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
i
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
ii
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
iii
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.
iv
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.
v
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
vi
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
1
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
2
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
3
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
4
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).
5
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
6
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).
7
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
8
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
9
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).
10
Table 1.3: Total number of opisthobranchs found at various locations around the world, in both northern and southern hemispheres (Bennett, 2013).
Locality Total Sampling Period
Average Latitude
No. 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
11
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.
12
Table 1.4: Comparison of diversity estimates of opisthobranchs for surveys this survey and surveys undertaken in similar localities. Adapted from Bennett (2013)
Location
Surveyed
Year Survey Duration No. Species
Dampier
Archipelago
1998
1999
156 hours 90
Montebello Islands 1993 135 hours 63
Murion Islands &
Exmouth Gulf
1996 72 hours 54
Coral Bay 2013 60 hours 56
Bernier and Dorre
Islands
1995 66 hours 55
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
13
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.
14
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.
15
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).
16
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
17
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.
18
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.
19
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).
20
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
21
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
22
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:
23
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).
24
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.
25
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 km
2
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 km
2
0
10
20
30
40
50
60
70
80
Geraldton Easter Wallabi Pelsaert
Nu
mb
er
of
Ind
ivid
ua
ls
Shallow
Deep
0
2
4
6
8
10
12
14
Geraldton Easter Wallabi Pelsaert
Nu
mb
er
of
Sp
eci
es
Shallow
Deep
26
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
27
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.
28
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.
29
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
30
compared to the shallow sites. The shallow survey sites at the Wallabi Group resulted in
the least amount of variability.
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
0.0
1.0
2.0
3.0
4.0
5.0
6.0
7.0
Geraldton Easter Group Wallabi Group Pelsaert Group
Me
an
Nu
mb
er
of
Ind
ivid
ua
ls
Shallow
Deep
31
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.
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
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
Geraldton Easter Group Wallabi Group Pelsaert Group
Me
an
Nu
mb
er
of
Sp
eci
es
Shallow
Deep
32
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.
33
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.
34
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).
Figure 3.6.1: Shannon Weaver diversity index for mean nudibranchs found across the two study regions
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
1.8
2
Geraldton Easter Group Wallabi Group Pelsaert Group
Sh
an
no
n W
ea
ve
r D
ive
rsit
y I
nd
ex
Shallow
Deep
35
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).
36
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.
37
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).
38
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.
39
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
40
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
41
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
42
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
43
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
44
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
45
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
46
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
47
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
48
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
49
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).
50
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
51
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).
52
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.
53
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.
54
6.0 REFERENCE LIST
Aboul-ela, I.A., 1959. On the food of Nudibranchs. Biological Bulletin 117, 439–442.
Aerts, L., 1994. Seasonal distribution of nudibranchs in the Southern Delta Area, S.W.
Netherlands. Journal of Molluscan Studies 60, 129–139.
Aguado, F., Marin, A., 2007. Warning coloration associated with nematocyst-based
defences in Aeolidiodean nudibranchs. Journal of Molluscan Studies 73, 23–28.
Babcock, R., Kelly, S., Shears, N.T., Walker, J.W., Willis, T.J., 1999. Changes in
community structure in temperate marine reserves. Marine Ecology Progress Series
189, 125–134.
Benkendorff, K., Przeslawski, R., 2008. Multiple measures are necessary to assess rarity
in marco-molluscs: a case study from southeastern Australia. Marine Ecology
Research Centre; School of Environment, Science and Engineering 1–50.
Bennett, L.C., 2013. Studies of the diversity, distribution, abundance and feeding ecology
of Opisthobranchia in Coral Bay , Western Australia. Murdoch University.
Bertsch, H., 2010. Nudibranch feeding biogeography: ecological network analysis of inter-
and intra- provincial variations. Thalassas: An International Journal of Marine
Sciences 27, 155–168.
Caputi, N., Fletcher, W.J., Pearce, A., Chubb, C.F., 1996. Effect of the Leeuwin Current
on the recruitment of fish and invertebrates along the Western Australian coast.
Marine and Freshwater Research 47, 147–155.
Caputi, N., Jackson, G., Pearce, A., 2014. Management implications of climate change
effects on fisheries in WA: an example of an extreme event. In: Caputi, N., Jackson,
55
G and Pearce, A. The marine heat wave off Western Australia during the summer of
2010/11 – 2 years on. Western Australia.
Chang, Y.-W., Mok, H.-K., Chen, T.-C., Yu, M.-H., Willan, R.C., 2013. Diel variation
affects estimates of biodiversity and abundance of nudibranch (Gastropoda) faunas.
Nautilus 127, 19–28.
Chavanich, S., Viyakarn, V., Sanpanich, K., Harris, L.G., 2013. Diversity and occurrence
of nudibranchs in Thailand. Marine Biodiversity 43, 31–36.
Chavez, F.P., 2012. Climate change and marine ecosystems. Proceedings of the National
Academy of Sciences of the United States of America 109, 19045–6.
Cheney, K.L., Cortesi, F., How, M.J., Wilson, N.G., Blomberg, S.P., Winters, a E.,
Umanzör, S., Marshall, N.J., 2014. Conspicuous visual signals do not coevolve with
increased body size in marine sea slugs. Journal of evolutionary biology 27, 676–87.
Cobb, G., Mullins, D., 2014. Nudibranchs of the Sunshine Coast, Queensland and
Tasmania, Australia: Indo-pacific nudibranchs. URL
http://nudibranch.com.au/specieslist.html (accessed 30/04/2014).
Coleman, N., 2001. 1001 Nudibranchs: Catalogue of Indo-Pacific sea slugs. Neville
Coleman’s Underwater Geographic Pty Ltd: Queensland, Australia.
Collins, L.B., Zhu, Z.R., Wyrwoll, K.H., 1996. The structure of the Easter Platform ,
Houtman Abrolhos Reefs : Pleistocene foundations and Holocene reef growth 135,
1–13.
Cresswell, G., 1991. The Leeuwin Current - observations and recent models. Journal of
the Royal Society of Western Australia 74, 1–14.
56
Cresswell, G., 1996. The Leeuwin Current near Rottnest Island , Western Australia.
Marine and Freshwater Research 47, 483–487.
Cresswell, G., Domingues, C.M., 2009. Leeuwin current. CSIRO Marine and Atmospheric
Research 444–454.
Debelius, H., Kuiter, R.H., 2007. Nudibranchs of the world. IKAN-Unterwasserarchiv:
Frankfurt, Germany.
Devlin, M.J., Brodie, J., 2005. Terrestrial discharge into the Great Barrier Reef Lagoon:
nutrient behavior in coastal waters. Marine pollution bulletin 51, 9–22.
Domenech, A., Avila, C., Ballesteros, M., 2002. Spatial and temporal variability of the
Opisthobranch molluscs of Port Lligat Bay, Catalonia, NE Spain. Journal of
Molluscan Studies 68, 29–37.
Fahey, S.J., Garson, M.J., 2002. Geographic variation of natural products of tropical
nudibranch Asteronotus cespitosus. Journal of Chemical Ecology 28, 1773–1785.
Faucci, A., Toonen, R.J., Hadfield, M.G., 2007. Host shift and speciation in a coral-
feeding nudibranch. Proceedings of the Royal Society of Biological Sciences 274,
111–119.
Feng, M., McPhaden, M.J., Xie, S., Hafner, J., 2013. La Niña forces unprecedented
Leeuwin Current warming in 2011. Scientific reports 3, 1277.
Feng, M., Slawinski, D., Beckley, L.E., Keesing, J.K., 2010. Retention and dispersal of
shelf waters influenced by interactions of ocean boundary current and coastal
geography. Marine and Freshwater Research 61, 1259–1267.
57
Feng, M., Weller, E., Hill, K., 2009. The Leeuwin Current, In a marine climate change
impacts and adaptation report card for Australia 2009. CSIRO Marine and
Atomospheric Research, NCCARF Publication 05/09.
Fogg-Matarese, S., 2009. The use of cnidarian nematocysts by the Aeolidian nudibranch
Cratena pilata. University of Rhode Island, ProQuest, UMI Dissertations Publishing
3380534.
Garcia, F.J., Bertsch, H., 2009. Diversity and distribution of the Gastropoda
Opisthobranchia from the Atlantic Ocean: A global biogeographical approach.
Scientia Marina 73, 153–160.
García-Matucheski, S., Muniain, C., 2011. Predation by the nudibranch Tritonia odhneri
(Opisthobranchia: Tritoniidae) on octocorals from the South Atlantic Ocean. Marine
Biodiversity 41, 287–297.
Garson, M.J., Chem, F.C., 2004. Chemical associations between Australian nudibranchs
and their dietary sponges. Chemistry in Australia 16–18.
Gaughan, D.J., 2007. Potential mechanisms of influence of the Leeuwin Current eddy
system on teleost recruitment to the Western Australian continental shelf. Deep Sea
Research Part II: Topical Studies in Oceanography 54, 1129–1140.
Gersbach, G.H., Pattiaratchi, C.B., Ivey, G.N., Cresswell, G.R., 1999. Upwelling on the
south-west coast of Australia—source of the Capes Current? Continental Shelf
Research 19, 363–400.
Gochfeld, D.J., Aeby, G.S., 1997. Control of populations of the coral-feeding nudibranch
Phestilla sibogae by fish and crustacean predators. Marine Biology 130, 63–69.
58
Hadfield, M.G., 1987. The Biology of Nudibranch Larvae. Nordic Society Oikos 14, 85–95.
Hatcher, B.G., 1991. Coral reefs in the Leeuwin Current - an ecological perspective.
Journal of the Royal Society of Western Australia 74, 115–127.
Hegge, B., Eliot, I., Hsu, J., Summer, F., Hegget, B., Eliott, I., Hsut, J., 1996. Sheltered
Sandy Beaches of Southwestern Australia. Journal of Coastal Research 12, 748–
760.
Holliday, D., Beckley, L., Millar, N., Olivar, M., Slawinski, D., Feng, M., Thompson, P.,
2012. Larval fish assemblages and particle back-tracking define latitudinal and cross-
shelf variability in an eastern Indian Ocean boundary current. Marine Ecology
Progress Series 460, 127–144.
Hoover, R. A., Armour, R., Dow, I., Purcell, J.E., 2012. Nudibranch predation and dietary
preference for the polyps of Aurelia labiata (Cnidaria: Scyphozoa). Hydrobiologia
690, 199–213.
Hughes, L., 2003. Climate Change and Australia : trends, projections and impacts. Austral
Ecology 28, 423–443.
Hutchins, J.B., Pearce, A.F., 1994. Influence of the Leeuwin Current on recruitment of
tropical reef fishes at Rottnest Island, Western Australia. Bulletin of Marine Science
54, 245–255.
IPCC, 2007. The physical science basis, Contribution of working group I to the Fourth
Assessment, Report of the Inertgovernmenral Panel of Climate Change. Cambridge
University Press, Cambridge, United Kingdom and New York 996.
Johnson, C.R., Banks, S.C., Barrett, N.S., Cazassus, F., Dunstan, P.K., Edgar, G.J.,
Frusher, S.D., Gardner, C., Haddon, M., Helidoniotis, F., Hill, K.L., Holbrook, N.J.,
59
Hosie, G.W., Last, P.R., Ling, S.D., Melbourne-Thomas, J., Miller, K., Pecl, G.T.,
Richardson, A.J., Ridgway, K.R., Rintoul, S.R., Ritz, D.A., Ross, D.J., Sanderson,
J.C., Shepherd, S.A., Slotwinski, A., Swadling, K.M., Taw, N., 2011. Climate change
cascades: Shifts in oceanography, species’ ranges and subtidal marine community
dynamics in eastern Tasmania. Journal of Experimental Marine Biology and Ecology
400, 17–32.
Johnson, R.F., Gosliner, T.M., 2012. Traditional taxonomic groupings mask evolutionary
history : A molecular phylogeny and new classification of the Chromodorid
nudibranchs. PLoS ONE 7, e33479.
Jörger, K.M., Schrödl, M., Schwabe, E., Würzberg, L., 2014. A glimpse into the deep of
the Antarctic Polar Front – Diversity and abundance of abyssal molluscs. Deep Sea
Research Part II: Topical Studies in Oceanography 108, 93–100.
Kay, A.E., Young, D.K., 1969. The Doridacea (Opisthobranchia; Mollusca) of the
Hawaiian Islands. Pacific Science 23, 172–231.
Kelmo, F., Attrill, M.J., Gomes, C.T., Jones, M.B., 2004. El Nino induced local extinction
of coral reef bryozoan species from Northern Bahia, Brazil. Biological Conservation
118, 609–617.
Lambert, W.J., 1991. Coexistence of hydroid-eating nudibranchs: recruitment and non-
equilibrial patterns of occurence. Journal of Molluscan Studies 57, 35–47.
Lambert, W.J., 1991. Coexistence of hydroid eating nudibranchs: Do feeding biology and
habitat use matter? Biological Bulletin 181, 248–260.
Levin, L.A., 2006. Recent progress in understanding larval dispersal: New directions and
digressions. Oxford University Press 46, 282–297.
60
Lock, K., Newman, P., Burton, M., Pn, P.N., Kl, K.L., Mb, M.B., Camplin, M., Bernard,
M.C., Bp, P., Bullimore, R., Ab, A.B., Archer, J., Jat, T., Fk, F.K., 2010. Skomer
Marine Nature Reserve Nudibranch Diversity Survey 2010, CCW Regional Report
10/11.
Martin, R., Tomaschko, K., Walther, P., 2006. Protective skin structures in shell-less
marine gastropods. Marine Biology International Journal on Life in Oceans and
Coastal Waters.
McCuller, M.I., 2012. The influence of abiotic and biotic factors on two nudibranchs
feeding upon Membranipora membranacea in the Southern Gulf of Maine. Masters
Abstracts International. 51, 84.
Morgan, G.J., Wells, F.E., 1991. Zoogeographic provinces of the Humboldt, Benguela and
Leeuwin Current systems. Journal of the Royal Society of Western Australia 74, 59–
69.
O’Hara, T.D., 2002. Endemism, rarity and vulnerability of marine species along a
temperate coastline. Invertebrate Systematics 16, 671–684.
Olsen, D.A., Hayes, J.W., Booker, D.J., Barter, P.J., 2014. A model incorporating
disturbance and recovery processes in benthic invertebrate habitat - flow time series.
River Research and Applications 30, 413–426.
Pattiaratchi, C., Woo, M., 2009. The mean state of the Leeuwin Current system. Journal
of the Royal Society of Western Australia 92, 221–241.
Pearce, A.F., 1991. Eastern Boundary Currents of the southern hemisphere. Journal of
the Royal Society of Western Australia 74, 35–45.
61
Pearce, A.F., 1997. The Leeuwin Current and the Houtman Abrolhos Islands in: The
marine flora and fauna of the Houtman Abrolhos Islands, Western Australia.
Proceedings from the 7th Internations Marine Biological Workshop, Western
Australian Museum, Perth, 11-46.
Pearce, A.F., Feng, M., 2013. The rise and fall of the “marine heat wave” off Western
Australia during the summer of 2010/2011. Journal of Marine Systems 111-112,
139–156.
Pearce, A.F., Pattiaratchi, C., 1999. The Capes Current : a summer countercurrent flowing
past Cape Leeuwin and Cape Naturaliste , Western Australia. Continental Shelf
Research 19, 401–420.
Pearce, A.F., Rossbach, M., Tait, M., Brown, R., 1999. Sea temperature variability off
Western Australia 1990 to 1994, Fisheries Research Report No. 111.
Pearce, A.F., Slawinski, D., Feng, M., Hutchins, B., Fearns, P., 2011. Modelling the
potential transport of tropical fish larvae in the Leeuwin Current. Continental Shelf
Research 31, 2018–2040.
Pechenik, J.A., 1999. On the advantages and disadvantages of larval stages in benthic
marine invertebrate life cycles. Marine Ecology Progress Series 177, 269–297.
Perry, A.L., Low, P.J., Ellis, J.R., Reynolds, J.D., 2005. Climate change and distribution
shifts in marine fishes. Science 308, 1912–1915.
Phillips, J.C., Huisman, J.M., 2009. Influence of the Leeuwin Current on the marine flora
of the Houtman Abrolhos. Journal of the Royal Society of Western Australia 92, 139–
146.
62
Pielou, E.E., 1966. The measurement of diversity in different types of biological
collections. Journal of Theoretical Biology 13, 131–144.
Przeslawski, R., Ahyong, S., Byrne, M., Wörheide, G., Hutchings, P., 2008. Beyond corals
and fish: the effects of climate change on noncoral benthic invertebrates of tropical
reefs. Global Change Biology 14, 2773–2795.
Richardson, A.J., Bakun, A., Hays, G.C., Gibbons, M.J., 2009. The jellyfish joyride:
causes, consequences and management responses to a more gelatinous future.
Trends in Ecology & Evolution 24, 312–322.
Rogers, C.S., 1993. Hurricanes and coral reefs: The intermediate disturbance hypothesis
revisited. Coral Reefs 23, 127–137.
Rudman, W.B., 1984. The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-
West Pacific: a review of the genera. Zoological Journal of the Linnean Society 81,
115–273.
Rudman, W.B., 1991. Purpose in Pattern: The Evolution of Colour in Chromodorid
Nudibranchs. Journal of Molluscan Studies 57, 5–21.
Rudman, W.B., 1998. Australian Museum’s sea slug forum: Chromodoris westraliensis].
URL http://www.seaslugforum.net/showall/chrowest (accessed 26/10/2014).
Rudman, W.B., 2010. Australian Museum’s sea slug forum. URL
http://www.seaslugforum.net/ (accessed 30/04/2014).
Rykiel, E.J., 1985. Towards a definition of ecological disturbance. Australian Journal of
Ecology 10, 361–365.
63
Scheffers, A.M., Scheffers, S.R., Kelletat, D.H., Squire, P., Collins, L., Feng, Y., Zhao, J.-
X., Joannes-Boyau, R., May, S.M., Schellmann, G., Freeman, H., 2012. Coarse clast
ridge sequences as suitable archives for past storm events? Case study on the
Houtman Abrolhos, Western Australia. Journal of Quaternary Science 27, 713–724.
Shannon, C.E., Weaver, W., 1963. The Mathematical Theory of Communication, Physics
Today. University of Illinois: Urbana.
Smale, D.A., Wernberg, T., 2012. Ecological observations associated with an anomalous
warming event at the Houtman Abrolhos Islands, Western Australia. Coral Reefs 31,
441.
Thompson, T.E., 1958. The naural history, embryology, larval biology and post-larval
development of Adalaria proxmia. Philosophical Transactions of the Royal Society of
London. Series B. Biological Sciences 242, 1–57.
Todd, C.D., 1981. The ecology of nudibranch molluscs. Oceanography and Marine
Biology, Annual Review 19, 141–234.
Todd, C.D., Lambert, W.J., Thorpe, J.P., 1998. The genetic structure of intertidal
populations of two species of nudibranch molluscs with planktotrophic and pelagic
lecithotrophic larval stages: Are pelagic larvae “for” dispersal? Journal of
Experimental Marine Biology and Ecology 228, 1–28.
Trickey, J.S., Vanner, J., Wilson, N.G., 2013. Reproductive variance in planar spawning
Chromodoris species (Mollusca: Nudibranchia). Molluscan Research 33, 265–271.
Valdes, A., Ornelas-Gatdula, E., Dupont, A., 2013. Colour pattern variation in a shallow-
water species of Opisthobranch Mollusc. Biological Bulletin 224, 35–46.
64
Waite, A.M., Thompson, P.A., Pesant, S., Feng, M., Beckley, L.E., Domingues, C.M.,
Gaughan, D., Hanson, C.E., Holl, C.M., Koslow, T., Meuleners, M., Montoya, J.P.,
Moore, T., Muhling, B.A., Paterson, H., Rennie, S., Strzelecki, J., Twomey, L., 2007.
The Leeuwin Current and its eddies: An introductory overview. Deep Sea Research
Part II: Topical Studies in Oceanography 54, 789–796.
Watling, L., Norse, E.A., 1998. Disturbance of the seabed by mobile fishing gear: A
comparison to forest clearcutting. Conservation Biology 12, 1180–1197.
Watson, D.L., Harvey, E.S., 2009. Influence of the Leeuwin Current on the distribution of
fishes and the composition of fish assemblages. Journal of the Royal Society of
Western Australia 92, 147–154.
Wells, F.E., Bryce, C.W., 1993. Sea slugs of Western Australia. Western Australian
Museum: Perth, Western Australia.
Westera, M.B., Phillips, J.C., Coupland, G.T., Grochowski, A.J., 2009. Sea surface
temperatures of the Leeuwin Current in the Capes region of Western Australia :
potential effects on the marine biota of shallow reefs 197–210.
World Register of Marine Species. World Register of Marine Species taxon tree. URL
http://www.marinespecies.org/aphia.php?p=browser&id=412569&expand=true#ct
(accessed 21/10/2014).
Yong, K.W.L., Salim, A. a., Garson, M.J., 2008. New oxygenated diterpenes from an
Australian nudibranch of the genus Chromodoris. Tetrahedron 64, 6733–6738.
65
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
Location Survey Site Site Code GPS Coordinates (S; E) Site Depth
(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
66
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
67
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).
68
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).
69
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).
70
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).
Top Related