The Ecology of Cleaning Stations Used by Manta Alfredi in Ningaloo Reef, Western Australia

Home , Butterflyfish, Cleaning station, Cleaning symbiosis, False cleanerfish

The ecology of cleaning stations used by Manta alfredi in Ningaloo Reef, Western Australia

Hannah Ashe

School of Veterinary and Life Sciences

This thesis is presented as part of the requirements for the Degree of Bachelor of Science in Marine Sciene with Honours at Murdoch University.

2016

Declaration

I declare this thesis is my own account of my research and contains as its main content work which has not been previously submitted for a degree at any tertiary education

institution.

Hannah Ashe Acknowledgements There are many people I would like to acknowledge for their support and assistance throughout this year. Most importantly, thank you my supervisor Dr. Mike van Keulen for giving me the opportunity to take on such a wonderful project, and patience through the long lists of questions I always have. Frazer McGregor for his extensive manta ray knowledge and the time he dedicated to the fieldwork; without the two of you, this project would not have been possible.

Thank you to the amazing crew of Ningaloo Marine Interactions (Frazer, Peta, Karen,

Anna, Tom, and Lea), for welcoming me into your family as well as support and encouragement while out on the water. A special thanks to Karen for being my assistant when I needed extra help and enthusiasm to be a part of this project.

I would like to thank Alex Thornton for devoting your time to help watch the endless supply of videos. My thanks also go out to Nathan Beerkens for his eagerness and endless determination to identify some of the more pesky fish species, and James

Tweedley for his statistical expertise, for without it I would be lost. Special thanks to

Angus Lawrie for always having time to help me, and keeping me sane through the final weeks of this project. Finally to my family and friends who kept me calm when I was stressed and the infinite supply of encouragement for which I am the most grateful for.

iii

Abstract Cleaning stations, where fish are cleaned of their parasites, are one of the many microhabitats found within reef systems. This study was a preliminary evaluation of the ecology of three cleaning stations in Bateman Bay, Western Australia. Bateman

Bay is located just north of Coral Bay and home to a diverse range of species, notably the resident Reef Manta Ray (Manta alfredi). To do this, all fish species within the selected cleaning stations were identified, quantified and their behaviours recorded through video analysis. Over five months, a total of 144 different species were identified from 37 families, totalling over 3,800 individuals. Species richness and diversity significantly differed among sites (p < 0.05). Behaviours of species also showed trends of each cleaning station being used for different purposes. Feeding was most commonly seen at the Point Maud South (PMS) station, while the Point Maud

North (PMN) station experienced the most cleaning events. The third site, the Oyster

Bridge (OB) station experienced many individuals roaming around the area. However,

46 species were seen at all three locations, detecting similarities in species composition to some degree at each cleaning station; e.g. M. alfredi was cleaned at each location. From this information, motives for site preference cannot be conclusively determined; however results show environmental factors such as food availability may influence species abundance, composition and behaviours at cleaning stations.

Table of Contents

Table of Contents Acknowledgements ...... iii Abstract ...... iv Table of Contents ...... vi 1.0 Introduction ...... 1 1.1 Reef ecology ...... 1 1.2 Cleaning stations ...... 2 1.2.1 Origin of a cleaner ...... 3 1.2.2 Cleaner diversity ...... 3 1.2.3 Cleaning process ...... 4 1.2.4 Cleaner copycats ...... 6 1.2.5 Diet ...... 7 1.2.6 A symbiotic relationship? ...... 7 1.2.7 Costs and benefits ...... 9 1.3 Manta rays ...... 10 1.3.1 Species description ...... 11 1.3.2 Identification ...... 13 1.3.3 Feeding ...... 14 1.3.4 Movements ...... 15 1.3.5 Cleaning ...... 15 1.3.6 Vulnerability ...... 17 1.3.7 Ecotourism and towards sustainability ...... 18 1.4 Ningaloo Marine Park ...... 20 1.4.1 Tourism ...... 21 1.4.2 Coral Bay ...... 21 1.5 Aims and objectives ...... 22 2.0 Materials and Methods ...... 24 2.1 Study sites ...... 24 2.2 Data collection...... 27 2.3 Station uses ...... 28 2.4 Analyses ...... 28

2.4.1 Video analyses ...... 28 2.4.2 Data analyses ...... 29 3.0 Results ...... 30 3.1 Point Maud South...... 46 3.2 Point Maud North ...... 46 3.3 Oyster Bridge ...... 46 3.4 Cleaning ...... 47 3.5 Manta sightings ...... 47 4.0 Discussion ...... 48 4.1 Station diversity ...... 48 4.2 Station uses ...... 48 4.2.1 Point Maud South ...... 49 4.2.2 Point Maud North ...... 50 4.2.3 Oyster Bridge ...... 51 4.3 Common species ...... 52 4.4 Large clients ...... 53 4.5 Targeted species ...... 54 4.6 Limitations and future research considerations ...... 55 4.7 Conclusion ...... 56 5.0 References ...... 58

1.0 Introduction The function of coral reef ecosystems and how they have succeeded for millions of years is not attributed to one species, but the interactions of many. Ecology focuses on the broad understanding of relationships between organisms and their environment such as coral reefs, and their associated fauna (Bellwood and Wainwright 2002).

Although a healthy reef is historically measured by its percentage of coral cover (Bell and Galzin 1984), it is important to also consider the functional groups, ecosystem processes and feedbacks (Hughes et al. 2010).

1.1 Reef ecology Integral for many sedentary and mobile marine organisms, corals provide services such as shelter, food and substrates for attachment (Cole et al. 2008). Habitat complexity and rugosity also play a role in fish assemblages; a reef with various shelters will harbour a greater diversity of local fishes (Friedlander and Parrish 1998). Corallivorous species like the Crown-of-thorns starfish, Acanthaster planci or the Pebbled

Butterflyfish, Chaetodon multicinctus rely on hard corals as part of their diet (Glynn

1974, Gochfeld 2004). Smaller fish inhabiting coral reefs also provide a food source for many mid-trophic-level piscivores and top predators (Hixon 2015, Roff et al. 2016).

Parrotfish and damselfish are found along many tropical coral reefs, accounting for a large percentage of the herbivore population (Bellwood and Hughes 2001). This functional group provides a service to coral reefs on many levels by grazing on macroalgae (Mumby et al. 2006). Without herbivores, reefs can experience an overgrowth of macroalgae, blocking out sunlight which prevents the recruitment of juvenile corals, and promoting coral disease (Carpenter and Edmunds 2006). In a study on the Great Barrier Reef, herbivores were removed from an area for three years

(Bellwood et al. 2006). As a result of the exclusion, Sargassum growth reached 2 m, reducing coral recruitment by over half.

1.2 Cleaning stations Various microhabitats exist along reefs comprising of species networks essential in maintaining fish and reef health. Cleaning stations are areas where marine animals visit to have their surfaces freed of unwanted biotic matter by specialised individuals knowns as cleaners (Losey 1972). The interspecific interaction of being cleaned in an aquatic environment has been widely studied, involving the symbiotic relationship between two categories of animal, cleaner and client (Limbaugh 1961, Hobson 1971,

Losey 1972, Arnal et al. 2001, Bansemer et al. 2002, Clague et al. 2011, Sun et al. 2016).

Two forms of cleaning exist; the first is known as incidental or facultative cleaning

(Losey et al. 1994). In these cases, the cleaner does not clean the client for the sake of doing so, but instead feeds opportunistically. Surgeonfish are herbivores and known to pick off algae from turtle shells and body surfaces which in turn, can reduce drag produced by its build-up (Sazima et al. 2010). Observations have also been made of ocean sunfish remaining at the water’s surface to allow albatrosses to feed on their ectoparasites (Abe et al. 2012).

A second and more widely studied form of cleaning involves the removal of ectoparasites, diseased or injured tissue, mucus or scales from a client by a specially evolved individual (Losey 1972, Grutter 1997, Côté 2000, Arnal et al. 2001). Cleaner species vary from shrimps to fishes (Guimarães et al. 2007), and are located in habitats referred to as cleaning stations (Losey 1972). Cleaning stations are seen in various aquatic environments from temperate kelp habitats (Hobson 1971, Arnal and Morand

2001) to freshwater (Abel 1971, Severo-Neto and Froehlich 2016). However, most

2 stations are typically located in tropical coral reefs (Luiz et al. 2016). Visitors to cleaning stations, referred to as clients, are inspected and potentially cleaned by the cleaners.

Clients range from herbivorous damselfish (Cheney and Côté 2001), to megafauna such as manta rays and predatory sharks (O'Shea et al. 2010). An active habitat, some client species will actively make multiple visits, with a frequency ranging between 12 – 144 times per day (Grutter 1995). A single cleaner fish along the Great Barrier Reef can average 2,287 clients per day, providing them with a continuous and abundant food source (Grutter 1996b).

1.2.1 Origin of a cleaner Cleaning behaviour is considered a fairly recent evolutionary development, with some of the earliest evidence within the last 20 million years, but the majority from the past

10 million years (Baliga and Law 2015). Diversification of coral reefs in shallow-water marine systems is shown to be at its most prominent from the late Eocene through the early Miocene. Evidence of diversification in one of the most abundant cleaner families, Labridae, almost doubled during the Miocene; suggesting that the presence of reefs promoted diversification in the family (Baliga and Law 2015).

1.2.2 Cleaner diversity Over 100 teleost fish species have been classified as cleaners (Côté 2000). All crustaceans known to clean are found in the Order Decopoda; over 40 species have been recorded thus far, falling within 20 different genera (Becker and Grutter 2004).

Cleaners can be divided into two separate categories: facultative and obligate.

Facultative cleaners, as noted above, predominantly clean as juveniles, and can find other sources for feeding, therefore not dependent on cleaning alone for survival (Côté

2000). Obligate cleaners rely on cleaning for most, if not all, of their food resources.

Gobiidae and Labridae are among the most notable cleaning families of teleost fishes

(Côté 2000). Eight goby species have been identified as cleaners thus far and are predominantly found in tropical waters, occupying coral heads and sponges (Arnal and

Côté 1998, Whiteman and Côté 2002). They can be found solitary at a station, in male- female pairs, or groups up to 40 individuals (Whiteman and Côté 2002). The most studied cleaners however, belong to the family Labridae; with 58 species currently known to participate in cleaning behaviour at some life stage (Baliga and Law 2015).

Labroides dimidiatus (Common Cleanerfish) for example, is a widespread and well- studied cleaner (Randall 1958, Bshary and Würth 2001, Clague et al. 2011), found to clean on average 4.8 parasites per minute of inspection (Grutter 1996b).

1.2.3 Cleaning process The cleaning process has many steps involved, beginning with the visual identification of a cleaner or client by colouration or certain poses used to advertise. Once acknowledged, the cleaner inspects potential clients, deciding whether or not to commence cleaning. Used by a variety of species, cleaning interactions are an important process used to reduce ectoparasite loads and assist the healing progression from a prior injury (Sazima et al. 1998, Marshall and Bennett 2010a).

Prior to an interaction, clients use visual cues to seek out cleaners and cleaning stations

(Losey 1974, Stummer et al. 2004, Huebner and Chadwick 2012). In Puerto Rico, the combination of spherical coral heads, and the presence of the wrasse Thallasoma bifasciatum are used by clients for identifying the locations of a cleaning goby (Losey

1974). Size and length of lateral stripes is also used by clients to determine suitable cleaners (Stummer et al. 2004). The reef fish visual system is poor, with objects becoming blurry between 1 and 5 m (Marshall 2000); therefore it is suggested the

4 larger and bolder stripes allow for detection from a greater distance due to the amplified contrast against the cleaning station habitat.

Once clients approach the cleaning stations, advertisement is used to solicit service

(Losey 1972). For a cleaner fish, this involves a ‘dance’ where they swim in a zig-zag pattern in the water column (Côté 2000). Cleaners use this behaviour more frequently when exposed to piscivorous fish, regardless of parasite levels (Grutter 2004). This is known as ‘preconflict management behaviour’; thought to be used to avoid negative interactions with potentially dangerous clients. Advertisement can be accompanied with tactile stimulations across the surface of the client’s body, generally avoiding the head region (Sazima et al. 1998).

Alternatively, clients can solicit their need for service by posing (Losey 1972, Côté et al.

1998, Côté 2000, Arnal et al. 2001). Generally species-specific, posing entails variations of gill flaring, head- or tailstands and flaring of the fins. For example, Chromis punctipinnis (Blacksmith Fish) will cease swimming, flare its fins and remain motionless in either a head- or tail-down position (Hobson 1971). In larger species, the posing behaviour can include reduced swimming speed with flared gills and body angle tilted slightly upwards as they circle the station (Homma et al. 1999, Dewar et al. 2008,

Oliver et al. 2011). Posing frequency has also been shown to increase with greater parasite loads (Grutter 2004), and clients who pose can increase their chances of being cleaned (Côté et al. 1998). Not all fish pose, suggesting that clients who are already preferred by cleaners do not need to pose to be cleaned (Bansemer et al. 2002).

Although some species have been shown to be more frequent clients of cleaners, others are cleaned rarely if at all (Hobson 1971, Bshary and Grutter 2002, Dewar et al.

2008).

1.2.4 Cleaner copycats Cleaners are identified by their clients from afar by their appearance as well as movements; some non-cleaner species who have the ability to mimic a cleaner’s colour and mechanisms for advertisement take advantage of this (Springer and Smith-Vaniz

1972). Individuals will ‘trick’ clients by performing similar dances, but instead of cleaning will bite the host, consuming scales and tissue (Springer and Smith-Vaniz

1972, Randall 2005). Aspidontous taeniatus (Indo-Pacific Fangblenny), has evolved the same colour pattern as the Labroides dimidiatus (Common Cleanerfish) (Côté, 2000;

Figure 1).

Figure 1. The (a) cleaner Labroides dimidiatus and (b) its mimic Aspidontus tarniatus (Randall, 2005).

The colour patterns of mimics have been found to be temporary; e.g. when removed from the presence of cleaner fish, Plagiotremus rhinorhinchos (Bluestriped Fangblenny) reverted back to its original colouration, dropping its success rate of biting clients by

20% (Randall 2005). Another method used by mimics for biting clients involves the use of nearby cleaner species to increase the likelihood of feeding; the presence of L. dimidiatus attracts clients, therefore P. rhinorhinchos increases its striking rate to 80% when in proximity to the cleaner (Côté and Cheney 2004). Although this adaptation can benefit mimics, clients have been documented to leave the cleaning station after identifying a mimic, causing a negative interaction for all parties involved (Côté 2000).

1.2.5 Diet of cleaners Once the cleaner has chosen a client, it will examine the body surface by swimming close to the client. After inspection, cleaners will either choose to commence cleaning or swim away (Bshary and Schäffer 2002). During cleaning the client’s body surface including inside the mouth, buccal cavity and pharyngeal chamber will be inspected

(Baliga and Law 2015). Ectoparasites account for the majority a cleaner fish’s diet, in particular larval gnathiid isopods and parasitic copepods (Losey 1974, Arnal and

Morand 2001). Cleaner fish are able to consume up to 1,200 parasites per day, depending on the food availability and client visitations (Grutter 1999).

Mucus on the epithelial surface of the client is also consumed by cleaners. It is energy- rich, containing lipids, calories and carbohydrates; and offers great nutritional value

(Arnal and Morand 2001). Different fish species produce various types of mucus; the parrotfish Chlorurus sordidus has thick and opaque mucus, while the snapper Lutjanus fulviflamma has mucus which is clear, slimy and more watery in consistency (Grutter and Bshary 2004).

1.2.6 A symbiotic relationship? Studies suggest that cleaners gain a food source by foraging on the clients, and clients rid themselves of parasites, therefore cleaning is a mutually beneficial relationship

(Becker and Grutter 2004). When the gut contents of L. dimidiatus were examined in a region with high parasite loads, they contained large quantities of parasites and so suggested a mutualistic interaction (Grutter 1997). However, some studies have shown that even with all cleaners removed, the parasite loads on clients are not affected; therefore indicating a commensal relationship i.e. the client benefits but the host is not affected (Losey 1972, Grutter 1996a, 1997).

Mucus protects fish from parasites and can reduce friction during swimming, important for their overall wellbeing (Arnal and Morand 2001). When a cleaner consumes large amounts of mucus over multiple visits, it causes the client to expend more energy to replenish the mucus. In areas with fewer ectoparasites, cleaners are known to ingest more mucus than ectoparasites (Grutter 1997, Bansemer et al. 2002).

This interaction becomes more commensal or parasitic and is referred to as ‘cheating’

(Grutter 1997, Bansemer et al. 2002). In an attempt to terminate this negative interaction, the client will jerk away or act aggressively towards the cleaner (Bshary et al. 2008, Soares et al. 2008). This is suggested to be a mechanism used by clients to control cleaner behaviour and reduce the consumption of mucus or scales.

Clients who have a wide home range that encompasses multiple cleaning stations, are considered ‘choosy’ (Bshary and Noë 2003); another example of a mutualistic relationship, controlling cleaners to lessen the likliehood of them cheating. If clients have the option of selecting between multiple stations, they are more likely to return to the same cleaning station if their most recent interaction was a positive one (Bshary and Schäffer 2002). This is reflected in cleaners giving first priority to choosy clients over those with solitary access to the one station (Bshary 2001, Bshary and Noë 2003).

Studies have shown manta rays exhibit site fidelity to cleaning stations, with many visiting the same cleaning stations multiple days in a row (Dewar et al. 2008, Marshall et al. 2009, Couturier et al. 2011). If the client had to queue for service or experienced cheating, i.e. a negative interaction, their return rate dropped significantly (Bshary

2001). Cleaning stations with pairs of cleaners were found to be the most frequented, providing a higher quality of service (Bshary and Schäffer 2002, Bshary et al. 2008).

1.2.7 Costs and benefits Ectoparasites can cause disease, decreasing their reproductive success as well as weakening the host, making them vulnerable to predation (Lafferty and Morris 1996,

Moller et al. 1999). Cleaning therefore can be beneficial, providing cleaners with a source of food and clients with a reduction in parasites; however, both run the risk of interactions becoming negative and at a cost. These costs however do not outweigh the net gain, exhibited by the existence of cleaning stations in many different habitats, and involving a variety of species.

Although results vary, cleaning has been shown to significantly reduce ectoparasite quantities, with one study showing a reduction in parasite density by four to five times on clients (Grutter 1999, Cheney and Côté 2001). After two weeks without cleaners present, clients accumulated an average of 3.8 times more gnathiids than those who were able to interact with cleaners (Grutter 1999). These benefits are supported with evidence of clients with greater ectoparasite loads frequenting cleaning stations more often, and in some instances, being preferred to those with reduced ectoparasite loads

(Arnal et al. 2001, Soares et al. 2007). Cleaning has also been found to reduce stress in their clients (Bshary and Noë 2003); those without access to cleaner fish in their natural habitat and are unable to travel for services, experienced greater stress responses when captured than individuals with access. Other benefits, not only to the cleaner or client, are those to coral reefs. The presence of cleaners has been proven to increase the total abundance, individual growth and diversity of reef fish (Bshary 2003,

Clague et al. 2011, Sun et al. 2016).

Proposed costs to clients during a cleaning interaction include: exposure to attack while searching for cleaners, intruders to their territories and the possibility of being

‘cheated’ on by the cleaner (Cheney and Côté 2001). For territorial fish like Stegastes diencaeus (Longfin Damselfish), an increase in attacks by other damselfish corresponded to distance travelled outside their territory in search for cleaning if no stations were located in their area (Cheney and Côté 2001). This could be due to increased aggression in damselfish with cleaning stations in their territories and aggression towards all intruders, regardless if their purpose was solely for cleaning

(Cheney and Côté 2001).

Cleaners also run the risk of being eaten or attacked while providing a service to predatory clients (Francini–Filho et al. 2000). Although it is believed there are ways to prevent predations such as tactile stimulation and priority over other clients, instances of predation have still transpired (Côté 2000). Francini-Fiho et al. (2000) documented predation on the cleaner wrasse Thalasomo noronhanum by its grouper client

Cephalopholis fulva. Despite the risks associated with cleaning predatory clients, cleaners were not shown to prefer safer clients; cleaning gobies in fact show preferential treatment to dangerous clients (Soares et al. 2007).

1.3 Manta rays Manta alfredi (Reef Manta Ray) is a reliable client, showing evidence of site fidelity

(Homma et al. 1999, Marshall et al. 2009, Couturier et al. 2011). Research of such behaviours has resulted in the use of cleaning stations for ecotourism; a form of tourism with ecological principles and aims to support the destination’s local resources, operators, guides and other occupations (Sirakaya et al. 1999). Visiting cleaning stations on manta ray dives and snorkels is a lucrative industry, valued at US

$73 million annually across 23 countries (O'Malley et al. 2013).

1.3.1 Species description Sharks and rays belong to the subclass Elasmobranchii. Family Mobulidae comprises of the devil rays, which includes eleven species (Dewar et al. 2008). A distinctive feature of the family is two cephalic lobes which extend from the head. These lobes can be manipulated in shape, to unfurl and form a tunnel for feeding, or curled up for travelling. Within this family are two genera, Mobula and Manta; Manta ays differ from the Mobula genus by their mouths, positioned forward instead of ventrally

(Homma et al. 1999).

Although they are the largest member of the Mobulidae family, there has been relatively little research on manta rays until recently. One significant scientific discovery was recognition of the previously thought single species, Manta birostris, to in fact be two distinct species of manta rays, M. alfredi and M. birostris (Marshall et al.

2009). Manta alfredi (Reef Manta Ray) is found in shallower habitats closer to shore.

They range in size from 3.6 to 5.5 m from wingtip to wingtip, with typically a darker dorsal surface and lighter ventral surface. Manta alfredi can been identified by white markings which make a curved y-shape on its dorsal surface, as well as ventral spot patterns between gill slits, and across the body (Marshall et al. 2009; Figure 2a,b).

a) b)

Figure 2. Manta alfredi viewed from the (a) dorsal and (b) ventral side.1

A melanistic form of manta ray has also been seen (Homma et al. 1999, Marshall et al.

2009, Deakos 2010). They are entirely black on the dorsal side (Figure 3a) which continues to the ventral surface where white patches are present between the gills and its abdominal area (Figure 3b) with on occasion, white patches where the gills end and wings begin. Much less common is albino manta rays, they are almost entirely pale with black accent patterns on their dorsal side, instead of white (Marshall et al. 2009).

a) b)

Figure 3. Melanistic colouration of the reef manta ray (Manta alfredi) viewed from the (a) dorsal and (b) ventral side.

Manta birostris (Oceanic Manta Ray) is larger in size, reaching over 7m (Homma et al.

1999). Unlike M. alfredi they have a more geometric shape of shoulder patch markings on the dorsal surface (Figure 4a) and dark-coloured bands present on the posterior edge of the pectoral fins on the ventral surface (Marshall et al. 2009; Figure 4b).

Typically inhabiting pelagic waters, M. birostris has a distinctive calcified mass where a spine is embedded just below the dorsal fin and ventral pigmentation is near the lower abdominal area. Although rare, micro-sympatry has been suggested with sightings of both species in the same area documented, possibly attributed to high productivity

(Mourier 2012).

1 All images, unless stated otherwise are photo credits of the author. 12

Figure 4. Manta birostris viewed from (a) dorsal and (b) ventral sides (U.S. Fish and Wildlife Service 2016; National Marine Sanctuaries 2013).

Manta alfredi (hereafter referred to as manta ray), are found in the tropical and subtropical regions of the Pacific, Atlantic and Indian Oceans but do not tend to travel into temperate waters north or south of 30 ° latitude (Marshall et al. 2009, Couturier et al. 2012). They are commonly seen off the coasts of Australia, Hawaii, Yap, Maldives,

Indonesia, Japan, South Africa, Mozambique, Brazil and French Polynesia (Homma et al. 1999, Yano et al. 1999, Dewar et al. 2008, Luiz Jr et al. 2009, Marshall et al. 2009,

Deakos 2010, Anderson et al. 2011, Jaine et al. 2012, Mourier 2012). To date, the largest number of individually identified M. alfredi is found in the Maldives with 1,835 recorded individuals (Kitchen-Wheeler et al. 2012).

1.3.2 Identification Researchers have discovered the spot patterns on the ventral side of the manta ray is unique for each individual and has become a non-invasive and useful tool to track new and reoccurring individuals over time (Homma et al. 1999, Dewar et al. 2008, Kitchen-

Wheeler 2010, Marshall and Bennett 2010b, Couturier et al. 2012). Site fidelity is the reutilisation or return of an animal to a previously occupied area for social interactions, territoriality, breeding, or the use of resources (Giuggioli and Bartumeus 2012).

Tracking manta rays has provided evidence of site fidelity and return visits to the same

13 areas for several consecutive days at a time (Dewar et al. 2008). Over longer periods, they have also been found to inhabit the same general areas, revealing residency patterns. The photographic collection of ventral spot patterns, over time, can build inferences on population dynamics, patterns of reoccurrences and male-female ratios

(Kitchen-Wheeler et al. 2012).

1.3.3 Feeding Mantas are planktivorous, feeding almost exclusively on zooplankton (Marshall et al.

2009, Deakos 2010, Couturier et al. 2012). During feeding, the mantas will unfurl their cephalic lobes to assist in funnelling plankton into their open mouths. Small projections on their gills called gill-rakers will filter and catch food while swimming through the water column, also known as ram filter feeding. The abundance and distribution of zooplankton in the water are thought to influence the behaviours and group sizes of feeding manta rays (Osada 2010, McCauley et al. 2014). Feeding has been shown to increase with higher chlorophyll a concentrations, new moon and just after the high tide (Anderson et al. 2011, Jaine et al. 2012). It is suggested the strong currents bring in greater amounts of nutrient-rich waters, attracting mantas to a site (Anderson et al.

2011, Armstrong et al. 2016).

Depending on the environment and plankton densities, manta rays can execute various feeding behaviours such as: repeated backwards summersaults (barrel rolling) (Deakos

2010; Figure 5) circular swimming along a horizontal plane (Gadig and Neto 2014), and moving back and forth along the surface (surface feeding) (Jaine et al. 2012).

Figure 5. Manta ray feeding shown by cephalic lobes unfurled and mouth open making a backwards flip known as a ‘barrel roll’ to capture plankton.

1.3.4 Movements Manta alfredi are a highly migratory species, showing seasonal and diurnal movements

(Dewar et al. 2008, Deakos 2010, Jaine et al. 2012, Couturier et al. 2014, McCauley et al. 2014). Germanov and Marshall (2014) documented movements of M. alfredi between marine protected areas, however, when travelling between the areas they crossed unprotected waters and busy shipping corridors. Although they can travel a long distance, research has proven site fidelity or affinity in some regions (Marshall et al. 2009, Couturier et al. 2011, Braun et al. 2015).

1.3.5 Cleaning Areas of common aggregation and typical visitations have been documented around cleaning stations and areas producing large amounts of food sources, with up to 80 recorded feeding at the same site (Dewar et al. 2008, Marshall et al. 2009, Couturier et al. 2011, Jaine et al. 2012). Not only do they utilise cleaning stations for ectoparasite removal, but have also been documented visiting with fresh bite wounds from sharks

(Marshall and Bennett 2010a). As a manta passes over a cleaning station they relax

15 their cephalic lobes, flare their gills and open their mouths while slowing down, even sometimes hovering over the station (Homma et al. 1999; Figure 6). Intestinal eversion has been documented, thought to allow for the removal of parasites and undigestible matter (Clark et al. 2008). Typically they will make multiple passes around the station, or if multiple stations are close together, travel between them to maximize cleaning time.

Figure 6. Manta ray passing over a cleaning station with multiple cleaners present.

Although shorter sessions are common, the longest documented visit at a cleaning station is 300 minutes by M. alfredi at Osprey Reef on the Great Barrier Reef (O'Shea et al. 2010). They are known to make multiple visits a day to cleaning stations, across consecutive days (Dewar et al. 2008, Couturier et al. 2011, Jaine et al. 2012). Studies also show site fidelity to cleaning stations with many visiting the same locations multiple days in a row (Dewar et al. 2008, Marshall et al. 2009, Couturier et al. 2011).

One exception is presumed with an abundance of cleaning stations in an area (Kitchen-

Wheeler 2010). Cleaning is found to increase with sea temperature but decreases with higher wind speed and during the new and full moon; with visitation to the stations highest in the early morning to early afternoon, similar to other clients (Dewar et al. 16

2008, Jaine et al. 2012). High tide and the beginning of the ebb tide were found to be peak times for cleaning mantas (O'Shea et al. 2010, Jaine et al. 2012).

The combination of their philopatric nature and evidence of aggregations makes cleaning stations focal areas for research and ecotourism (Marshall et al. 2009,

Anderson et al. 2011, Kitchen-Wheeler et al. 2012, Germanov and Marshall 2014).

Studies also focusing on population estimates, seasonal occurrences, and movement patterns are commonly conducted at similar locations (Dewar et al. 2008, Deakos

2010, Couturier et al. 2014). Manta rays in Mozambique were found to visit certain cleaning stations year round and therefore used as study sites for shark-bite injuries

(Marshall and Bennett 2010a). Their slow movements and relaxed behaviour while being cleaned made them easily approachable for measurements and photo identification. In a nine-year study that monitored cleaning stations to estimate population size in the Maldives, 1,835 individuals were identified, which to date is the largest number of individually identified mantas (Kitchen-Wheeler et al. 2012).

1.3.6 Vulnerability The IUCN Red List for Threatened Animals reassessed both manta species in 2011, categorizing them as ‘Vulnerable’ from their previously ‘Near Threatened’ status. It has been suggested that the population has experienced a 30% decline over the last three generations (Dewar et al. 2008). More recently, Rohner et al. (2013) estimated an 88% decline between 2003 and 2011 off Mozambique to artisanal harvest. Fishing practices include gillnetting, harpooning and trawling (Homma et al. 1999, White et al. 2006,

Couturier et al. 2012). Trade is estimated to value approximately $5 million annually, and the catch from 2000 – 2007 increased from 900 to 3,300 tonnes uninclusive of undocumented catches and bycatch (O'Malley et al. 2013). The manta ray’s K-selected

17 life history traits such as low fecundity, late maturation, and long gestation period can make it difficult for them to recover from population decline.

1.3.7 Ecotourism and towards sustainability Manta ray capture is prohibited in many regions such as the Philippines, Mexico and

Australia (White et al. 2006, Croll et al. 2016). A driving factor for change came from the economic impact manta rays have when utilised for ecotourism (Homma et al.

1999; Figure 7); dives and snorkels with the megafauna brings in a direct revenue of approximately US $73 million annually (O'Malley et al. 2013). This realisation has has also transitioned other countries into protecting the species from fishing pressures in certain areas, such as Indonesia in 2014 (Germanov and Marshall 2014).

Figure 7. Aggregation of feeding manta rays and their onlookers (photo credit: Pauly Carlyon).

Some areas require permits for operating an ecotour business for mantas, however, there are no set regulations for interacting with the megafauna (Germanov and

Marshall 2014, Venables et al. 2016). Certain locations such as in Ningaloo Reef,

Western Australia have established a voluntary code of conduct including vessel speed

18 restrictions and distances to be kept by swimmers and vessels for the safety of the manta ray (Daw 2009).

With increasing ecotourism, an increase in boat activity and human presence comes hand in hand. With many manta rays spotted close to the surface, they are vulnerable to boating accidents, as evidence by mantas bearing scars from boat propellers

(Deakos 2010; Figure 8). Other threats to manta populations include habitat degradation, climate change, pollution or other fishing-related injuries such as entanglement in marine debris (Couturier et al. 2012). Deakos (2010) observed 1 in 10

M. alfredi had lost a cephalic lobe caused by fishing-lines.

Figure 8. Manta ray with lacerations from a boat propeller in Ningaloo Reef, Western Australia (Photo credit: Mike van Keulen).

There has been an increase in published studies on the Mobulidae since 1990, however, relatively few focusing on biology and ecology (Couturier et al. 2012). Little is known about their lifespan, growth rates, age at sexual maturity and long-term movements. 19

1.4 Ningaloo Marine Park Western Australia is home to Ningaloo Reef, one of the world’s largest fringing reefs and largest in Australia. Stretching approximately 290 km along the North West Cape, it is the only widespread system on the west coast of a continent (Cassata and Collins

2008). First established in 1987 it was amended in 2004 to include all of Ningaloo Reef, from Carnarvon to Exmouth. With many areas open to the public for multi-use, 34% of the park is reserved as a sanctuary and closed to fishing (Little et al. 2014). In June

2011 the Ningaloo Coast was placed on the World Heritage list, recognising its outstanding universal value.

Two currents run through the Ningaloo Marine Park (NMP), the Leeuwin Current and the opposing Ningaloo Current (MPRA 2005). The Leeuwin Current (LC) is unique as it is the only eastern boundary current which flows poleward, carrying warm water that is low in nutrients and salinity southward along the West Australian coastline (Pearce and

Pattiaratchi 1999). The Ningaloo Current (NC) flows northward and pushes between the LC and the coastline, driven by the strong summer southerly winds (Woo et al.

2006). The two currents interchange with the seasons; LC being strongest and closest to the shore during autumn and winter, while the NC is present in late spring and summer months. These currents make up a large contribution to the area’s unique ecosystem allowing for both tropical and temperate waters within a small area (MPRA

2005). The southern portion of the reef has fringing reefs which are disjointed and become more continuous towards the northern sections. The lagoon varies between

200 m up to 7 km in width, with regular gaps allowing for long reef segments. Some areas within the lagoon and backed by the reef, allow for patch reefs as well as platform reefs near the shore. Water movement is through wave action over the reef

20 crest, wind-driven circulation, and tides, while flushing of the lagoonal waters is through small gaps in the reef (D'Adamo and Simpson 2001).

1.4.1 Tourism Due to the area’s unique geographical and oceanographic features, and despite its remoteness from the closest metropolis Perth, the area welcomes approximately

200,000 visitors annually (Jones et al. 2009). With easy access from shore to various activities along near-pristine coral reefs, the park is marketed as a premier tourism destination (MPRA 2005, Cassata and Collins 2008). Marine habitats range from seagrass beds to coral reefs and mangroves. Vast arrays of fauna can be found such as schools of trevally, reef sharks, dugongs, mana rays and whale sharks. Visitors to NMP partake in many marine activities with snorkelling and sightseeing considered the most important (Jones et al. 2009). A notable activity is the seasonal aggregations of up to

500 whale sharks who visit the NMP, allowing visitors the opportunity to combine tourism and environmental education (Catlin and Jones 2010). Whale shark ecotourism alone has been documented to attract over 17,000 people annually with more than

3,000 interactions documented in 2010 (Anderson et al. 2014).

1.4.2 Coral Bay Coral Bay is a small town along the NMP with its main source of income from nature- based tourism (Jones et al. 2009). Visitors are found to be most interested in touring, and 84% are attracted to the area for snorkelling. Resident manta rays are also found to reside within NMP, particularly around Bateman Bay just north of Coral Bay

(McGregor et al. 2008). Interactions with this charismatic megafauna began in the early

1990s when spotted while on the whale shark vessel. Due to the increase in popularity, by 2003 five manta tour vessels were in operation and can currently take over 130 passengers a day to swim with manta rays (Venables et al. 2016). Although information 21 on manta ray ecotourism is not as readily available as that of whale sharks, in 2009 it was estimated 10,000 individuals took part in manta ray interactions with an annual income of AUD $1.2 million (Daw 2009).

1.5 Aims and objectives Within Ningaloo Reef, manta rays exhibit seasonal fidelity to certain areas, using many of the same cleaning stations (F. McGregor, pers. comm.). A habitat documented to be relied upon for anthropogenic use including manta ray research, tourism and sport fishing, it is imperative to expand our knowledge on these areas. Studies which focus on multiple cleaning stations within a designated site have been seldom conducted.

Additionally, interactions and habits of other individuals within the area are not focused on. While cleaning is what these habitats are most well-known for, additional behaviours such as feeding and hunting, influence species presence and manta ray visitation in Ningaloo Reef. Understanding the ecology of these cleaning stations will help create a baseline of information for future monitoring.

This study assesses the ecology of three major cleaning stations in Bateman Bay known to experience frequent manta ray visitation. The first of its kind, the research is aimed at gathering knowledge on the visiting and resident species at each cleaning station, but without consideration of months of the year. Manta rays are not present at each site year-round, but rather show seasonal preferences to an area. Other fish species such as those belonging to the family Scaridae (Parrotfish), are known to visit cleaning stations for their removal services, providing additional food sources for the cleaners; however those species are not well known.

The aims of this project are: (1) determine whether there are similarities and differences in the taxonomic and trophic diversity of fishes at each cleaning station, (2)

22 identify additional clients who visit the stations, (3) describe and categorise uses of the cleaning stations by fish species.

It is hypothesised that some similarities in fish assemblages will be found between sites, however due to differences in reef habitat and water flow between sites, the abundance of these species and use of habitat will differ.

2.0 Materials and Methods

2.1 Study sites Bateman Bay (23° 03’ S: 113° 46’ E) is the largest lagoon within the Ningaloo Marine

Park, located just north of Coral Bay. The sandy bay of approximately 100 km2 extends up to 7 km from shore and has a wide deep channel (between 8 and 20 m in depth).

These features, in addition to its proximity to the Cardabia Passage (a 5 km gap in the reef), allows this location easy access to the open ocean (van Keulen 2002). Tidal rages are approximately 1.2 m and semi-diurnal. Study sites were within Bateman Bay, between the southern edge of Point Maud, to just south of the Bateman Sanctuary

Zone (Figure 9). The three cleaning stations were chosen, based from previous knowledge of manta ray visitation patterns by ecotourism operators (F. McGregor pers. comm.).

Figure 9. Location of Coral Bay in Western Australia with (a) the areas of each study site chosen boxed in yellow and (b) the two sanctuary zones within Bateman Bay highlighted in green (Google maps; Department of Parks and Wildlife and Department of Fisheries 2014).

Point Maud North (PMN) and South (PMS) sites are within the Maud Sanctuary Zone

(MPRA 2005; Figure 9b) experiencing an increase in manta ray sightings during the spring and summer months. They are approximately 100 m apart with an average depth at both stations of 8 m. Located just off shore from Maud’s Landing, these sites are located in a channel which experiences a south-to-north current, varying in strength with the tides. Both stations are large coral bommies between 10-11 m across, covered in Sargassum during the winter months and surrounded by sand.

The Point Maud north bommie has a central, large coral head with a dead patch at the top, thought to be the result of a resident Loggerhead turtle (Figure 10a). Surrounding 25 the coral head are smaller patches of rubble and corals. PMN has no Sargassum growing on the main coral head, but rather surrounding the area in smaller patches, staying shorter in length and less dense. The Point Maud south station is composed of a combination of coral heads and rubble. PMS also has a larger portion of its rocky and coral surface covered in tall Sargassum during autumn, reaching its highest point in

May (Figure 10b). Both experience drastic changes in Sargassum coverage towards spring (Figure 10 c, d).

Point Maud North Point Maud South a) b)

c) d)

Figure 10. The Point Maud sites before (a,b) and after (c, d) the winter storms have washed away the Sargassum.

The third site is referred to as Oyster Bridge, located north of the Maud’s Landing and south of the Bateman Sanctuary Zone, it exhibits and increase of manta ray visitations during the winter months (F. McGregor, pers. comm.). Different in benthic habitat, this area stretches along a limestone shelf and is parallel to the shore. Atop the shelf are small sponges and corals which are scattered about with shorter stalks of algae growing alongside (Figure 11). This area experiences swell-induced surge, becoming very strong in certain conditions. Various cleaning stations have been identified along

26 the shelf however only one area was selected to be monitored. The average depth of the shelf is approximately 8.6 m which drops to approximately 9.7 m off the shelf.

Figure 11. The northern most cleaning station, Oyster Bridge, located south of the Bateman Sanctuary zone in the Ningaloo Marine Park, with a manta ray coming in to be cleaned from the seaward side off of the shelf.

2.2 Data collection Fieldwork was conducted over the course of five months from mid-March through to mid-July 2016.To monitor each site a GoPro HERO4 camera with underwater housing was attached to an orange dive weight for easier identification underwater. The field of view was set to ultra-wide to view as much of the site as possible, with 30 frames per second (FPS) for the use of clear images in seek mode. A large concrete brick was placed at each site to mark the designated area and the GoPro camera placed on top.

Using bricks also gave a better view of the tall bommies at PMN and PMS, without as much overexposure from the sun through the water. Each site was monitored for 2 hrs at the same time of day, and at all three sites simultaneously if weather and visibility permitted.

Camera deployments were made opportunistically from an ecotourism vessel and therefore recordings from the more remote site of Oyster Bridge were restricted by

27 time, manta ray sightings and water visibility. Samples from OB represented less than half of the total number of days analysed, covering only six days in two consecutive months, which was not sufficient variation for comparison and analysis.

2.3 Station uses Once fish were identified in the recordings, they were designated a behaviour based on their use of the station. Five categories were created: visiting, roaming, resident, feeding and cleaning (Table 1).

Table 1. Classification of uses of cleaning station habitat by individuals and descriptions used to categorise each individual.

Behaviour Description

Visitor Passed through the cleaning station but was not seen again for the (V) remainder of the recording Roaming Seen more than once through the recording but did not partake in any (Ro) activity within the cleaning station Resident Remained at the cleaning station for the duration of the recording (R) Feeding Seen mostly feeding for the times seen within the recording (F) Cleaning Visited the station to be cleaned by cleaners (C)

2.4 Analyses

2.4.1 Video analyses Videos were viewed for the duration of the 2 hr recording. Taxa were identified using identification books (Allen 2009, Swainston 2010) and web references

(fishesofaustralia.net.au; fishbase.org). Abundance was recorded as the maximum number (maxN) of individuals of a species present in the camera view at once (Cappo et al. 2004, Watson et al. 2010). MaxN removes the likelihood of doubling counts of the same individual and therefore is commonly used for abundance counts. Each individual seen on the video was identified at least to family level and to species

28 possible. Individuals were then designated a behaviour from Table 1. If a cleaning event occurred the species involved were also recorded.

2.4.2 Data analyses Analyses were performed using the PRIMER-E V6 software with the additional

PERMANOVA package (Plymouth Routines in Multivariate Ecological Research;

Anderson et al. 2008). Due to large quantities of zero counts, analyses assuming normality of errors were not able to be used. A one-way Permutational Multivariate

Analysis of Variance (PERMANOVA; Anderson 2001) was performed to identify significant differences in species diversity between the study sites. Raw data was square-root transformed because values ranged from zero to over one hundred. A

Bray-Curtis similarity for multivariate analysis matrix was performed to create a resemblance matrix. An ordination plot via non-metric Multi-Dimensional Scaling

(nMDS; Clarke 1993) was used to show trends in species composition between sites.

An Analysis of Similarities (ANOSIM; Clarke 1993) was used to examine where significant differences between sites and months occurred. A shade plot was also created to display the top 35 species averaged per site from the transformed data and seriated to maximize differences among sites using PRIMER-E V7 software (Clarke and

Gorley 2015).

Behaviours assigned to individuals were averaged across days for each site to compare and look for trends in station use. Species were then grouped at the family level to allow for comparison on a broader scale. Each family was also designated a feeding group based on the trophic level of the majority of species in the family: predator, invertivore, corallivore/omnivore or herbivore. Trophic levels were determined using the Marine Trophic Index reported by FishBase (http://fishbase.org; Pauly and Watson

2005, Frias-Torres et al. 2015). Families with only one sighting, at a single cleaning station were removed from further analysis and considered to be seen only by chance.

3.0 Results Sampling was conducted over 15 days throughout the five month study period, totalling 84 hrs between the three cleaning stations. Video recordings were collected for equal periods at Point Maud North (PMN) and Point Maud South (PMS). Recordings from Oyster Bridge (OB) were only conducted over six days; four days in May and two from July. From this data, 144 different species were identified, representing over

3,800 individuals from various families (Table 2).

Table 2. Species table showing the total number of individuals throughout the recordings (N), their average number (Avg), percentage of contribution to the overall total (%), and the species' rank based on percentage contribution (R). Arranged by overall rankings, the top three species from each site, and accumulatively across sites are indicated in red.

Total OB PMN PMS Common Scientific Name Family [N] Avg [%] R [N] Avg [%] R [N] Avg [%] R [N] Avg [%] R Name Greenfin Chlorurus sordidus Scaridae 326 21.7 8.4 1 7 1.2 1.4 20 162 10.8 8.7 1 157 10.5 10.5 2 Parrotfish Palenose Scarus psittacus Scaridae 288 22.2 7.4 2 7 1.2 1.4 21 88 5.9 4.7 4 193 12.9 12.9 1 Parrotfish Moon Wrasse Thalassoma lunare Labridae 163 10.9 4.2 3 35 5.8 6.8 3 66 4.4 3.5 6 62 4.1 4.1 5 Golden Gnathanodon Carangidae 162 18.0 4.2 4 1 0.2 0.2 80 156 10.4 8.3 2 5 0.3 0.3 57 Trevally speciosus Bludger Carangoides Carangidae 148 16.4 3.8 5 2 0.3 0.4 59 137 9.1 7.3 3 9 0.6 0.6 37 Trevally gymnostethus Schlegel's Scarus schlegeli Scaridae 146 9.7 3.8 6 43 2.9 2.3 10 103 6.9 6.9 3 Parrotfish Black Siganus fuscescens Siganidae 141 11.8 3.6 7 81 5.4 4.3 5 60 4.0 4.0 7 Rabbitfish Spangled Lethrinus nebulosus Lethrinidae 107 9.7 2.8 8 3 0.5 0.6 40 48 3.2 2.6 8 56 3.7 3.7 8 Emperor Longnose Hipposcarus Scaridae 103 6.9 2.7 9 30 2.0 1.6 13 73 4.9 4.9 4 Parrotfish longiceps Yellowmask Acanthurus Acanthuridae 103 7.4 2.7 10 3 0.5 0.6 45 39 2.6 2.1 11 61 4.1 4.1 6 Surgeonfish xanthopterus Pomacentrus Neon Damsel Pomacentridae 98 32.7 2.5 11 98 16.3 19.0 1 coelestis Two-line Monocle Scolopsis billneata Nemipteridae 90 6.0 2.3 12 2 0.3 0.4 51 54 3.6 2.9 7 34 2.3 2.3 9 Bream Yellowtail Lethrinus atkinsoni Lethrinidae 75 5.0 1.9 13 21 3.5 4.1 4 25 1.7 1.3 18 29 1.9 1.9 11 Emperor Common Labroides Labridae 74 5.3 1.9 14 17 2.8 3.3 5 32 2.1 1.7 12 25 1.7 1.7 15 Cleanerfish dimidiatus Bicolour Parupeneus Mullidae 56 3.7 1.4 15 3 0.5 0.6 42 25 1.7 1.3 19 28 1.9 1.9 12 Goatfish barberinoides Grey Reef Carcharhinus Carcharhinidae 53 3.5 1.4 16 1 0.2 0.2 72 48 3.2 2.6 9 4 0.3 0.3 59 Shark amblyrhynchos 31

Table 2 cont. Species table showing the total number of individuals throughout the recordings (N), their average number (Avg), percentage of contribution to the overall total (%), and the species' rank based on percentage contribution (R). Arranged by overall rankings, the top three species from each site, and accumulatively across sites are indicated in red.

Thicklip Hemigymnus Labridae 53 3.5 1.4 17 3 0.5 0.6 47 26 1.7 1.4 17 24 1.6 1.6 16 Wrasse melapterus Bluespot Chaetodon plebeius Chaetodontidae 50 3.6 1.3 18 16 2.7 3.1 6 21 1.4 1.1 25 13 0.9 0.9 30 Butterflyfish Brown Tang Zebrasoma scopas Acanthuridae 49 3.3 1.3 19 23 1.5 1.2 23 26 1.7 1.7 14 Linespot Meiacanthus Blenniidae 46 3.5 1.2 20 11 1.8 2.1 10 20 1.3 1.1 26 15 1.0 1.0 25 Fangblenny grammistes Goldstripe Chaetodon Chaetodontidae 45 3.0 1.2 21 9 1.5 1.7 13 22 1.5 1.2 24 14 0.9 0.9 27 Butterflyfish aureofasciatus Painted Diagramma pictum Haemulidae 43 3.1 1.1 22 4 0.7 0.8 35 18 1.2 1.0 31 21 1.4 1.4 17 Sweetlips labiosum Yellowspot Parupeneus indicus Mullidae 42 3.0 1.1 23 15 1.0 0.8 38 27 1.8 1.8 13 Goatfish Stripey Lutjanus Lujanidae 42 3.5 1.1 24 4 0.7 0.8 33 28 1.9 1.5 14 10 0.7 0.7 34 Snapper carponotatus Redblotched Coris aygula Labridae 42 2.8 1.1 25 1 0.2 0.2 81 26 1.7 1.4 16 15 1.0 1.0 26 Wrasse Common Plectropomus Serranidae 41 2.9 1.1 26 25 1.7 1.3 20 16 1.1 1.1 24 Coral Trout leopardus Floral Maori Cheilinus Labridae 40 2.9 1.0 27 5 0.8 1.0 28 14 0.9 0.7 40 21 1.4 1.4 18 Wrasse chlorourus Blacksaddle Parupeneus Mullidae 39 3.0 1.0 28 15 2.5 2.9 7 17 1.1 0.9 32 7 0.5 0.5 43 Goatfish spilurus Pencil Acanthurus Acanthuridae 39 3.0 1.0 29 7 0.5 0.4 58 32 2.1 2.1 10 Surgeonfish dussimeri Tripletail Cheilinus trilobatus Labridae 37 2.8 1.0 30 19 1.3 1.0 28 18 1.2 1.2 20 Maori Wrasse Grey Damsel Pomacentrus reidi Pomacentridae 35 5.8 0.9 31 35 5.8 6.8 2 Silverstreak Stethodulis Labridae 35 2.7 0.9 32 5 0.8 1.0 27 12 0.8 0.6 45 18 1.2 1.2 21 Wrasse strigiventer Darktail Lujanus Lujanidae 34 2.6 0.9 33 15 1.0 0.8 39 19 1.3 1.3 19 Snapper lemniscatus Slingjaw Epibulus insidiator Labridae 34 2.3 0.9 34 17 1.1 0.9 34 17 1.1 1.1 22 Wrasse

Longfin Heniochus Chaetodontidae 33 3.0 0.8 35 13 2.2 2.5 8 11 0.7 0.6 47 9 0.6 0.6 36 Bannerfish acuminatus Blacktip Epinephelus Serranidae 31 2.2 0.8 36 3 0.5 0.6 43 12 0.8 0.6 43 16 1.1 1.1 23 Rockcod fasciatus Red Scargocentron Holocentridae 28 7.0 0.7 37 23 1.5 1.2 22 5 0.3 0.3 56 Squirrelfish rubrum Bluespine Naso unicornis Acanthuridae 28 2.0 0.7 38 2 0.3 0.4 57 25 1.7 1.3 21 1 0.1 0.1 92 Unicornfish Lined Ctenochaetus Acanthuridae 28 2.2 0.7 39 28 1.9 1.5 15 Bristletooth striatus Redspot Stethojulis Labridae 28 2.5 0.7 40 6 1.0 1.2 25 12 0.8 0.6 46 10 0.7 0.7 35 Wrasse bandanensis Chameleon Scarus chameleon Scaridae 27 2.3 0.7 41 4 0.7 0.8 32 13 0.9 0.7 41 10 0.7 0.7 33 Parrotfish Birdnose Gomphosus varius Labridae 25 1.8 0.6 42 11 0.7 0.6 48 14 0.9 0.9 28 Wrasse Racoon Chaetodon lunula Chaetodontidae 23 1.6 0.6 43 18 1.2 1.0 29 5 0.3 0.3 52 Butterflyfish Margined Chelmon marginalis Chaetodontidae 23 2.1 0.6 44 2 0.3 0.4 52 15 1.0 0.8 35 6 0.4 0.4 48 Coralfish Lined Chaetodon Chaetodontidae 23 2.9 0.6 45 1 0.2 0.2 68 15 1.0 0.8 36 7 0.5 0.5 42 Butterflyfish lineolatus Peacock Cephalopholis Serranidae 23 1.8 0.6 46 20 1.3 1.1 27 3 0.2 0.2 70 Rockcod argus Charcoal Pomacentrus Pomacentridae 22 1.7 0.6 47 7 1.2 1.4 19 9 0.6 0.5 55 6 0.4 0.4 49 Damsel brachialis Rainbow Scolopsis Monocle Nemipteridae 20 1.5 0.5 48 7 0.5 0.4 57 13 0.9 0.9 29 monocramma Bream Lemon Pomacentrus Pomacentridae 20 1.8 0.5 49 1 0.2 0.2 71 18 1.2 1.0 30 1 0.1 0.1 80 Damsel moluccensis Pastel Slender Hologymnosus Labridae 19 1.9 0.5 50 12 0.8 0.6 44 7 0.5 0.5 47 Wrasse doliatus Diamond Anampses Labridae 19 2.4 0.5 51 13 0.9 0.7 42 6 0.4 0.4 51 Wrasse caeruleopunctatus 33

Sevenband Thalassoma Labridae 18 1.6 0.5 52 10 0.7 0.5 52 8 0.5 0.5 40 Wrasse septemdasciatum Threadfin Chaetodon auriga Chaetodontidae 17 1.9 0.4 53 4 0.7 0.8 30 2 0.1 0.1 89 11 0.7 0.7 31 Butterflyfish Threespot Siganus trispilos Siganidae 17 1.7 0.4 54 17 1.1 0.9 33 Rabbitfish Aulostomus Trumpetfish Aulostomidae 17 1.5 0.4 55 10 0.7 0.5 51 7 0.5 0.5 46 chinesis Sixband Pomacanthus Pomacanthidae 16 1.6 0.4 56 4 0.7 0.8 29 9 0.6 0.5 54 3 0.2 0.2 65 Angelfish sextriatus Sp 05 N/A N/A 16 1.5 0.4 57 10 1.0 0.5 50 6 0.8 0.4 50 Pomacanthus Blue Angelfish Pomacanthidae 15 1.5 0.4 58 7 1.2 1.4 17 5 0.3 0.3 64 3 0.2 0.2 66 semicirculatus Scissortail Abudefduf Pomacentridae 15 2.5 0.4 59 15 0.9 0.8 37 1 0.1 0.1 79 Sergeant sexfasciatus Parrotfish 09 N/A Scaridae 15 1.5 0.4 60 2 0.3 0.4 53 6 0.4 0.3 63 7 0.5 0.5 44 Sixband Scarus frenatus Scaridae 14 1.6 0.4 61 3 0.2 0.2 78 11 0.7 0.7 32 Parrotfish Sharpnose Cheilio inermis Labridae 14 1.8 0.4 62 8 1.3 1.5 16 2 0.1 0.1 97 4 0.3 0.3 63 Wrasse Checkerboard Halichoeres Labridae 14 1.6 0.4 63 3 0.5 0.6 48 10 0.7 0.5 53 1 0.1 0.1 98 Wrasse hortulanus Moorish Idol Zanclus cornutus Zanclidae 13 1.9 0.3 64 10 1.7 1.9 12 3 0.2 0.2 77

Spotbanded Chaetodon Chaetodontidae 12 1.5 0.3 65 6 1.0 1.2 23 6 0.4 0.3 61 Butterflyfish punctatofasciatus Longnose Lethrinus olivaceus Lethrinidae 12 1.7 0.3 66 3 0.5 0.6 41 4 0.3 0.2 69 5 0.3 0.3 53 Emperor Reef Manta Manta alfredi Mobulinae 12 1.5 0.3 67 8 1.3 1.5 15 3 0.2 0.2 76 1 0.1 0.1 85 Ray Steephead Chlorurus Scaridae 12 2.0 0.3 68 1 0.2 0.2 74 6 0.4 0.3 62 5 0.3 0.3 55 Parrotfish microrhinos Sp 08 N/A N/A 12 2.4 0.3 69 12 2.0 2.3 9 Redbreast Cheilinus fasciatus Labridae 12 2.0 0.3 70 7 0.5 0.4 59 5 0.3 0.3 58 Maori Wrasse 34

Bicolour Labroides bicolor Labridae 12 1.3 0.3 71 9 0.6 0.5 56 3 0.2 0.2 72 Cleanerfish Chevron Chaetodon Chaetodontidae 11 1.8 0.3 72 8 1.3 1.5 14 3 0.2 0.2 73 Butterflyfish trifascialis Flutemouth Fistularia spp. Fistulariidae 11 1.8 0.3 73 6 1.0 1.2 24 5 0.3 0.3 54 spp. Bluebarred Scarus ghobban Scaridae 11 1.4 0.3 74 5 0.8 1.0 26 3 0.2 0.2 79 3 0.2 0.2 69 Parrotfish Keyhole Centropyge tibicen Pomacanthidae 10 1.3 0.3 75 3 0.2 0.2 70 7 0.5 0.5 41 Angelfish Bluestriped Plagiotremus Blenniidae 10 1.7 0.3 76 7 1.2 1.4 18 2 0.1 0.1 86 1 0.1 0.1 76 Fangblenny rhinorhynchos Candystripe Apogon Apogonidae 10 3.3 0.3 77 10 0.7 0.5 49 Cardinalfish endekataenia Bengal Abudefduf Pomacentridae 10 1.4 0.3 78 2 0.1 0.1 91 8 0.5 0.5 38 Sergeant bengalensis Whitepatch Dischistodus Pomacentridae 10 2.5 0.3 79 10 1.7 1.9 11 Damsel chrysopoecilus Sp 01 N/A N/A 10 3.3 0.3 80 2 0.2 0.1 94 8 1.0 0.5 39

Bluefaced Pomacanthus Pomacanthidae 9 1.5 0.2 81 6 0.4 0.3 60 3 0.2 0.2 64 Angelfish xanthometopon Spot-tail Coris caudimacula Labridae 8 1.1 0.2 82 7 1.2 1.4 22 1 0.1 0.1 99 Wrasse Choerodon Blue Tuskfish Labridae 8 1.3 0.2 83 5 0.3 0.3 68 3 0.2 0.2 71 cyanodus Longfin Platax punnatus Ephippidae 7 1.8 0.2 84 3 0.2 0.2 75 4 0.3 0.3 60 Batfish Frostback Eponephelus Serranidae 7 1.4 0.2 85 3 0.2 0.2 81 4 0.3 0.3 62 Rockcod bilobatus Hawaiian Rhinecathus Balistidae 7 1.2 0.2 86 7 0.5 0.5 45 Triggerfish aculeatus Blacktip Reef Carcharhinus Carcharhinidae 6 1.2 0.2 87 3 0.2 0.2 71 3 0.2 0.2 67 Shark melanopterus Giant Sepia apama Sepiidae 6 1.2 0.2 88 3 0.5 0.6 39 3 0.2 0.2 68 Cuttlefish 35

Honeycomb Cantherhines Monacanthidae 6 1.5 0.2 89 4 0.7 0.8 31 1 0.1 0.1 103 1 0.1 0.1 83 Leatherjacket pardalis Loggerhead Caretta caretta Cheloniidae 6 1.0 0.2 90 5 0.3 0.3 66 1 0.1 0.1 84 Turtle Inshore Acanthurus Acanthuridae 6 1.5 0.2 91 1 0.2 0.2 79 3 0.2 0.2 83 2 0.1 0.1 74 Surgeonfish grammoptilus Yellowspotted Pseudobalistes Balistidae 6 1.2 0.2 92 2 0.3 0.4 61 3 0.2 0.2 84 1 0.1 0.1 96 Triggerfish fuscus Fiveband Hemigymnus Labridae 6 1.2 0.2 93 4 0.7 0.8 37 2 0.1 0.1 75 Wrasse fasciatus False Aspidontus Blenniidae 5 1.3 0.1 94 2 0.3 0.4 50 3 0.2 0.2 72 Cleanerfish taeniatus Western Kyphosuscornelii Kyphosidae 5 2.5 0.1 95 5 0.3 0.3 65 Buffalo Bream Eagle Ray spp. N/A Mylipbatidae 5 5.0 0.1 96 3 0.2 0.2 74 2 0.1 0.1 73

Green Jobfish Aprion virescens Lujanidae 5 2.5 0.1 97 5 0.3 0.3 67 Surf Scarus rivulatus Scaridae 4 1.0 0.1 98 3 0.2 0.2 80 1 0.1 0.1 86 Parrotfish Hypogaleus Pencil Shark Triakidae 4 1.3 0.1 99 4 0.3 0.3 61 hyugaensis Sp 07 N/A N/A 4 4.0 0.1 100 4 0.7 0.8 34

Horseface Naso fageni Acanthuridae 4 1.3 0.1 101 3 0.5 0.6 46 1 0.1 0.1 93 Unicornfish Starry Abalistes stellatus Balistidae 4 1.0 0.1 102 2 0.3 0.4 60 1 0.1 0.1 109 1 0.1 0.1 95 Triggerfish Bridled Sufflamen Balistidae 4 1.0 0.1 103 4 0.7 0.8 36 Triggerfish fraenatum Ornate Macropharyngodon Leopard Labridae 4 1.0 0.1 104 4 0.7 0.8 38 ornatus Wrasse Aspidontus Lance Blenny Blenniidae 3 1.5 0.1 105 1 0.2 0.2 65 2 0.1 0.1 87 dussumieri Blotched Tarniura meyeni Myliobatiformes 3 1.0 0.1 106 2 0.1 0.1 88 1 0.1 0.1 77 Fantail Ray

Crowned Canthigaster Tetraodontidae 3 1.0 0.1 107 2 0.3 0.4 54 1 0.1 0.1 87 Toby axiologus Bluespotted Cephalopholis Serranidae 3 1.5 0.1 108 2 0.1 0.1 93 1 0.1 0.1 88 Rockcod cuanostigma Yelloedge Coronation Variola louti Serranidae 3 1.0 0.1 109 3 0.2 0.2 82 Trout Chinaman Epinephelua Serranidae 3 1.0 0.1 110 2 0.3 0.4 55 1 0.1 0.1 107 Rockcod rivulatus Sp 03 N/A N/A 3 1.0 0.1 111 2 0.3 0.4 56 1 0.1 0.1 90 Sp 09 N/A N/A 3 1.0 0.1 112 3 0.5 0.6 44

Whitetip Reef Triaenodon obesus Carcharhinidae 3 1.0 0.1 113 3 0.2 0.2 85 Shark Emperor Pomacanthus Pomacanthidae 2 1.0 0.1 114 2 0.3 0.4 49 Angelfish imperator Teardrop Chaetodon Chaetodontidae 2 2.0 0.1 115 2 0.1 0.1 90 Butterflyfish unimaculatus Western Chaetodon assarius Chaetodontidae 2 2.0 0.1 116 1 0.2 0.2 69 1 0.1 0.1 101 Butterflyfish Red Emperor Lutjanus sebae Lethrinidae 2 1.0 0.1 117 2 0.1 0.1 92 Green Turtle Chelonia mydas Cheloniidae 2 2.0 0.1 118 1 0.1 0.1 102 1 0.1 0.1 82

Purple Epinephelus Serranidae 2 1.0 0.1 119 1 0.1 0.1 106 1 0.1 0.1 89 Rockcod cyanopodus Sp 06 N/A N/A 2 1.0 0.1 120 2 0.2 0.1 95

Sp 11 N/A N/A 2 1.0 0.1 121 1 0.2 0.2 78 1 0.1 0.1 108 Spotted Naso brevirostris Acanthuridae 2 1.0 0.1 122 2 0.3 0.4 58 Unicornfish Whitespotted Canthidermis Balistidae 2 1.0 0.1 123 2 0.1 0.1 96 Triggerfish maculatus Scribbled Anampses Labridae 2 1.0 0.1 124 1 0.1 0.1 111 1 0.1 0.1 97 Wrasse geographicus Speckled Anampses Labridae 2 1.0 0.1 125 2 0.1 0.1 98 Wrasse meleagrides

Ringed Hologymnosus Slender Labridae 2 1.0 0.1 126 2 0.1 0.1 99 annulatus Wrasse Yellowtail Chaetodontoplus Pomacanthidae 1 1.0 0.0 127 1 0.2 0.2 62 Emperor personifer Barred Diploprion Serranidae 1 1.0 0.0 128 1 0.2 0.2 63 Soapfish bifasciatum Bigeye spp. N/A Pricanthidae 1 1.0 0.0 129 1 0.2 0.2 64 Yellow Ostracian cubicus Ostraciidae 1 1.0 0.0 130 1 0.2 0.2 66 Boxfish Yellowstripe Pentapodus Nemipteridae 1 1.0 0.0 131 1 0.2 0.2 67 Threadfin aureofasciatus Forcipiger Forceps Fish Chaetodontidae 1 1.0 0.0 132 1 0.1 0.1 100 flavissimus Common Pterios volitans Scorpaenidae 1 1.0 0.0 133 1 0.2 0.2 70 Lionfish Cowtail Pastinachus atrus Dasyatidae 1 1.0 0.0 134 1 0.1 0.1 78 Stingray Common Tursiops aduncus Delphinidae 1 1.0 0.0 135 1 0.1 0.1 81 Dolphin Scrawled Aluterus scriptus Monacanthidae 1 1.0 0.0 136 1 0.1 0.1 104 Leatherjacket Order: Octopus N/A 1 1.0 0.0 137 1 0.2 0.2 73 Octopoda Spotted Didon hystrix Diodontidae 1 1.0 0.0 138 1 0.2 0.2 75 Porcupinefish Blacksaddle Canthigaster Tetraodontidae 1 1.0 0.0 139 1 0.2 0.2 76 Toby valentini Potato Epinephelus tukula Serranidae 1 1.0 0.0 140 0 0.0 0.0 114 1 0.1 0.1 105 Rockcod Sp 02 N/A N/A 1 1.0 0.0 141 1 0.2 0.2 77 Sp 10 N/A N/A 1 1.0 0.0 142 1 0.1 0.1 91

Tiger Shark Galeocerdo cuvier Galeocerdo 1 1.0 0.0 143 1 0.1 0.1 94

Orangestripe Balistapus Balistidae 1 1.0 0.0 144 1 0.1 0.1 110 Triggerfish undulatus Total Species 3885 517 1869 1499

The family Labridae (wrasses) had the highest number of species, with a total of 23 species recognised followed by the Chaetodontidae (butterflyfish; 11 species) and

Scaridae (parrotfish; 10 species). Chlorurus sordidus (Greenfin Parrotfish) was the most abundant species between the three study sites, accounting for 8.4 % of total abundance, followed by Scarus psittacus (Palenose Parrotfish) with 7.4% of total abundance (Table 2). The most abundant species at PMN was also C. sordidus (8.67%), second only to S. psittacus at PMS contributing 10.5%. Species composition at OB differentiated to the other sites; C. sordidus and S. psittacus ranked 20th and 21st respectively, contributing to less than 2% of the overall abundance. Pomacentrus coelestis (Neon Namsel) was most commonly seen at OB making up 19.0% of total abundance.

Comparing species diversity and richness between sites, an ANOSIM test revealed each cleaning station to be significantly different from the other (p < 0.05). Both Point Maud locations are relatively close in proximity, however significantly different in species richness and individual species, allowing for them to be considered two separate study sites. A diversity matrix revealed significant differences between stations in all analyses

(Table 3). ANOSIM was used to compare species composition at different months, resulting in a significant difference over time (p < 0.05).

Table 3. Results of a One-Way ANOVA, comparing all (OB- PMN-PMS), and PMN-PMS on number of species (S), number of individuals (N), species richness (R), and species diversity using the Shannon Index (J’).

Site S N R J' All 3.25 E-07 4.73 E-05 1.23 E -06 8.45 E-07 PMN-PMS 0.0054 0.22 0.011 0.25

An nMDS plot of the transformed data gives a visual representation of the similarities between PMN and PMS without consideration of months, as well as the difference in

40 species composition at OB (Figure 12). The two Point Maud sites appear to be similar, shown by data points grouped close together, but do not overlap, showing differences between sites.

Figure 12. A non-metric Multidimensional Scaling (nMDS) plot of species composition at Oyster Bridge (blue), Point Maud North (red) and Point Maud South (green). Each point represents a separate recording.

Although differences are clear between the three stations, some similarities in species were documented; a total of 46 species from 19 families were recorded at all three sites. To identify influential species from each site, the top 35 species were selected in and represented as a shade plot (Figure 13).

Figure 13. Shade plot illustrating the square root transformed MaxN of species, filtering only the top 35 most common species from each site. Shading indicates the relative abundance of species at the different sites from light (low abundance) to dark shading (high abundance).

Many of the top species found solely at OB were some of the most dominating species in the area such as Pomacentrus reidi (Grey damsel) and Pomacentrus coelestis (Neon damsel). This pattern is not seen at either of the Point Maud sites with the most common species at PMN being Cholorurus sordidus (Greenfin parrotfish)and PMS, as well as a high abundance of Scarus psittacus (Palenose parrotfish) at PMS. Labroides dimidiatus (Common Cleanerfish), Meiacanthus grammistes, (Linespot Fangblenny),

Lethrinus atkinsoni (Yellowtail Emperor) and Thalassoma lunare (Moon Wrasse) were some of the commonly seen species in all three sites across the sampling period.

Once taxa were grouped into family, only 30 of the 37 were used for further analyses to examine trophic classes (Figure 14). Herbivores were the most abundant trophic level identified within all three sites, accounting for 40.57% of the fish at OB, 34.93% at

PMN and 51.62% at PMS.

11.48 9.3 %

40.5733.0 12.815.78 % % 26.232.17 %

34.93%43.7 41.032.80%

10.0 24.27%30.3 8.00%

16.76%16.6 5.5 5.52% 51.1 51.62% 26.11%25.9

Figure 14. The study area in Bateman Bay showing the proportion of feeding groups found at each study site in the study area of Bateman Bay, Ningaloo Marine Park, Western Australia.

Residents made up a large proportion of individuals at each site, accounting for 38.90% at OB, 24.02% at PMN and 31.34% at PMS (Figure 15). Cleaning events were the least common, with the largest proportion being found at PMS at only 3.04% of the total behaviours observed at each site.

1.71% 9.68%

9.7 20.49%20.5

38.938.90% 29.22%29.2

3.04% 7.66%

7.7 39.43% 39.4 24.024.02%

25.925.85%

1.38%

17.41%17.4 24.97%25.0 24.90%24.9 31.34%31.3

Figure 15. The study area in Bateman Bay showing the proportion of behaviours documented at each study site; Cleaning (C), feeding (F), resident (R), roaming (R0), and visiting (V).

20 15 a) b)

15 Corallivore/ Predator 10 Omnivore 10

Average abundance Average 5

0 0 Angelfish Butterflyfish Cardinalfish Puffer

c) d) 20 45 40

15 Invertivore 35 30 Herbivore 25 10 20 15

Average abundance Average 5 10 5 0 0

Figure 16. Average abundance of trophic groups at each site (+- SD) of (a) predators, (b), corallivore/omnivores (c) invertivores and (d) herbivores. Categorisation was made using the Fishbase.org marine trophic index (Pauly and Watson 2005).

3.1 Point Maud South Over 50% of this cleaning station was composed of herbivores (Figure 14), mainly represented by the parrotfish with an average of 37.5 individuals per recording (Figure

16d). Predators and the corallivore/omnivores were similar to OB with emperors and butterflyfish being the most abundant families seen (Figure 16a, b). This site showed the most evenly distributed behaviours, but with the largest proportion of feeing events (25.0%) compared to the other sites (Figure 15). Cleaning was seen the least observed activity (1.4%).

3.2 Point Maud North Herbivores were the most common feeding group, composing mainly of wrasse. More predators were seen at PMN than any other site, accounting for 41.0% of the population (Figure 16b). Trevally were most dominant over any other family, however the other commonly seen predators had similar averages ranging from 4.1 to 5.3 individuals per recording. Some of these included the emperor, rockcod and bream.

Butterflyfish were the leading corallivorous/omnivorous family, and wrasse seen on average 20.5 individuals per recording as the most abundant invertivore (Figure 16).

PMN experienced the largest proportion of visitors of the three sites (39.4%), and the most cleaning events (3.0%). Roaming and residents were similar, however feeding was rarely seen.

3.3 Oyster Bridge Herbivores were the most common feeding group, with damselfish in greatest abundance, found most often at OB with 25.2 individuals per recording (Figure 16).

Emperors were the most frequently seen predator, averaging 4.5 individuals per 2 hour recording. Wrasses were the most common invertivores identified at OB, as well as at the two PM sites. Corallivore/omnivores were largely composed of the butterflyfish.

The majority of individuals seen were residents (38.9%), however roaming was also commonly documented (29.2%). Cleaning was seldom documented, only 1.7% of the time, as well as feeding (9.7%).

3.4 Cleaning Individuals were found to be using the cleaning station for each of the outlined purposes. A total of 90 cleaning events were recorded, from 30 different species. PMN experienced the most cleaning events, followed by PMS. However, when only averaging the number of cleaning events per recording, OB had the second highest number of cleaning events. Labroides dimidiatus was found at all three sites, but the greatest proportion was at OB with an average of 3.4 individuals per sample. The most common species to be cleaned between all three stations was Lethrinus atkinsoni

(Yellowtail Emperor) and Hemigymnus melapterus (Thicklip Wrasse).

3.5 Manta sightings Each cleaning station was visited at least once by Manta alfredi for cleaning purposes and a total of six cleaning events were recorded. The most sightings occurred at OB with eight in total, including four cleaning events, three roaming and one visit. Both

Point Maud sites had one cleaning event which was by the same manta ray, making large rotations between sites. PMN also experienced two additional visitations by other manta rays over the course of the videos. The cleaner L. dimidiatus was identified cleaning each manta ray client on all six events; however others were also seen on occasion taking part in the cleaning process. These species included:

Heniochus acuminatus (Longfin Bannerfish), Thalassoma lunare (Moon Wrasse),

Aspidontus taeniatus (False Cleanerfish), Chaetodon aureofasciatus (Goldstripe

Butterflyfish).

4.0 Discussion

4.1 Station diversity There is great diversity in the fish species known to use cleaning stations (Losey 1972,

Arnal and Côté 1998, Grutter et al. 2003); this study). Factors such as salinity, water motion and temperature can influence species distribution and habitat use (Bellwood and Wainwright 2001). The three cleaning stations in this study are close enough in proximity and depth to not experience differences in temperature or salinity; however water motion can be a factor resulting in diversity between Point Maud and Oyster

Bridge sites. Bellwood and Wainwright (2001) suggested that some fishes such as the scarids (parrotfish) and labrids (wrasse), depending on their pectoral fin to body ratio, will favour certain habitats due to its degree of water movement. Both Point Maud sites experience the same south-to-north current, while Oyster Bridge is exposed to more of a swell-induced surge. Both PMN and PMS harbour many of the same species, possibly visiting both stations over the course of a day. Species richness and number of individuals recorded was however, significantly different between sites. The seasonal abundance of Sargassum growth found at each site is also a factor which could contribute to the results of species recorded. Between March and May, the density and height of the Sargassum had increased substantially at PMS; by May it was so high, many fish travelling within the station could not be seen. Therefore more species may have been present during these recordings but not documented, perhaps accounting for the difference in species numbers and richness between PMN and PMS.

4.2 Station uses Station uses were are also different among the three sites, with more individuals using the PMS station for feeding and roaming, while the PMN and OB stations were more

48 commonly used for roaming or passing through. Cleaning was a minor component of the behaviours recorded.

4.2.1 Point Maud South The largest proportion of herbivores was seen at PMS, as well as the greatest proportion of feeding individuals. It is assumed that this cleaning station is used primarily for feeding during the winter months. Scarids were seen at the greatest concentrations at PMS, feeding on the Sargassum. For this study they were grouped together as herbivores, therefore it is possible the presence of Sargassum is influencing preference of feeding to this location over the nearby station of PMN.

Seasonal grazing has been identified in damselfish, surgeonfish and parrotfish (Ferreira et al. 1998), and it is likely this study was conducted during the optimal feeding time for the PMS site because of the high biomass of Sargassum.

Although PMS is an identified cleaning station, Scarus frenatus (Sixband Parrotfish) and

Chlorurus sordidus (Greenfin Parrotfish) were the only parrotfish species seen being cleaned at PMS on two occasions. Similar patterns were seen with Hemigymnus melapterus (Thicklip Wrasse) where the majority of encounters were feeding, with two cleaning events documented. It is possible these cleaning events are opportunistic, where individuals visit the cleaning station for feeding purposes and take advantage of the additional cleaning service if needed.

Large groups of juvenile (and what appeared to be female) C. sordidus, were the most commonly seen residents at the station. Complex habitats can harbor fish from predators, allowing for species richness to remain intact (Wilson et al. 2009). The substrate of PMS, with its structural complexity and large quantities of algae makes it an ideal place for juveniles. Predatory fish were also documented roaming the area. It

49 is possible many of the predatory species such as Lethrinus nebulosus (Spangled

Emperor) and Plectropomus leopardus (Common Coral Trout) were hunting for small fishes.

4.2.2 Point Maud North Data from PMN shows the greatest abundance of predators and visiting individuals over the other locations. This can be attributed to one recording where a school of approximately 300 Trevally spp. (Gnathanodon speciosus and Carangoides gymnostethus) swam through the cleaning station, causing the peak in Trevally and possibly to the greater proportion of visiting individuals to the station. It does appear however, the school was using the cleaning station. On one occasion, a G. speciosus

(Golden Trevally) was seen being cleaned; by travelling through the cleaning station the school appears to allow for individuals to stop and be cleaned if needed.

Almost half of the individuals documented over the course of the study period were visiting (only seen once), more often than any other behaviour at the cleaning station;

L. nebulosus and Carcharhinus amblyrhynchos (Grey Reef Shark) being the most common. Site fidelity is seen in C. amblyrhynchos with movements between and among reef platforms (Heupel et al. 2010). Therefore due to the many sightings throughout the study, PMN could be within its habitat range and sightings marked as visits are from the shark simply cruising through its home range.

Although feeding was also seen from a variety of species, similar to those at PMS, most occurrences were documented only once, by one individual. The quantity of

Sargassum present at PMN appeared to be much less than PMS, therefore many individuals exhibit preference to PMS for feeding.

Cleaning events were documented more frequently, and over a larger variety of species at this site. The most commonly cleaned species was H. melapterus followed by

Scarus schlegeli (Schlegel’s Parrotfish). Hemigymnus melapterus was also found feeding at this site on many occasions. It is presumed that, although PMN is not as appealing for feeding, individuals will come to be cleaned while also using this opportunity to feed.

4.2.3 Oyster Bridge The feeding guilds and behaviours of fish at Oyster Bridge were very different from those at the Point Maud sites, possibly due to the contrast in substrate, currents and benthos at this site. The site exhibits a had a greater abundance of herbivores than other trophic groups; however it was not by the scarids but Pomacentridae

(damselfish) with approximately 25 individuals seen per recording. These numbers are mostly inclusive of Pomacentrus coelestis (Neon Damsel) and Pomacentrus reidi (Grey

Damsel). There are large proportions of residents at OB, the greatest of all three sites at nearly 39.0%, also accredited mostly to the damselfish populations. Certain species of damselfish are known for their aggressive and territorial behaviour towards their habitats, protecting hiding places and food sources (Robertson 1984). Diversity and abundance of client species to a cleaning station is also seen to vary with the presence of territorial damselfish (Arnal and Côté 1998). Due to small numbers of damselfish present at either PM site, their abundance at OB shows another contributing factor to the site’s significant differences in species diversity.

Roaming was also commonly seen among individuals. Due to the topographic features of this location, the increase in this behaviour may be a result of species swimming back and forth along the shelf. Forceful surge can also make remaining in one spot

51 difficult, particularly for the smaller species; therefore it is possible the low occurrences of feeding behaviour are attributed to the water movements.

Although this site had the least amount of recordings it also had the greatest number of L. dimidiatus present with an average of 3.4 individuals per day; one more on average than both PM sites. Studies show L. dimidiatus has fixed cleaning stations on coral reefs, where they service new and reoccurring clients (Randall 1958), and their home ranges on patch reefs, are smaller than those at a fringing reef (Oates et al.

2010). Although the area chosen at Oyster Bridge is a known cleaning station it could be more associated to a fringing reef, as opposed to isolated patches as seen at Point

Maud. With greater home ranges at OB, seeing overlapping ranges with fellow cleanerfish is possible, resulting in the increase of individuals. However, cleaning events were not common, perhaps attributed the large proportion of blenny species present, which are known to mimic cleaners (Randall 2005). Research shows clients have been known to leave cleaning stations upon identifying a mimic (Côté 2000). As this site had the fewest recordings, it was also expected to have less cleaning interactions compared to the other sites. This station shows many uses but does not seem to favour particular behaviours. With the abundance of cleaners and blennies present however, it is likely an attractive area for potential clients.

4.3 Common species The wrasse, parrotfish and emperors were the most common families between study sites, each family belonging to a different feeding group, showing trophic diversity.

Labroides dimidiatus is known to influence a reef’s health, species richness and diversity, attracting site-attached adults as residents, juveniles and visitor fishes

(Bshary 2003, Grutter et al. 2003, Sun et al. 2016). The presence of L. dimidiatus may

52 be an identifying feature to some species of a healthy reef and diversity-rich environment, in turn influencing their presence.

Many species showed preferences in behaviours depending on the cleaning station, while some exhibited consistency across locations. The Fistularia spp. (Flutemouth) was seen hunting through both PMS and OB on many occasions, with two successful feeding attempts documented. This species was not seen at cleaning stations for any other purposes but it shows this habitat is relied upon by Fistularia spp. for prey.

Epinephelus fasciatus (Blacktip Rockcod) was documented at each site with the same behaviour of resting along the bottom guarding its home, classified as a resident.

Although other factors may influence residence preferences, such as a food source, it appears in the video to simply protect its domain.

The dominating cleaner species among the three sites is L. dimidiatus, however another cleaner wrasse was also documented in recordings; Labroides bicolor (Bicolour

Cleanerfish). The cleaner was observed on multiple days but also seen on three occasions, cleaning visiting clients at both PMN and PMS. Studies show L. bicolor has a larger home range than L. dimidiatus (Oates et al. 2010), interacting with clients at different stations. While L. dimidiatus exhibits a home range of a single island station at

PM, L. bicolor shows signs of migrating between the various coral bommies, cleaning clients present at the time.

4.4 Large clients Larger species of elasmobranch such as Tarniura meyeni (Blotched Fantail Ray), C. amblyrhynchos and M. alfredi were also recorded as clients to the cleaning stations.

Each species had at least one cleaning interaction at one or multiple locations. Manta alfredi was cleaned once at Point Maud. The individual began its cleaning interaction at

53 the northern site, and then was seen at the southern site moments later. This cleaning behaviour exhibited by M. alfredi further supports how the stations may be connected.

The largest proportion of manta ray sightings was at the OB site; three roaming, one visitor, and four cleaning events. Being a migratory species and showing seasonal movement patterns (Dewar et al. 2008, McCauley et al. 2014), manta rays in the

Bateman Bay area show patterns of site preference for cleaning at OB during the winter months, coinciding with the study period (F. McGregor, pers. comm.).

Carcharhinus amblyrhynchos was also observed posing for cleaning on four occasions, but only at PMN, possibly demonstrating cleaning station preferences. Both ray species were the only individuals seen being cleaned by multiple cleaner species. As they are large clients, with the possibility of a greater ectoparasite load, many cleaners are able to take advantage of the food source.

4.5 Targeted species The Point Maud study sites are within the Maud Sanctuary Zone, where fishing of any kind is prohibited (Department of Parks and Wildlife and Department of Fisheries

2014). Targeted families such as the emperors, snapper and rockcods were found at all three cleaning stations on regular occasions, with the greatest number of individuals on average at Point Maud. This suggests cleaning stations, are important habitats for targeted fish as well as sites for cleaning. Oyster Bridge is outside of the Sanctuary

Zone and therefore vulnerable to fishing pressures. Without more evidence, it can only be proposed that smaller numbers of targeted fish is due to such activities, but can potentially have negative effects. Predators near or at the top of food webs can influence the ecology of ecosystems (McClanahan 2000); their decrease in numbers or absence is known to have trickle down effects to many other species, referred to as a trophic cascade (Bond 1994, Heithaus et al. 2008). The loss of predatory fish at Oyster 54

Bridge could affect the cleaning station’s functionality, making it less appealing to manta rays and other species residing and visiting the station.

4.6 Limitations and future research considerations Due to time constraints, fieldwork was conducted over five months (March to July) of

2016. This research would benefit from consistent monitoring across all seasons to provide a more accurate representation of cleaning station use and species diversity from the three sites. More replications at sites would also allow for an improved understanding of manta ray visits to cleaning stations and their seasonal shifts from one site to the other.

Most expeditions into the field were made possible by cooperation from a manta ray ecotourism vessel; however this posed its own limitations. Time constraints became a factor with deployments of the recording devices in order to ensure paying customers on the vessel were given optimal time in the water. The Point Maud sites were in close proximity to many popular snorkelling sites and visibility was typically good, making recordings from this area possible every day on the water. Oyster Bridge was difficult to access, as it was further away from the common areas of manta ray sightings.

Visibility was also an issue for camera deployment at OB, with some days of no deployments for fear of losing the camera, as well as not being able to identify species during analysis. This restriction would also benefit with more time in the field to account for the days without deployments. A research vessel was used on some occasions; although full use of a research vessel is ideal and recommended, it was beyond the scope of this study.

Underwater visual census (UVC), similarly to the methods used in this study, is useful in assessing species richness and abundances (Davis et al. 2015). However, limitations to

55 these methods are present such as observer biases. Nearly every video was watched by a single individual to reduce the chance of one species being identified differently by multiple viewers, nevertheless there is also the chance of misidentification by the main viewer. With the assistance of recordings as opposed to real-time underwater viewing, the chances are reduced, but days with poor lighting and visibility make identification difficult. Some fish would appear as a dark outline making some species only distinguishable by colouration, problematic.

Given time and resource limitations, along with the lack of baseline data for which this study could further expand upon, measuring station uses and fish behaviour was the most effective approach to gain a basic understanding of the cleaning station’s ecology.

4.7 Conclusion Research focussing on cleaner and client interactions has been conducted; however documentation of cleaning station ecology with an emphasis on other interactions within these habitats is absent. Information presented in this study expands our knowledge on the ecology of cleaning stations and what purposes, aside from cleaning, these habitats serve for various species. Patterns and trends of species composition at three cleaning stations in Bateman Bay, Western Australia were examined, highlighting their similarities and differences.

Similarities in species composition are apparent between comparable benthic habitats, but the use of cleaning stations by these fish varies. Cleaning stations which are distinctively different in water movement and topography show expected differences with certain species. Although cleaning events between Labroides dimidiatus and prospective clients are seen at each station, it was not the most prominent use of the

56 station by visitors and residents. Each station showed variations of uses from feeding, providing shelter for resident fish, areas for roaming and hunting. From this it can be determined that depending on the species and habitat, cleaning stations can be used for different purposes; behaviours such as parrotfish feeding on Sargassum are likely to be contributing to maintaining the health of the cleaning station for its residents.

The patterns of visitation to cleaning stations by M. alfredi each year are still poorly understood. Due to the vast differences between Oyster Bridge and Point Maud, variances in benthic composition are unlikely to be responsible. It is however, conceivable the species and families commonly seen at each site serve as visual cues to manta rays as healthy and dependable cleaning stations, with the ability to provide sufficient cleaning services. Further research into the station preferences of the manta rays of Ningaloo Reef, with additional studies on cleaning stations not used by manta rays for comparison will assist in the understanding of this behaviour. With continuous monitoring of cleaning station ecology, predictors of station health could be achieved and used as baseline data for additional sites. Cleaning stations are important habitats with proven benefits to coral reef and fish health, reduced stress of its inhabitants, and an increase in fish diversity. These stations are used by many species including M. alfredi and should be better understood on a broader scale, with the possibility of protection from fishing pressures to assist in maintaining its integrity.

5.0 References

Abe, T., K. Sekiguchi, H. Onishi, K. Muramatsu, and T. Kamito. 2012. Observations on a

school of ocean sunfish and evidence for a symbiotic cleaning association with

albatrosses. Marine Biology 159:1173-1176.

Abel, E. F. 1971. On the Ethology of Cleaning Symbiosis between European Fresh Water

Fishes in Their Natural Habitat. Oecologia 6:133-151.

Allen, G. 2009. Field Guide to Marine Fishes of Tropical Australia and South-East Asia.

Fourth edition. Western Australian Museum, Welshpool, Western Australia.

Anderson, D. J., H. T. Kobryn, B. M. Norman, L. Bejder, J. A. Tyne, and N. R. Loneragan.

2014. Spatial and temporal patterns of nature-based tourism interactions with

whale sharks (Rhincodon typus) at Ningaloo Reef, Western Australia. Estuarine,

Coastal and Shelf Science 148:109-119.

Anderson, M., R. N. Gorley, and R. K. Clarke. 2008. Permanova+ for Primer: Guide to

Software and Statisticl Methods.

Anderson, M. J. 2001. A new method for non-parametric multivariate analysis of

variance. Austral Ecology 26:32-46.

Anderson, R. C., M. S. Adam, and J. I. Goes. 2011. From monsoons to mantas: seasonal

distribution of Manta alfredi in the Maldives. Fisheries oceanography 20:104-

113.

Armstrong, A. O., A. J. Armstrong, F. R. A. Jaine, L. I. E. Couturier, K. Fiora, J. Uribe-

Palomino, S. J. Weeks, K. A. Townsend, M. B. Bennett, and A. J. Richardson.

2016. Prey Density Threshold and Tidal Influence on Reef Manta Ray Foraging

at an Aggregation Site on the Great Barrier Reef. PLoS One 11:e0153393.

Arnal, C., and I. M. Côté. 1998. Interactions between cleaning gobies and territorial

damselfish on coral reefs. Animal Behaviour 55:1429-1442. 58

Arnal, C., I. M. Côté, and S. Morand. 2001. Why Clean and Be Cleaned? The Importance

of Client Ectoparasites and Mucus in a Marine Cleaning Symbiosis. Behavioral

Ecology and Sociobiology 51:1-7.

Arnal, C., and S. Morand. 2001. Importance of ectoparasites and mucus in cleaning

interactions in the Mediterranean cleaner wrasse Symphodus melanocercus.

Marine Biology 138:777-784.

Baliga, V. B., and C. J. Law. 2015. Cleaners among wrasses: Phylogenetics and

evolutionary patterns of cleaning behavior within Labridae. Molecular

Phylogenetics and Evolution 94, Part A:424-435.

Bansemer, C., A. S. Grutter, and R. Poulin. 2002. Geographic Variation in the Behaviour

of the Cleaner Fish Labroides dimidiatus (Labridae). Ethology 108:353-366.

Becker, J. H., and A. S. Grutter. 2004. Cleaner shrimp do clean. Coral Reefs 23:515-520.

Bell, J., and R. Galzin. 1984. Influence of live coral cover on coral-reef fish communities.

Marine Ecology Progress Series 15:265-274.

Bellwood, D., and P. Wainwright. 2001. Locomotion in labrid fishes: implications for

habitat use and cross-shelf biogeography on the Great Barrier Reef. Coral Reefs

20:139-150.

Bellwood, D. R., and T. P. Hughes. 2001. Regional-Scale Assembly Rules and

Biodiversity of Coral Reefs. Science 292:1532-1535.

Bellwood, D. R., T. P. Hughes, and A. S. Hoey. 2006. Sleeping Functional Group Drives

Coral-Reef Recovery. Current Biology 16:2434-2439.

Bellwood, D. R., and P. C. Wainwright. 2002. Chapter 1 - The History and Biogeography

of Fishes on Coral Reefs A2 - Sale, Peter F. Pages 5-32 Coral Reef Fishes.

Academic Press, San Diego, California.

Bond, W. J. 1994. Keystone Species. Pages 237-253 in E.-D. Schulze and H. A. Mooney,

editors. Biodiversity and Ecosystem Function. Springer Berlin Heidelberg, Berlin,

Heidelberg.

Braun, C. D., G. B. Skomal, S. R. Thorrold, and M. L. Berumen. 2015. Movements of the

reef manta ray (Manta alfredi) in the Red Sea using satellite and acoustic

telemetry. Marine Biology 162:2351-2362.

Bshary, R. 2001. Chapter 7: The cleaner fish market. Pages 146-172 in R. Noe, J. van

Hoof, and P. Hammersein, editors. Economics in Nature. Caimbridge University

Press, New York.

Bshary, R. 2003. The cleaner wrasse, Labroides dimidiatus, is a key organism for reef

fish diversity at Ras Mohammed National Park, Egypt. Journal of Animal Ecology

72:169-176.

Bshary, R., and A. S. Grutter. 2002. Asymmetric cheating opportunities and partner

control in a cleaner fish mutualism. Animal Behaviour 63:547-555.

Bshary, R., A. S. Grutter, A. S. T. Willener, and O. Leimar. 2008. Pairs of cooperating

cleaner fish provide better service quality than singletons. Nature 455:964-966.

Bshary, R., and R. Noë. 2003. Chapter 9: The ubiquitous influence of partner choice on

the dynamics of cleaner fish–client reef fish interactions. Pages 167-184. in P.

Hammerstein, editor. Genetic and cultural evolution of cooperation. The MIT

Press, Caimbridge, Massachusetts.

Bshary, R., and D. Schäffer. 2002. Choosy reef fish select cleaner fish that provide high-

quality service. Animal Behaviour 63:557-564.

Bshary, R., and M. Würth. 2001. Cleaner fish Labroides dimidiatus manipulate client

reef fish by providing tactile stimulation. Proceedings of the Royal Society of

London B: Biological Sciences 268:1495-1501. 60

Cappo, M., P. Speare, and G. De'ath. 2004. Comparison of baited remote underwater

video stations (BRUVS) and prawn (shrimp) trawls for assessments of fish

biodiversity in inter-reefal areas of the Great Barrier Reef Marine Park. Journal

of Experimental Marine Biology and Ecology 302:123-152.

Carpenter, R. C., and P. J. Edmunds. 2006. Local and regional scale recovery of Diadema

promotes recruitment of scleractinian corals. Ecology Letters 9:271-280.

Cassata, L., and L. B. Collins. 2008. Coral reef communities, habitats, and substrates in

and near sanctuary zones of Ningaloo Marine Park. Journal of Coastal Research

24:139+.

Catlin, J., and R. Jones. 2010. Whale shark tourism at Ningaloo Marine Park: A

longitudinal study of wildlife tourism. Tourism Management 31:386-394.

Cheney, K. L., and I. M. Côté. 2001. Are Caribbean cleaning symbioses mutualistic?

Costs and benefits of visiting cleaning stations to longfin damselfish. Animal

Behaviour 62:927-933.

Clague, G. E., K. L. Cheney, A. W. Goldizen, M. I. McCormick, P. A. Waldie, and A. S.

Grutter. 2011. Long-term cleaner fish presence affects growth of a coral reef

fish. Biology Letters 7:863-865.

Clark, T. B., Y. P. Papastamatiou, and C. G. Meyer. 2008. Intestinal eversion in a free-

ranging manta ray (Manta birostris). Coral Reefs 27:61-61.

Clarke, K. R. 1993. Non-parametric multivariate analyses of changes in community

structure. Australian Journal of Ecology 18:117-143.

Clarke, K. R., and R. N. Gorley. 2015. PRIMER v7: User Manual/Tutorial. PRIMER-E,

Plymouth.

Cole, A. J., M. S. Pratchett, and G. P. Jones. 2008. Diversity and functional importance

of coral‐feeding fishes on tropical coral reefs. Fish and Fisheries 9:286-307. 61

Côté, I. M. 2000. Evolution and ecology of cleaning symbioses in the sea.

Oceanography and Marine Biology 38:311-355.

Côté, I. M., C. Arnal, and J. Reynolds. 1998. Variation in posing behaviour among fish

species visiting cleaning stations. Journal of Fish Biology 53:256-266.

Côté, I. M., and K. L. Cheney. 2004. Distance–dependent costs and benefits of

aggressive mimicry in a cleaning symbiosis. Proceedings of the Royal Society of

London B: Biological Sciences 271:2627-2630.

Couturier, L. I. E., C. L. Dudgeon, K. H. Pollock, F. R. A. Jaine, M. B. Bennett, K. A.

Townsend, S. J. Weeks, and A. J. Richardson. 2014. Population dynamics of the

reef manta ray Manta alfredi in eastern Australia. Coral Reefs 33:329-342.

Couturier, L. I. E., F. R. A. Jaine, K. A. Townsend, S. J. Weeks, A. J. Richardson, and M. B.

Bennett. 2011. Distribution, site affinity and regional movements of the manta

ray, Manta alfredi (Krefft, 1868), along the east coast of Australia. Marine and

Freshwater Research 62:628-637.

Couturier, L. I. E., A. D. Marshall, F. R. A. Jaine, T. Kashiwagi, S. J. Pierce, K. A.

Townsend, S. J. Weeks, M. B. Bennett, and A. J. Richardson. 2012. Biology,

ecology and conservation of the Mobulidae. Journal of Fish Biology 80:1075-

1119.

Croll, D. A., H. Dewar, N. K. Dulvy, D. Fernando, M. P. Francis, F. Galván-Magaña, M.

Hall, S. Heinrichs, A. Marshall, D. McCauley, K. M. Newton, G. Notarbartolo-Di-

Sciara, M. O'Malley, J. O'Sullivan, M. Poortvliet, M. Roman, G. Stevens, B. R.

Tershy, and W. T. White. 2016. Vulnerabilities and fisheries impacts: the

uncertain future of manta and devil rays. Aquatic Conservation: Marine and

Freshwater Ecosystems 26:562-575.

D'Adamo, N., and C. J. Simpson. 2001. Review of the oceanography of Ningaloo Reef

and adjacent waters: Marine Management Support, Ningaloo. Department of

Conservation and Land Management, Marine Conservation Branch, Fremantle,

Western Australia.

Davis, T., D. Harasti, and S. D. Smith. 2015. Compensating for length biases in

underwater visual census of fishes using stereo video measurements. Marine

and Freshwater Research 66:286-291.

Daw, B. H. 2009. Management of Manta Ray Interactive Tourism in Ningaloo Marine

Park Western Australia.in Department of Environment and Conservation.

Western Australia.

Deakos, M. H. 2010. The ecology and social behavior of a resident manta ray (M.

alfredi) population off Maui, Hawaii. University of Hawaii Manoa.

Department of Parks and Wildlife, and Department of Fisheries. 2014. Ningaloo Marine

Park Sanctuary Zones and Murion Islands Marine Management Area.in

Australian Government, editor. Exmouth, Western Australia.

Dewar, H., P. Mous, M. Domeier, A. Muljadi, J. Pet, and J. Whitty. 2008. Movements

and site fidelity of the giant manta ray, Manta birostris, in the Komodo Marine

Park, Indonesia. Marine Biology 155:121-133.

Ferreira, D. E. L., A. C. Peret, and R. Coutinho. 1998. Seasonal grazing rates and food

processing by tropical herbivorous fishes. Journal of Fish Biology 53:222-235.

Francini–Filho, R., R. Moura, and I. Sazima. 2000. Cleaning by the wrasse Thalassoma

noronhanum, with two records of predation by its grouper client Cephalopholis

fulva. Journal of Fish Biology 56:802-809.

Frias-Torres, S., H. Goehlich, C. Reveret, and P. H. Montoya-Maya. 2015. Reef fishes

recruited at midwater coral nurseries consume biofouling and reduce cleaning

time in Seychelles, Indian Ocean. African Journal of Marine Science 37:421-426.

Friedlander, A. M., and J. D. Parrish. 1998. Habitat characteristics affecting fish

assemblages on a Hawaiian coral reef. Journal of Experimental Marine Biology

and Ecology 224:1-30.

Gadig, O. B. F., and D. G. Neto. 2014. Notes on the feeding behaviour and swimming

pattern of Manta alfredi (Chondrichthyes, Mobulidae) in the Red Sea. acta

ethologica 17:119-122.

Germanov, E. S., and A. D. Marshall. 2014. Running the gauntlet: regional movement

patterns of Manta alfredi through a complex of parks and fisheries. PLoS One

9:e110071.

Giuggioli, L., and F. Bartumeus. 2012. Linking animal movement to site fidelity. Journal

of Mathematical Biology 64:647-656.

Glynn, P. W. 1974. The impact of Acanthaster on corals and coral reefs in the eastern

Pacific. Environmental Conservation 1:295-304.

Gochfeld, D. J. 2004. Predation-induced morphological and behavioral defenses in a

hard coral: implications for foraging behavior of coral-feeding butterflyfishes.

Marine Ecology Progress Series 267:145-158.

Grutter, A. S. 1995. Relationship between cleaning rates and ectoparasite loads in coral

reef fishes. Marine Ecology Progress Series 118:51-58.

Grutter, A. S. 1996a. Experimental demonstration of no effect by the cleaner wrasse

Labroides dimidiatus (Cuvier and Valenciennes) on the host fish Pomacentrus

moluccensis (Bleeker). Journal of Experimental Marine Biology and Ecology

196:285-298. 64

Grutter, A. S. 1996b. Parasite removal rates by the cleaner wrasse Labroides

dimidiatus. Marine Ecology Progress Series 130:61-70.

Grutter, A. S. 1997. Spatiotemporal Variation and Feeding Selectivity in the Diet of the

Cleaner Fish Labroides dimidiatus. Copeia 1997:346-355.

Grutter, A. S. 1999. Cleaner fish really do clean. Nature 398:672-673.

Grutter, A. S. 2004. Cleaner Fish Use Tactile Dancing Behavior as a Preconflict

Management Strategy. Current Biology 14:1080-1083.

Grutter, A. S., and R. Bshary. 2004. Cleaner fish, Labroides dimidiatus, diet preferences

for different types of mucus and parasitic gnathiid isopods. Animal Behaviour

68:583-588.

Grutter, A. S., J. M. Murphy, and J. H. Choat. 2003. Cleaner fish drives local fish

diversity on coral reefs. Current Biology 13:64-67.

Guimarães, P. R., C. Sazima, S. F. d. Reis, and I. Sazima. 2007. The nested structure of

marine cleaning symbiosis: is it like flowers and bees? Biology Letters 3:51-54.

Heithaus, M. R., A. Frid, A. J. Wirsing, and B. Worm. 2008. Predicting ecological

consequences of marine top predator declines. Trends in ecology & evolution

23:202-210.

Heupel, M. R., C. A. Simpfendorfer, and R. Fitzpatrick. 2010. Large–Scale Movement

and Reef Fidelity of Grey Reef Sharks. PLoS One 5:e9650.

Hixon, M. A. 2015. Predation: piscivory and the ecology of coral-reef fishes. Pages 41-

52 in C. Mora, editor. Ecology of Fishes on Coral Reefs. Caimbridge University

Press, Caimbridge.

Hobson, E. S. 1971. Cleaning symbiosis among California inshore fishes. Fishery Bulletin

69:491-523.

Homma, K., T. Maruyama, T. Itoh, and H. Ishihara. 1999. Biology of the Manta ray,

Manta birostris Walbaum, in the Indo-Pacific. Pages 209-216 in Proceedings of

the 5th Indo-Pacific Fish conference, Noumea - New Caledonia, 3-8 November

1997.

Huebner, L. K., and N. E. Chadwick. 2012. Reef fishes use sea anemones as visual cues

for cleaning interactions with shrimp. Journal of Experimental Marine Biology

and Ecology 416–417:237-242.

Hughes, T. P., N. A. Graham, J. B. Jackson, P. J. Mumby, and R. S. Steneck. 2010. Rising

to the challenge of sustaining coral reef resilience. Trends in ecology &

evolution 25:633-642.

Jaine, F. R., L. I. Couturier, S. J. Weeks, K. A. Townsend, M. B. Bennett, K. Fiora, and A. J.

Richardson. 2012. When giants turn up: sighting trends, environmental

influences and habitat use of the manta ray Manta alfredi at a coral reef. PLoS

One 7:e46170.

Jones, T., M. Hughes, D. Wood, A. Lewis, and P. Chandler. 2009. Ningaloo Coast Region

Visitor Statistics.in Sustainable Tourism Cooperative Research Centre, editor.

Cooperative Research Centre, Gold Coast, Australia.

Kitchen-Wheeler, A.-M. 2010. Visual identification of individual manta ray (Manta

alfredi) in the Maldives Islands, Western Indian Ocean. Marine Biology Research

6:351-363.

Kitchen-Wheeler, A.-M., C. Ari, and A. J. Edwards. 2012. Population estimates of Alfred

mantas (Manta alfredi) in central Maldives atolls: North Male, Ari and Baa.

Environmental Biology of Fishes 93:557-575.

Lafferty, K. D., and A. K. Morris. 1996. Altered behavior of parasitized killifish increases

susceptibility to predation by bird final hosts. Ecology 77:1390-1397. 66

Limbaugh, C. 1961. Cleaning Symbiosis. Pages 42-49. Scientific American 205:42-49.

Little, R., O. Thebaud, and B. Fulton. 2014. Evaluation of management strategies in

Ningaloo Marine Park, Western Australia. International Journal of Sustainable

Society 6:102-119

Losey, G. S. 1972. Ecological Importance of Cleaning Symbiosis. Copeia:820-833.

Losey, G. S. 1974. Cleaning Symbiosis in Puerto Rico with Comparison to the Tropical

Pacific. Copeia 1974:960-970.

Losey, G. S., G. H. Balazs, and L. A. Privitera. 1994. Cleaning symbiosis between the

wrasse, Thalassoma duperry, and the green turtle, Chelonia mydas. Copeia:684-

690.

Luiz Jr, O. J., A. P. Balboni, G. Kodja, M. Andrade, and H. Marum. 2009. Seasonal

occurrences of Manta birostris (Chondrichthyes: Mobulidae) in southeastern

Brazil. Ichthyological Research 56:96-99.

Luiz, O. J., E. M. P. Madin, J. S. Madin, A. H. Baird, and A. S. Grutter. 2016. A tropical

cleaner wrasse finds new clients at the frontier. Frontiers in Ecology and the

Environment 14:110-111.

Marshall, A. D., and M. B. Bennett. 2010a. The frequency and effect of shark-inflicted

bite injuries to the reef manta ray Manta alfredi. African Journal of Maine

Science 32:573-580.

Marshall, A. D., and M. B. Bennett. 2010b. Reproductive ecology of the reef manta ray

Manta alfredi in southern Mozambique. Journal of Fish Biology 77:169-190.

Marshall, A. D., L. J. V. Compagno, and M. B. Bennett. 2009. Redescription of the genus

Manta with resurrection of Manta alfredi (Krefft, 1868) (Chondrichthyes;

Myliobatoidei; Mobulidae). Zootaxa:1-28.

Marshall, J. N. 2000. Communication and camouflage with the same ‘bright’ colours in

reef fishes. Philosophical Transactions of the Royal Society of London B:

Biological Sciences 355:1243-1248.

McCauley, D. J., P. A. DeSalles, H. S. Young, Y. P. Papastamatiou, J. E. Caselle, M. H.

Deakos, J. P. A. Gardner, D. W. Garton, J. D. Collen, and F. Micheli. 2014.

Reliance of mobile species on sensitive habitats: a case study of manta rays

(Manta alfredi) and lagoons. Marine Biology 161:1987-1998.

McClanahan, T. 2000. Recovery of a coral reef keystone predator, Balistapus undulatus,

in East African marine parks. Biological Conservation 94:191-198.

McGregor, F., M. Van Keulen, A. Waite, and M. Meekan. 2008. Foraging Ecology and

Population Dynamics of the Manta Ray, Manta birostris in Lagoonal Waters of

Ningaloo Reef, Western Australia.in Joint Meeting of Ichthyologists and

Herpetologists, Montreal, Canada.

Moller, A., P. Christe, and E. Lux. 1999. Parasitism, host immune function, and sexual

selection. Quarterly Review of Biology74:3-20.

Mourier, J. 2012. Manta rays in the Marquesas Islands: first records of Manta birostris

in French Polynesia and most easterly location of Manta alfredi in the Pacific

Ocean, with notes on their distribution. Journal of Fish Biology 81:2053-2058.

MPRA, C. 2005. Management plan for the Ningaloo Marine Park and Muiron Islands

Marine Management Area: 2005–2015. Perth, Western Australia: Conservation

and Land Management and Marine Parks and Reserves Authority, Government

of Western Australia 111.

Mumby, P. J., C. P. Dahlgren, A. R. Harborne, C. V. Kappel, F. Micheli, D. R. Brumbaugh,

K. E. Holmes, J. M. Mendes, K. Broad, and J. N. Sanchirico. 2006. Fishing, trophic

cascades, and the process of grazing on coral reefs. Science 311:98-101. 68

National Marine Sanctuaries,. 2013. Manta Rays.

http://flowergarden.noaa.gov/newsevents/namecontestarticle.html

O'Malley, M. P., K. Lee-Brooks, and H. B. Medd. 2013. The Global Economic Impact of

Manta Ray Watching Tourism. PLoS One 8:e65051.

O'Shea, O. R., M. J. Kingsford, and J. Seymour. 2010. Tide-related periodicity of manta

rays and sharks to cleaning statiosn on a coral reef. CSIRO 61:65-73.

Oates, J., A. Manica, and R. Bshary. 2010. The shadow of the future affects cooperation

in a cleaner fish. Current Biology 20:R472-R473.

Oliver, S. P., N. E. Hussey, J. R. Turner, and A. J. Beckett. 2011. Oceanic sharks clean at

coastal seamount. PLoS One 6:e14755.

Osada, K. 2010. Relationship of Zooplankton Emergence, Manta Ray Abundance: And

SCUBA Diver Usage Kona Hawaii. University of Hawai'i at Hilo.

Pauly, D., and R. Watson. 2005. Background and interpretation of the ‘Marine Trophic

Index’ as a measure of biodiversity. Philosophical Transactions of the Royal

Society B: Biological Sciences 360:415-423.

Pearce, A., and C. Pattiaratchi. 1999. The Capes Current: a summer countercurrent

flowing past Cape Leeuwin and Cape Naturaliste, Western Australia.

Continental Shelf Research 19:401-420.

Randall, J. E. 1958. A review of the labrid fish genus Labroides, with descriptions of two

new species and notes on ecology. Pac Sci 12:324 - 347.

Randall, J. E. 2005. A review of mimicry in marine fishes. Zoological Studies 44:299-328.

Robertson, D. R. 1984. Cohabitation of Competing Territorial Damselfishes on a

Caribbean Coral Reef. Ecology 65:1121-1135.

Roff, G., C. Doropoulos, A. Rogers, Y.-M. Bozec, N. C. Krueck, E. Aurellado, M. Priest, C.

Birrell, and P. J. Mumby. 2016. The ecological role of sharks on coral reefs.

Trends in ecology & evolution 31:395-407.

Rohner, C. A., S. J. Pierce, A. D. Marshall, and S. J. Weeks. 2013. Trends in sightings and

environmental influences on a coastal aggregation of manta rays and whale

sharks. Marine ecology. Progress series (Halstenbek) 482:153-168.

Sazima, C., A. Grossman, and I. Sazima. 2010. Turtle cleaners: reef fishes foraging on

epibionts of sea turtles in the tropical Southwestern Atlantic, with a summary

of this association type. Neotropical Ichthyology 8:187-192.

Sazima, I., R. L. Moura, and J. Luiz Gasparini. 1998. The Wrasse Halichoeres

Cyanocephalus (labridae) as a Specialized Cleaner Fish. Bulletin of Marine

Science 63:605-610.

Severo-Neto, F., and O. Froehlich. 2016. Cleaning behaviour of the cichlid Mesonauta

festivus in the Pantanal wetlands: evidence of a potential freshwater cleaning

station. Marine and Freshwater Behaviour and Physiology 49:63-68.

Sirakaya, E., V. Sasidharan, and S. Sönmez. 1999. Redefining Ecotourism: The Need for

a Supply-Side View. Journal of Travel Research 38:168-172.

Soares, M. C., R. Bshary, S. C. Cardoso, and I. M. Côté. 2008. The Meaning of Jolts by

Fish Clients of Cleaning Gobies. Ethology 114:209-214.

Soares, M. C., S. C. Cardoso, and I. M. Côté. 2007. Client preferences by Caribbean

cleaning gobies: food, safety or something else? Behavioral Ecology and

Sociobiology 61:1015-1022.

Springer, V. G., and W. F. Smith-Vaniz. 1972. Mimetic relationships involving fishes of

the family Blenniidae. Smithsonian Contributions to Zoology:1-36.

Stummer, L. E., J. A. Weller, M. L. Johnson, and I. M. Côté. 2004. Size and stripes: how

fish clients recognize cleaners. Animal Behaviour 68:145-150.

Sun, D., K. L. Cheney, J. Werminghausen, E. C. McClure, M. G. Meekan, M. I.

McCormick, T. H. Cribb, and A. S. Grutter. 2016. Cleaner wrasse influence

habitat selection of young damselfish. Coral Reefs 35:427-436.

Swainston, R. 2010. Swainston's Fishes of Australia. Penguin Group, New York, New

York.

U.S. Fish and Wildlife Service. 2016.

https://www.fws.gov/international/cites/cop16/manta-rays.html. van Keulen, M. 2002. Chapter 2: Algae. In: Fitzpatrick, B.M. and Penrose, H.M. (eds) A

preliminary marine ecological sturvey of Bateman Bay, Ningaloo Reef. Page 58.

Oceanwise Environmental Scientists, Perth, Western Australia.

Venables, S., F. McGregor, L. Brain, and M. van Keulen. 2016. Manta ray tourism

management, precautionary strategies for a growing industry: a case study

from the Ningaloo Marine Park, Western Australia. Pacific Conservation

Biology:-.

Watson, D. L., E. S. Harvey, B. M. Fitzpatrick, T. J. Langlois, and G. Shedrawi. 2010.

Assessing reef fish assemblage structure: how do different stereo-video

techniques compare? Marine Biology 157:1237-1250.

White, W. T., J. Giles, Dharmadi, and I. C. Potter. 2006. Data on the bycatch fishery and

reproductive biology of mobulid rays (Myliobatiformes) in Indonesia. Fisheries

Research 82:65-73.

Whiteman, E., and I. Côté. 2002. Cleaning activity of two Caribbean cleaning gobies:

intra‐and interspecific comparisons. Journal of Fish Biology 60:1443-1458.

Wilson, S. K., A. M. Dolman, A. J. Cheal, M. J. Emslie, M. S. Pratchett, and H. P. A.

Sweatman. 2009. Maintenance of fish diversity on disturbed coral reefs. Coral

Reefs 28:3-14.

Woo, M., C. Pattiaratchi, and W. Schroeder. 2006. Dynamics of the Ningaloo Current

off Point Cloates, Western Australia. Marine and Freshwater Research 57:291-

301.

Yano, K., F. Sato, and T. Takahashi. 1999. Observations of mating behavior of the manta

ray,manta birostris, at the ogasawara islands, japan. Ichthyological Research

46:289-296.