard error
29
compared to the shallow sites. The shallow survey sites at the Wallabi Group resulted in the least amount of variability.
7.0
6.0
5.0
4.0 Shallow
3.0 Deep
2.0 Mean Number of Individuals of Number Mean
1.0
0.0 Geraldton Easter Group Wallabi Group Pelsaert Group
Figure 3.3.1: The average nudibranchs found each study trip at each study site comparing the variation between shallow and deep study sites per transect
3.4 Total Species Analyses
To investigate whether there was a difference in the mean number of species in shallow vs. deep sites a T-test was performed. No significant difference was observed between the mean number of species at shallow (mean = 1.63, SE = 0.372) and deep sites (mean
= 1.54, SE = 0.078) per transect, (α = 0.05, t29 = 0.22, p-value = 0.826). A significant difference in the mean number of species per transect between the four study sites was observed using ANOVA (α = 0.05, F(3,89) = 6.43, p-value = 0.001). To determine if
Geraldton was the driving factor for the significant difference result the analysis was performed again excluding Geraldton; a significant difference was observed between the three Abrolhos Island sites (ANOVA: α=0.05, F(2,71)=5.18, p-value=0.008). The largest
30
number of species per transect was found at the Easter Group (mean = 10, ± 0.31) followed by the Wallabi Group (mean = 6.7, ± 0.26 SE) and the Pelsaert Group (mean =
5.5, ± 0.19), and lastly the lowest recorded species per transect was at Geraldton (mean
= 2.4, ± 0.24 SE).
The mean number of nudibranch species found across each sub-region varied with
Geraldton having a mean of 0.6 (± 0.21) for the shallow sites and a mean of 0.8 (± 0.25) for the deep sites per transect (Figure 3.3.2). In the Abrolhos Islands region, the Easter
Group had the highest mean number of species of nudibranchs per transect over the duration of the study at both shallow and deep study sites with a mean of 2.9 (± 0.14) and
2.1 (±0.18) species respectively. The Wallabi Group had a mean of 1.7 (± 0.24) species of nudibranchs per transect for both shallow and deep sites. The Pelsaert Group had a mean of 1.4 (± 0.11 SE) across the shallow sites and 1.3 (±0.07) species across the deep sites per transect.
3.5
3.0
2.5
2.0 Shallow
1.5 Deep
Mean Number of Species of Number Mean 1.0
0.5
0.0 Geraldton Easter Group Wallabi Group Pelsaert Group
Figure 3.3.2: The average species of nudibranchs found each study trip at each study site comparing the variation between shallow and deep study sites per transect
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3.5 Interactions
To explore interactions between sub-region and depth for individual counts and species counts, two factorial ANOVAs were carried out. Sub-region was a significant factor for number of individuals per transect and depth was not significant (F(3,89) = 0.08, p-value =
0.778) (Figure 3.5.1). An interaction was observed between depth and sub-region but was found to be not significant (F(3,89) = 0.11, p-value = 0.952). For the number of species region was significant and depth was not significant (F(3,89) = 0.58, p-value = 0.448)
(Figure 3.5.2). The interaction between depth and region was not significant (F(3,89) = 0.62, p-value = 0.601).
Figure 3.5.1: Results from factorial ANOVA with the mean number of individual nudibranchs found at the different sites, compared with depth.
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Figure 3.5.2: Results from factorial ANOVA with the mean number of species of nudibranchs found at the different sites, compared with depth.
3.6 Species Diversity and Evenness Indices
Of the four sub-regions sampled, Geraldton had an overall total of six species across all shallow sites and an overall total of two species across the deep sites. The Abrolhos
Islands had an overall total of 14 species across all shallow sites and an overall total of nine species across all deep sites.
The Shannon-Weaver index of diversity (H’) and Pielou’s evenness index (J’) were calculated for several different factors across the study. Firstly the diversity and evenness of all species found was calculated, generating a diversity index of 1.71 and an evenness index of 0.58 for the Midwest region of Western Australia.
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Species diversity and evenness were greater inshore at Geraldton (H’ = 1.93, J’ = 0.93), than at the Abrolhos Islands (H’ = 1.62, J’ = 0.10). Diversity and evenness for depth variations was greater at shallow sites (H’ = 1.97, J’ = 0.47), than at the deep sites (H’ =
1.32, J’ = 0.90). A species diversity index was calculated for all of the survey sites across the shallow and deep sampling sites (Figure 3.2.1). The Easter Group (H’ = 1.90, J’ =
0.76) and the Pelsaert Group (H’ = 1.90, J’ = 0.82) had the equal greatest diversity across shallow sites compared to Geraldton (H’ = 1.59, J’ = 0.89) and the Wallabi Group (H’ =
0.92, J’ = 0.57) (Figure 3.6.1). The Pelsaert Group (H’ = 1.30, J’ = 0.67) had the greatest diversity across deep sample sites followed by the Wallabi Group (H’ = 1.11, J’ = 0.62), the Easter Group (H’ = 1.07, J’ = 0.60) and Geraldton (H’ = 0.67, J’ = 0.97).
2
1.8
1.6
1.4
1.2
1 Shallow Deep 0.8
0.6
Shannon Weaver Diversity Index DiversityWeaver Shannon 0.4
0.2
0 Geraldton Easter Group Wallabi Group Pelsaert Group
Figure 3.6.1: Shannon Weaver diversity index for mean nudibranchs found across the two study regions
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3.7 Connectivity
Bray-Curtis similarity cluster and Multi-Dimensional Scaling (MDS) plots were created to explore the species abundance, diversity and depth preference between sample sites.
Geraldton is clearly different to the island groups, with distinct differences in species abundance not only between sub-regions but between depths as well (Figure 3.7.1,
Figure 3.7.2). To better understand similarity in the Abrolhos Islands groups, Geraldton was excluded from the MDS analysis in Figure 3.7.3. The similarity of individual sampling sites was compared with two shallow sites from the Pelsaert Group having less than 20% similarity compared to the other island group sampling sites.
Figure 3.7.1: Dendrogram of hierarchical clustering combining all sampled sites from March to August 2014, using group average linking of Bray-Curtis coefficient (Southern Group is referring to Pelsaert Group).
35
Figure 3.7.2: MDS analysis of nudibranch abundance at all sample sites showing depth as a factor.
Figure 3.7.3: MDS analysis of nudibranch abundance at the Island sample sites (excluding Geraldton) showing similarity with depth as a factor.
36
Whilst Figure 3.7.1 shows the grouped averages of abundance of all sites sampled,
Figure 3.7.4, shows the condensed group averages of abundance specific to depth preference. There is a clear separation between Geraldton and the island sites in Figure
3.7.4 the Wallabi Group was found to have the most similarity between deep and shallow sites compared to the Easter Group and the Pelsaert Group, which have the most similarities between sites of the same depth. MDS similarity of island sampling sites, excluding Geraldton to allow for clearer comparison, illustrated a similarity of 90% between the Wallabi Group shallow and deep sampling sites, with the Easter and
Southern Group having 60% similarity (Figure 3.7.5). No sites were determined to be more than 90% similar.
Figure 3.7.4: Dendrogram of hierarchical clustering of sub-regions sampled, defined by depth preference, using group average linking of Bray-Curtis coefficient (Southern Group is referring to Pelsaert Group).
37
Figure 3.2.5: MDS analysis and similarity clustering of all island sites (excluding Geraldton) (Southern Group is referring to Pelsaert Group).
3.8 Substrate Preference and Activity
Substrate type and activity of each nudibranch found was determined using field observations and photographs taken at the time of observation. The majority of nudibranchs were found on either rocky reef or macroalgae substrates, with moving being the dominant activity at both shallow and deep sites (Figure 3.8.1). Shallow and deep sites combined resulted in rocky reef and macroalgae being the overall dominant substrate types (31.4%), followed by crustose coralline algae (14.5%), sand/coral rubble
(11.5%), sessile organisms (6.4%), unidentified (3.4%) and corals (1.3%). The activities of each nudibranch were combined for the shallow and deep sites finding moving to be the dominant activity (79.4%), followed by stationary (18.9%), mating (1.4%) and laying eggs
(0.3%). Out of the 6.5% of nudibranchs found on sessile organisms, 4% were classified as stationary.
38
Figure 3.8.1: Percentage of individual nudibranchs combined of both shallow and deep sites and their respective activity compared to the substrate they were found inhabiting
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4.0 DISCUSSION
4.1 Estimating and Comparing Diversity
Limited studies on nudibranch species diversity have been carried out in Western
Australia, with the Western Australian Museum responsible for the majority of specimen identifications. The total of nineteen species (16 from the Abrolhos Islands and 7 from
Geraldton) were reported in this study, which is comparable to the study by Bennett
(2013). Bennett found 56 opisthobranchs in the Coral Bay region, 49 of these were nudibranchs. Species came from ten different nudibranch families with seven of these families also encountered in this study. Of the 49 species identified in Coral Bay, eight species were also identified in this study, including the unidentified Gymnodoris citrina, which was identified by Bennett as Gymnodoris sp. 1. The species Tritoniopsis alba was identified in the study by Bennett (2013) at Coral Bay; expert consultation for this study concluded that T. alba is only found in the northern hemisphere (pers. comm. Nerida
Wilson 2014). Therefore the species Tritoniopsis elegans is the correct species; with distributions that reach the Indo-Pacific. This species was therefore counted as T. elegans for comparisons with this study. There were 74 more species of opisthobranchs found at the Dampier Archipelago than in this study of the Midwest region. All of the species found in this study have a tropical, Indo-West Pacific distribution; none were temperate species.
It was anticipated that some temperate species would be found in this study as the
Abrolhos Islands is a transition zone for both tropical to temperate marine organisms
(Wells and Bryce, 1993). It might be expected that additional survey efforts in the Midwest region will uncover a number of temperate species.
Comparisons of species abundance can be made with other studies in the Indo-Pacific, outside Australia that had similar research methods. Chavanich et al. (2013) explored the diversity and occurrence of nudibranchs in Thailand, finding Chromodorididae to be the dominant family accounting for 35% of the total number of species found. This study also
40
found Chromodorididae to be the dominant family with 47% of the total number of species
(n=8). There were 96 nudibranch species identified in the study from Thailand, eight of these species are the same as the species from this study. The remaining 11 species from this study that were not found in Thailand were comprised mainly of chromodorids that are endemic to Western Australia (Chromodoris westraliensis and Chromodoris cf. westraliensis); and also species of chromodorids that require further genetic analysis, destructive sampling for accurate identification and species that have only been identified from the Ningaloo Reef (Chromodoris cf. annae, Chromodoris sp. 24 and Chromodoris cf. sp. 24). Chavanich et al. (2013) concluded the study by stating “it is likely the present number of Thai nudibranchs is an underestimation and that additional species will be discovered in the future”. Future investigations will need to be made into the presence and abundance of temperate nudibranch species at Geraldton and the Abrolhos Islands.
During the study, three sampling trips were carried out over a five month period, each in a different season. The variation in numbers over each sampling trip is quite possibly attributable to seasonality in nudibranchs, length of life cycle during each season and food available in the habitat seasonally. Abundance fluctuations in nudibranch populations can be explained by a reduction in food supply in a locality (Aboul-ela, 1959). Seasonality was not a major aim of this study as time constraints did not allow a full year to collect a complete data set; therefore the results presented from this study should be treated as a
‘snap-shot’ of species diversity and abundance in the Midwest region. The fieldwork period was not long enough to determine any kind of seasonal trends; however small scale seasonality may have played a role in the findings, with 20-30 less individuals found during the winter survey trip compared to the autumn and spring months. Individual nudibranchs were also observed to be notably smaller in size during the spring sampling trip compared to the first two sampling trips (pers. obs.). If seasonality was to be assessed, sampling would also need to take place in summer months and potentially for two seasonal rotations to gain a better understanding of nudibranchs and their
41
relationship with the seasons. Some species of nudibranch live for several months while others up to two years. Aerts (1994) found that temperature fluctuations over the seasons have an influence on annual species of nudibranchs as they are not strongly associated with their food sources. Sub-annual species are not directly influenced by temperature fluctuations however. These species generally feed on seasonally variable resources making the abundance of their dietary species the primary influence of population abundance (Aerts, 1994; McCuller, 2012). Because the project used volunteer field assistants, there is a possibility that some nudibranchs were missed while the volunteers were developing nudibranch location skills. Using the same two divers for each of the fieldwork trips would reduce this type of error.
4.2 Family Level Analysis
Species-level identification of nudibranchs from the genus Chromodoris was relatively difficult. Due to this uncertainty, where possible, analysis of data was performed using family or genus information. Colouration between species in the Chromodorididae is very similar, making it hard to accurately differentiate between the different species. To accurately identify nudibranch individuals to genus and species level without using destructive sampling methods close attention must be paid to the visible distinguishing features of each individual; these can be body shape, size, exposed or hidden gills, whether pustules or cerata are present, and colour variation. Valdes et al. (2013) pointed out the need for caution when making generalisations about the evolutionary role of colouration in opisthobranchs; results from their study showed external colouration and pattern of species not to be associated with genetic structure. The colouration of the difficult individuals was all the same: blue, black, white and orange, with distinguishing features being black line markings, presence of white along the edge on the mantle and punctate pattern across the surface of the body. Consultation with taxonomic experts concluded that if the individual had a punctate pattern with white pigment on the mantle
42
flap it belonged to Chromodoris annae but if it was found to have blue on the mantle flap it belonged to Chromodoris westraliensis. If the animal had a dorsal black stripe between the rhinophores but had clear markings from either C. annae or C. westraliensis it was classified as similar to (cf.) these species. If there was no punctate pattern on the animal at all it was then classified as Chromodoris sp. 24. (Rudman, 1984, 1998)
The most abundant family found was Chromodorididae. Chromodoris westraliensis was the dominant species found during this study and is endemic to Western Australia (Wells and Bryce, 1993), found in the Indo-West Pacific region, ranging from tropical to sub- tropical zones along the Western Australian coast (Debelius and Kuiter, 2007). Rudman
(1991) found colour patterns in chromodorids can exist between unrelated species within a colour group. These species can occur sympatrically in discrete geographic regions.
The colour groups for species are the most developed in isolated regions in warm temperate or sub-tropical waters. Rudman found that species of sympatric colour groups are often locally abundant with closely related species within a colour group, usually allopatric with wide geographic ranges. Rudman also found that chromodorid nudibranchs in semi-isolated geographic regions of high endemism, with high species diversity on the fringes of main oceans, are considered the centers of chromodorid speciation; this describes the exact location of the Abrolhos Islands. The Abrolhos Islands is an isolated, remote area with several hundred kilometers to the nearest coral reef system. It is believed that members of the Chromodoris genus are going through a phase of rapid speciation at the moment along the Western Australian coastline (pers. comm. Nerida
Wilson, 2014). Assortive mating is one method that can lead to population subdivision, adaptation and divergence (Faucci et al., 2007). Chromodoris produces planktotrophic veliger larvae that undergo a short embryonic period before hatching after 5-7 days
(Trickey et al., 2013). Przeslawski et al. (2008) discusses groups of benthic invertebrates that are potentially more vulnerable to extinction due to environmental change revealing that gastropods with planktotrophic larvae development had the highest rates of
43
speciation. Further studies are being conducted by the Western Australian Museum, awaiting genetic results to see if members of the Chromodoris genus are undergoing acute speciation and creating hybrid species (pers. comm. Nerida Wilson, 2014).
High numbers of Chromodoris westraliensis individuals can indicate that this species is thriving in its environment, being classed in less than 10% of species endemic to Western
Australia (Wells and Bryce, 1993). The second most abundant species found,
Chromodoris sp. 24 has not been fully described, although it has distinct markings and has previously been found on the Ningaloo reef (Debelius and Kuiter, 2007). Johnson and
Gosliner (2012) researched the taxonomic evolutionary history of chromodorid nudibranchs, revealing the need for more evolutionary studies of colour patterns and trophic specialisation. They documented the many taxonomic, nomenclatural and species delineation problems that still require refinement within the chromodorid nudibranchs.
4.3 Total Species and Abundance
Equal numbers of nudibranchs were found at shallow and deep sites. The depth categories chosen (1-2 m and 5-8 m) support different organisms and consequently are comprised of a number of different seaweeds and cnidarians that have been known to influence nudibranch abundance (García-Matucheski and Muniain, 2011). Some species of nudibranchs live at greater depths than others, with species found at depths ranging from shallow reefs in Hawaii (Kay and Young, 1969) to abyssal shelves 4 km deep in the
Arctic (Jörger et al., 2014). A diversity survey in the United Kingdom focused on sites ranging from 15 m to 40 m (Lock et al., 2010) resulting in the identification of 55 species.
There is limited published literature on depth variation in nudibranchs. Bennett (2013) suggested that diversity increases with depth but may be related to increased water flow in an area. The results of this study did not reflect a significant difference in the number of species found at shallow or deep sites. Studies on depth categories of greater variation or
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sites that are influenced by increased water flows may have returned a different result.
Habitat types and food sources for nudibranchs vary with depth, These factors are presumed to be the main driver of abundance of species in an area. Investigations into key nudibranch prey items; sponges, hydroids and bryozoans seasonal occurrence may help in predicting abundance of sub-annual nudibranch species (Aerts, 1994; Lock et al.,
2010)
A significant difference in abundance of nudibranchs was observed between sampling sub-regions. There was a clear difference between the number of individual nudibranchs found at Geraldton, across both shallow and deep sites, and the three Abrolhos Island groups. A significant difference of abundances was also observed between sampling sub- regions at the Abrolhos Islands. There were clear differences in the number of species of nudibranchs found at the Geraldton survey sites compared to the Abrolhos Island groups.
A significant difference was within the Abrolhos Island groups also observed when the
Geraldton sites were excluded from the analysis. These results indicate that Geraldton is not the solitary driver for the initial significant result in both cases, although supporting analysis of clustering techniques clearly identifies Geraldton as the main driver. Further analysis showed a significant difference between island groups identifying the Easter
Group as having a marked difference in abundance and species numbers compared to the two other island groups, indicating that Geraldton is significantly different to the three island groups, with the Easter Group having a more subtle influence on abundance and species numbers within the island sites. Further investigations into the abundance and species of nudibranchs across the Abrolhos Island groups should be undertaken before any conclusions can be made from these results.
The Easter Group had the greatest abundance and species of nudibranchs found in this study. The Wallabi Group and the Pelsaert Group had similar abundance and numbers of species with Geraldton having the least nudibranch abundance and number of species. A steady decline in species abundance is present with increasing longitude, indicating
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distance from the mainland may be linked to the influence of the Leeuwin Current. Garcia and Bertsch (2009) found presence-absence of species in a biogeographical region to have a latitudinal gradient in distribution when assessing genus level classification. The overall abundance and distribution of nudibranchs across the study sub-regions were significantly different, and perhaps related to the physical characteristics of the regions.
Domenech et al. (2002) observed that depth, water movement, habitat and presence of prey in a location had an effect on the distribution of opisthobranchs. Higher energy environments returned lower opisthobranchs in an area. The low number of nudibranch species found at Geraldton may be attributed to the different marine environments in each region. Geraldton does not receive the full influence of the Leeuwin Current like the
Abrolhos Islands, with the Capes Current influencing marine species when it is the dominant current in summer months (Westera et al., 2009). The Abrolhos Islands and
Geraldton are home to a mixture of temperate and tropical species of marine flora and fauna (Smale and Wernberg, 2012), although fewer tropical species occur in Geraldton compared to the Abrolhos Islands. The coastline of Geraldton is a low to moderate energy environment (characterised by stronger water movement from dominant swell). Strong water movement causing sediment to re-suspend, creating turbid conditions in the area, may have had an effect on nudibranch distribution and abundance. Habitat differences and nudibranch prey items at each site contributed to nudibranch abundance in each sub- region.
Anthropogenic effects on the Abrolhos Island reef habitats could potentially have an effect in the abundances of nudibranchs found at each island group. The lobster industry at the
Abrolhos Islands has been established for generations and involves fishermen disturbing the coral reef systems in localised areas with fishing equipment. The equipment is heavy and has the potential to damage coral reefs, leaving areas of coral rubble, which nudibranchs have been found to inhabit. Structural diversity of benthic ecosystems is reduced by the used of mobile fishing equipment, that crushes, buries and exposes
46
marine animals (Watling and Norse, 1998). Further information on the effects fishing activities have had on the Abrolhos Island benthic invertebrate marine environment needs to be obtained. The degree of disturbance inflicted on the marine habitat over generations should be investigated.
The influence of depth was analysed and showed no significance difference at the sites; and there was no significant interaction found between depth and sub-region. Sub-region was analysed alone and showed a significant difference, suggesting that the predominant influence in nudibranch abundance and species richness is the region they are found in.
4.4 Species Diversity and Evenness
This study was carried out during the day-time, like the majority of species diversity studies. Night-time surveys of nudibranchs have been relatively neglected posing the question: do day-time surveys produce an accurate species diversity result? Nudibranchs are cryptic, mysterious organisms with nocturnal tendencies (Gochfeld and Aeby, 1997).
Due to logistical constraints, night-time surveys were not conducted during this study, implying predominantly nocturnal nudibranchs were not identified and were not included in the abundance and diversity data presented in this study. Chang et al., (2013) performed diel (i.e. day and night) surveys finding that different species were abundant during the day-time compared to the night-time surveys. These results highlight the need for an increase in diel or night-time surveys. Investigations into destructive day-time and night-time surveys could also result in increased species diversity and abundance in an area, as sections of reef nudibranchs are found inhabiting are rather complex. Without destructively sampling these areas we will never gain a truly accurate species abundance or diversity measure.
Although Geraldton had the lowest abundance of nudibranch out of the sub-regions, it was quite diverse. Geraldton was found to have a greater species diversity than the
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Abrolhos Islands; this is a rather surprising result. The Shannon-Weaver Diversity Index is calculated using the proportion of species found relative to each other. There was a greater unevenness in the proportions of species at the Abrolhos Islands, whereas
Geraldton had a more even proportion of each species. The intermediate disturbance hypothesis states that local species diversity is maximised when ecological disturbance is neither too rare nor too frequent (Rogers, 1993). The Geraldton marine environment is more exposed to swell when compared with the marine environment at the Abrolhos
Islands and could be considered partially disturbed. Disturbance is defined as a temporary change in average environmental conditions, causing a distinct change in the ecosystem (Rykiel, 1985). Processes that effect benthic invertebrate populations found to operate over small spatial scales (Olsen et al., 2014). Freshwater runoff in the coastal waters of Geraldton from the nearby Greenough and Chapman Rivers are natural sources of disturbance. Nutrients from agricultural catchment runoff can increase nutrients in the surrounding marine environment when outflow is deposited (Devlin and Brodie, 2005).
River outflow events have created severe turbid conditions and sedimentation issues along the coastline of Geraldton for several days (pers. obs.). Turbidity is considered a disturbance factor, caused by natural or anthropogenic influences. Turbid conditions are known to cause physiological stress on benthic invertebrates. The Leeuwin Current’s effect on the biota in Geraldton may have more of an influence than research suggests.
All of the species of nudibranchs identified in Geraldton were tropical species. More sample sites at Geraldton with more repetition would perhaps return a different result.
The Wallabi Group is more diverse in the deep sites compared to the shallow sites.
Commercial fishing activity or boating activity was found to decrease abundance of nudibranchs in an area (Domenech et al. 2002). Relatively low densities of fishing pressures exist at the Abrolhos Islands, with the benthic substrate unlikely to be influenced by boating activity. The commercial fishery at the Abrolhos Islands is highly unlikely to have an impact on the distribution and abundance of nudibranchs; hence the
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more likely reasoning for this result is site selection. The shallow sites that were randomly selected had less nudibranch species than the deeper sites.
4.5 Distribution
Geraldton was found to be distinctly different compared to the Abrolhos Island sites.
Differences in ecological and biological processes and habitat between Geraldton and the
Abrolhos Islands have been discussed in chapters above, with the dominant difference likely due to the Leeuwin Current and its effects on the regions. Geraldton and the
Abrolhos Islands both had a tropical species composition, with no temperate species found. The Wallabi Group is the northern most sub-region in the study. The high similarity of clustering between the shallow and deep sites within this group could be due to benthic habitat structure. The sampling design was random eliminating any bias when sites were chosen. The Wallabi Group is situated further into the Leeuwin Current; found to be the site of the most north-western sampling location in the study. The probable cause for the difference in sub-regions is the influence the Leeuwin Current has on the habitat composition.
The Leeuwin Current is believed to strongly influence recruitment of larvae with strong recruitment linked to increases in invertebrate abundance in subsequent years (Caputi et al., 1996). Watson and Harvey (2009) discussed fish larvae transport by the Leeuwin
Current from northern populations such as the Ningaloo Reef to southern ecosystems, such as the Abrolhos Islands. Effects of larvae dispersal and recruitment by the Leeuwin
Current between the three Abrolhos Island groups were found to be substantially weaker; although further studies are required to confirm this. The Leeuwin Current fluctuates during the year, with its strongest influence being felt during the winter months. These seasonal variations play an important role in the movement, survival and destination of larvae along the Western Australian coastline (Caputi et al., 1996; Gaughan, 2007).
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4.6 Substrate Preference and Activity
The literature has pointed to substrate preference of nudibranchs being highly dependent on prey resources in the area. Chavanich et al. (2013) found the majority of nudibranchs occured on coral rubble substrates (39%), followed by sand (28%) and sessile organisms
(25%). The preferred habitat for nudibranchs in this study was rocky reef and macroalgae substrates closely followed by crustose coralline algae. This may be an indication of the dominant flora present in the survey region. Rocky reef provides nudibranchs shelter and is generally comprised of colonies of sponges, bryozoans and hydroids; ideal nudibranch prey items. Bennett (2013) suggested that nudibranchs do not ‘live’ on the habitat their prey items are found on, they feed and then move back to reside and shelter in rocky reef, coral rubble or sand habitats. When located in-situ, 79% of nudibranchs observed in this study were moving, predominantly across rocky reef, macroalgae and coralline algae substrates. Stationary was the second most prevalent activity seen, with the majority of stationary nudibranchs found on rocky reef, macroalgae and coralline algae as well as sessile organisms. Results from this study show that the majority of nudibranchs found on sessile organisms are stationary. Therefore it can be concluded that nudibranchs can be seen ‘moving’ when in search for prey items and can be ‘stationary’ when feeding on said prey item.
4.7 General Discussion
Climate change is already having impacts on marine environments around the world.
Species of mollusc have extended their range and now are spread further from the polar regions than their natural distribution (Johnson et al., 2011; Perry et al., 2005). Prey items of nudibranchs are also exposed to effects from climate change. Research involving species of bryozoan communities in coral reef ecosystems has recorded local extinctions
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in several species with an increase in sea temperature, suggesting that impacts on larval survival and settlement are the most plausible explanation (Kelmo et al., 2004).
Nudibranchs are rather prey-specific organisms, only feeding on one or two species of prey items (Faucci et al., 2007). In this case, if nudibranchs that feed on the bryozoan species were present in the area they would also become extinct. Biodiversity variations, population extinctions, habitat degradation and climate changes are all important issues when monitoring biogeographical data (Bertsch, 2010). Nudibranchs are the top predator in the communities they feed on and the presence of these gastropods can be an indication of ecosystem health (Lock et al., 2010).
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5.0 CONCLUSION
No quantitative information on nudibranchs is currently available for Geraldton or the
Abrolhos Islands; consequently this study focused on obtaining baseline data on species abundance and diversity in the Midwest region of Western Australia. The species list presented in Chapter 3 is the one of the first species list of nudibranchs to be created for the Midwest region. Geraldton was found to be clearly different to the three Abrolhos
Island groups, with sub-region being a determining factor for abundance and species abundance. The variable distribution of nudibranch species over the geographic range in the Midwest is thought be due to the Leeuwin Current and the impacts associated with the prey items and substrate types nudibranchs prefer. There are numerous biotic and abiotic factors that influence the abundance of nudibranchs in a certain location; these include swell, available food, turbidity, time of day, temperature or predator presence. The
Leeuwin Current is predicted to be the main influence on nudibranch distribution in the
Midwest, varying with seasonality. The prediction that nudibranch species abundance is significantly different at varying depths was not supported by the findings of this study, but investigations into the influence of the above biotic factors could highlight biogeographical trends in nudibranch distribution. Further research into the degree of influence the
Leeuwin Current has on nudibranch populations in the Midwest region will allow future predictions.
This study has added to our knowledge of nudibranchs in the Midwest region of Western
Australia. Subsequent studies in this region will produce a species list that will contribute to the growing knowledge base of nudibranch diversity along the Western Australian coastline and can help identify northern and southern limits of species distributions.
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5.1. Future Implications
The Abrolhos Islands is a large and diverse marine environment that requires greater sampling effort to gain a better idea of species and abundance of nudibranchs. Greater sampling effort into destructive day-time and night-time sampling is also predicted to increase the number of species and abundance of nudibranchs found in the Midwest region.
To validate that high species diversity exists in Geraldton, additional, more intensive biogeographical and quantitative studies are required in the sub-region. This should be linked to research on the Leeuwin Current and the influence its processes have on localised areas in an effort to determine if the current is the major influence on dispersal method for nudibranchs that have planktotrophic larvae in the Midwest region.
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7.0 APPENDIX
Appendice 1:
A complete list of all 31 study sites, their GPS location, depth and site code name.
Table 1: Names and GPS coordinates of the sample sites at Geraldton and the Abrolhos Islands, including site code name, if the site is onshore or offshore and the average depth sampling was undertaken
Site Depth Location Survey Site Site Code GPS Coordinates (S; E) (m) Geraldton Port Gergory G11 28 11'2715" 114 14'2328" 2.0 Onshore North Marina 1 G12 28 45'1327" 114 36'5591" 2.5 North Marina 2 G13 28 45'1504" 114 36'5606" 1.5 Seperation Point G14 28 47'2361" 114 35'4389" 1.5 Drummonds G15 28 40'5683" 114 36'2220" 1.5 Lives 1 G51 28 46'371" 114 35'2186" 4.5 Lives 2 G52 28 46'080" 114 35'2211" 5.5 Wallabi Group W/Dick Island W11 28 29'6813" 113 45'2466" 1.5 Offshore S/W Gallows W12 28 28'8836" 113 45'9136" 1.5 W/Wann Island W13 28 28'0849" 113 45'2905" 2.5 Middle Ground W14 28 27'1022" 113 45'0080" 1.5 West Cardinal Marker W51 28 26'5860" 113 44'8144" 8.7 Public Mooring W52 28 27'7298" 113 46'1015" 6.8 Deep Lump Lagoon W53 28 29'0246" 113 45'3336" 6.8 Traitor Island W54 28 29'0299" 113 47'0203" 8.5
Easter Group Leo's E11 28 40'686" 113 52'435" 1.5 Offshore South Nature Strip E12 28 45'146" 113 45'629" 2.5 Middle Marker E13 28 43'1926" 113 47'5547" 1.5 Squid Hole E14 28 44'5509" 113 48'3843" 1.5 Kutas Corner E51 28 46'0388" 113 48'0899" 7.6 Three Sisters E52 28 44'4000" 113 44'0879" 4.1 Kacca Flat E53 28 45'2314" 113 45'2300" 7.1 Dougies Canyon E54 28 41'1950" 113 46'1570" 4.3 Pelsart Group Mid Rocks S11 28 53'9859" 113 55'3613" 2.4 Offshore South Basilie S12 28 53'3732" 113 57'4875" 2.0 Front Basilie S13 28 52'5158" 113 58'0028" 1.5 Public Mooring S14 28 51'419" 114 01'081" 1.5
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Sponge Lump S51 28 53'1001" 113 58'3429" 7.7 East Gergory Island S52 28 53'7245" 114 00'7446" 7.5 Coral Patches S53 28 51'4992" 114 01'1586" 8.0 Coral Patches PM S54 28 51'2219" 114 00'6829" 5.7
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Appendice 2:
Images of the dive site locations at each of the four regions
Figure 2.2: One of the four survey sites in the Geraldton region and the location of the five sampling sites (green balloons are shallow sample sites and green balloons with a dot are deep sample sites) (Google Earth, 2014).
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Figure 2.3: One of the four survey sites at Easter Group in the Abrolhos Islands region showing where the eight sampling sites are located (a pink balloon is a shallow sampling site and a pink balloon with a black dot is a deep sampling site) (Google Earth, 2014).
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Figure 2.4: One of the four survey sites at the Wallabi Group at the Abrolhos Islands region showing where the eight sampling sites are located (Google Earth, 2014).
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Figure 2.5: One of the four survey sites in the Pelsaert Group at the Abrolhos Islands region showing where the eight sampling sites are located (green balloons represent shallow study sites and green balloons with a black dot represent deep sampling sites) (Google Earth, 2014).
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