Alexandra S Grutter

University of Queensland | UQ · School of Biological Sciences

Settlement patterns of juvenile fish shape coral reef communities. During the recruitment process, predation rates are extremely high. However, the role that parental care plays in reducing mortality, especially by cryptic natural enemies such as parasites, remains largely unstudied. We investigated whether parental care in the spiny chromis damsel...

Gnathia antennacrassa sp. nov. from seagrass beds off Rottnest Island, Western Austra- lia is the first record of any gnathiid from the entirety of Western Australia; the male can be distinguished from congeners by the stout peduncular articles of the antenna. Gnath- ia taurus sp. nov. is described from two adult specimens reared from praniza larva...

Connectivity between habitats and ecological communities is a critical component of trophic structure. Coral reef systems include reef, seagrass, and mangrove habitats, and the movement of fishes is a key component of habitat connectivity among them. Fishes that undergo diel migrations between habitats are among the best-studied functional groups....

Grazing fishes farm algae, and consume algae, detritus and sediment and consequently differentially modify benthic communities. Manipulations of cleaner fish Labroides dimidiatus on reefs show that cleaners affect fish abundance differently according to grazer functional group. Accordingly, whether reefs are grazed differently, with consequences fo...

Cleaning symbiosis is critical for maintaining healthy biological communities in tropical marine ecosystems. However, potential negative impacts of mutualism, such as the transmission of pathogens and parasites during cleaning interactions, have rarely been evaluated. Here, we investigated whether the dedicated bluestreak cleaner wrasse Labroides d...

Cleaning symbioses are key mutualistic interactions where cleaners remove ectoparasites and tissues from client fishes. Such interactions elicit beneficial effects on clients’ ecophysiology, with cascading effects on fish diversity and abundance. Ocean acidification (OA), resulting from increasing CO2 concentrations, can affect the behavior of clea...

Coral reef mutualisms involve complex trophic ecological relationships that produce indirect effects. Excluding mutualistic cleaner fish Labroides dimidiatus from reefs indirectly increases the abundance of many fishes and reduces demersal stages of their ectoparasitic prey (gnathiid isopods). Whether cleaners affect populations of planktivorous fi...

Widespread coral mortality is leading to coral reef degradation worldwide. Many juvenile reef fishes settle on live coral, and their predator-avoidance behaviour is disrupted in seawater exposed to dead corals, ultimately increasing predation risk. Gnathiid isopods are micropredatory fish ectoparasites that occur in higher abundances in dead coral....

Aim Several drivers explain the global distribution of all reef fish. However, whether these drivers also explain the distribution and traits of a functional subgroup involving cleaner fishes remain unclear. Here we examine the variation in traits of cleaner fishes and test whether historical, environmental, ecological and geographical drivers are...

For the last seven decades, cleaning sym-biosis in the marine environment has been a research field of intrigue. There is substantial evidence that, by removing undesired items from their client fishes, cleaner organisms have positive ecosystem effects. These include increased fish recruitment, abundance and enhanced fish growth. However, the intim...

Game-theoretical models help us understand how and when cooperation can evolve and persist. However, current models fall short of explaining the striking amount of variation in cooperation levels that we observe in nature, even within a system. For example, an animal's ability to choose partners with which to interact can explain the maintenance of...

Cleaner fish remove parasites from other organisms, called clients. While there is an extensive body of work on the positive role of cleaners for their clients and reef communities, remarkably, potential parasites hosted by specialised cleaner fishes themselves have not been explored. In this study, we surveyed the parasite community of the Indo-Pa...

Gnathiid isopods, common fish ectoparasites, can affect fish physiology, behaviour and survival. Gnathiid juveniles emerge from the benthos to feed on fish blood. In the Caribbean, gnathiids are positively associated with dead coral and negatively associated with live coral, due to coral predation on gnathiids. However, such interactions were unstu...

In many mutualisms, benefits in the form of food are exchanged for services such as transport or protection. In the marine cleaning mutualism, a variety of “client” reef fishes offer “cleaner” fish Labroides dimidiatus access to food in the form of their ectoparasites, where parasite removal supposedly protects the clients. Yet, the health benefits...

Extreme warming events that contribute to mass coral bleaching are occurring with increasing regularity, raising questions about their effect on coral reef ecological interactions. However, the effects of such events on parasite-host interactions are largely ignored. Gnathiid isopods are common, highly mobile, external parasites of coral reef fishe...

Parasites can account for a substantial proportion of the biomass in marine communities. As such, parasites play a significant ecological role in ecosystem functioning via host interactions. Unlike macropredators, such as large piscivores, micropredators rarely cause direct mortality. Rather, micropredators impose an energetic tax, thus significant...

Territorial and roving grazing fishes farm, and feed on, algae, sediment, or detritus, thus exerting different influences on benthic community structure, and are common clients of cleaner fish. Whether cleaners affect grazing-fish diversity and abundance, and indirectly the benthos, was tested using reefs maintained free of the bluestreak cleaner w...

The reliance of parasites on their hosts makes host-parasite interactions ideal models for exploring ecological and evolutionary processes. By providing a consistent supply of parasites, in vivo monocultures offer the opportunity to conduct experiments on a scale that is generally not otherwise possible. Gnathiid isopods are common ectoparasites of...

The juveniles of gnathiid isopods are one of the most common fish ectoparasites in marine habitats and cause deleterious effects on fish by feeding on host blood and lymph. Reef fishes tend to engage in cooperative interactions with cleaning organisms to reduce their ectoparasite load. Ocean acidification (OA) pose multiple threats to marine life....

To develop an evolutionary theory of social decision making, we require an understanding of how in- dividuals utilize environmental cues to form decision rules. We exposed ‘cleaner’ fish (bluestreak cleaner wrasse, Labroides dimidiatus) to a biological market task, where giving priority to an ephemeral (i.e. ‘visitor’ client) food plate, over a per...

Predation on parasites is an important ecological process, but few experimental studies have examined the long-term impacts on the prey. Cleaner fish prey upon large numbers and selectively feed on the larger individuals of the ectoparasitic stage of gnathiid isopods. Removal of cleaner fish Labroides dimidiatus for 1.5–12.5 years negatively affect...

Mass coral bleaching events due to rising seawater temperatures are occurring with increasing frequency and are among the most conspicuous consequences of human-induced climate change. While bleaching events have clear impacts on the corals themselves, the impacts on other organisms and on the overall reef community are more difficult to assess. Th...

The pelagic larval stage is a critical component of the life cycle of most coral reef fishes, but the adaptive significance of this stage remains controversial. One hypothesis is that migrating through the pelagic environment reduces the risk a larval fish has of being parasitised. Most organisms interact with parasites, often with significant, det...

Benthic stages of cultured fishes’ ectoparasites are a major contributor to persistent reinfections in aquaculture. These stages are resistant to chemical therapies and are costly to manage in terms of time and labour. Cleaner shrimp, unlike cleaner fishes, prey on benthic stages, suggesting they have the potential to reduce parasite reinfection pr...

Chemical use is widespread in aquaculture to treat parasitic diseases in farmed fish. Cleaner fish biocontrols are increasingly used in fish farming as an alternative to medicines. However, cleaner fish are susceptible to some of their clients' parasites and their supply is largely dependent on wild harvest. In comparison, cleaner shrimp are not su...

Aim We studied the underlying biotic and abiotic drivers of network patterns in marine cleaning mutualisms (species feeding upon ectoparasites and injured tissues of others) at large spatial scales. Location: Eleven marine biogeographical provinces. Time period: 1971–2018. Major taxa studied: Reef fish and shrimps. Methods We combined field and li...

Reef fishes sustain injuries from various behavioural and environmental interactions. Injured fishes have been observed frequenting cleaning stations to be attended by different cleaner fishes. This symbiotic relationship between injured fishes and cleaner fishes has only been observed in the wild, and has never been demonstrated empirically for cl...

Cleaning organisms play a fundamental ecological role by removing ectoparasites and infected tissue from client surfaces. We used the well-studied cleaning mutualisms involving the cleaner wrasse,Labroides dimidiatus,to test how client cognition is affected by ectoparasites and whether these effects are mitigated by cleaners. Ambon damselfish (Poma...

Mutualisms are pivotal in shaping ecological communities. Iconic images of cleaner fish entering the mouths of predatory fish clients to remove ectoparasites epitomize their mutual benefit. Experimental manipulations of cleaner wrasse reveal declines in fish size and growth, and population abundance and diversity of client fishes in the absence of...

The transition between the planktonic and the benthic habitat is a critical period for the larvae of many demersal marine organisms. Understanding the potential constraints on the timing of this habitat transition, called settlement, is important to understanding their biology. Size-specific mortality can set the limits on lifestyle and help explai...

Many species engage in mutualistic relationships with other species. The physiological mechanisms that affect the course of such social interactions are little understood. In the cleaning mutualism, cleaner fish Labroides dimidiatus do not always act cooperatively by eating ectoparasites, but sometimes cheat by taking bites of mucus from so-called...

Cleaning symbiosis has been documented extensively in the marine environment over the past 50 years. We estimate global cleaner diversity comprises 208 fish species from 106 genera representing 36 families and 51 shrimp species from 11 genera representing 6 families. Cleaning symbiosis as originally defined, is amended to highlight communication be...

On coral reef systems, ‘client’ fishes combat relentless ectoparasitic infections by engaging in frequent mutualistic interactions with various ‘cleaner’ organisms. Clients are known to adjust their visits to cleaners according to their ectoparasite load. Whether physiological changes due to the ectoparasitic infection, prior to engaging in cleanin...

Generalized rule application promotes flexible behavior by allowing individuals to adjust quickly to environmental changes through generalization of previous learning. Here, we show that bluestreak 'cleaner' wrasse (Labroides dimidiatus) uses generalized rule application in their use of predators as social tools against punishing reef fish clients....

Species that exhibit ontogenetic variation in interspecific cleaning behaviours may offer insights into how interspecific cooperation evolves. We investigated the foraging ecology of the yellowtail tubelip wrasse (Diproctacanthus xanthurus), a facultative cleaner as a juvenile and corallivore as an adult, and compared its juvenile ecology with that...

Humans and other animals use previous experiences to make behavioural decisions, balancing the probabilities of receiving rewards or punishments with alternative actions. The dopaminergic system plays a key role in this assessment: for instance, a decrease in dopamine transmission, which is signalled by the failure of an expected reward, may elicit...

The presence of bluestreak cleaner wrasse, Labroides dimidiatus, on coral reefs increases total abundance and biodiversity of reef fishes. The mechanism(s) that cause such shifts in population structure are unclear, but it is possible that young fish preferentially settle into microhabitats where cleaner wrasse are present. As a first step to inves...

The cleaning behaviour of the bluestreak cleaner wrasse Labroides dimidiatus is extensively used as a model system for understanding cooperation. It feeds mainly on blood-sucking gnathiid isopods and also on the epidermal mucus of client fish; the nutritional quality of these foods, however, is unknown. The epidermal mucus of reef fish contains ult...

Mutualisms affect the biodiversity, distribution and abundance of biological communities. However, ecological processes that drive mutualism-related shifts in population structure are often unclear and must be examined to elucidate how complex, multi-species mutualistic networks are formed and structured. In this study, we investigated how the pres...

Animals establish privileged relationships with specific partners, which are treated differently from other conspecifics, and contribute to behavioral variation. However, there is limited information on the underlying physiological mechanisms involved in the establishment of these privileged ties and their relationship to individual cooperation lev...

Cleaning behavior is known as a classic example of cooperation between unrelated individuals. Although much is known of the behavioral processes underlying cooperative behavior, the physiological pathways mediating cooperation remain relatively obscure. Here, we show that altering the activity of serotonin on wild cleaner wrasses Labroides dimidiat...

Cleaning symbiosis encompasses a large diversity of organisms in reef systems, but has been mostly recorded at daytime. We report two instances of nocturnal cleaning by the shrimp Urocaridella sp. in a shipwreck at Tulamben, Bali, Indonesia. These cleaning episodes involved the pufferfish Arothron nigropunctatus and the rabbitfish Siganus studeri a...

Recent empirical research, mostly done on humans, recognizes that individuals' physiological state affects levels of cooperation. An individual's internal state may affect the payoffs of behavioural alternatives, which in turn could influence the decision to either cooperate or to defect. However, little is known about the physiology underlying con...

Deviations from model-based predictions of strategies leading to stable cooperation between unrelated individuals have raised considerable debate in regards to decision-making processes in humans. Here, we present data on cleaner wrasse (Labroides dimidiatus) that emphasize the importance of generalizing this discussion to other species, with the a...

Mimicry systems are frequently categorized by the type of benefit gained by the mimic's resemblance to its model: protection from threat, including predation (protective mimicry), and increased access to resources, including prey items (aggressive mimicry). These category types may not be mutually exclusive, and some mimics may gain more than one t...

Cleaner fishes are some of the most conspicuous organisms on coral reefs due to their behaviour and prominent body pattern, consisting of a lateral stripe and blue/yellow colouration. All obligate cleaner fishes share this body stripe pattern, which is an important signal for attracting client fishes. However, variability in the cleaning signal of...

High-energy wavelengths in the ultraviolet-B (UVB, 280-315 nm) and the UVA (315-400-nm) portion of the spectrum are harmful to terrestrial and aquatic organisms. Interestingly, UVA is also involved in the repair of UV induced damage. Organisms living in shallow coral reef environments possess UV absorbing compounds, such as mycosporine-like amino a...

In many instances of cooperation, only one individual has both the potential and the incentive to 'cheat' and exploit its partner. Under these asymmetric conditions, a simple model predicts that variation in the temptation to cheat and in the potential victim's capacity for partner control leads to shifts between exploitation and cooperation. Here,...

Investigations to determine whether juvenile gnathiid isopods are vectors of haemogregarines between coral reef fishes were undertaken at Lizard Island, Australia. Haemogregarina balistapi parasitaemias in triggerfish, Rhinecanthus aculeatus, decreased under gnathiid-free, laboratory conditions, compared with those in tagged R. aculeatus returned t...

Early life history traits, such as larval growth, influence the success of coral reef fish in the transition from the larval to the juvenile life phase. Few studies, however, have examined the relationship between parasites and growth in the early life history stages of such fishes. This study examined how parasite prevalence (% infected) and load,...

The cleaner fish Labroides dimidiatus affects the abundance of many fishes, including their juveniles, yet how they affect the post-settlement processes of conspecifics remains poorly known. Using a long-term experiment, where L. dimidiatus were regularly removed from seven patch reefs (removals) for 10 years or left undisturbed (controls) on nine,...

We investigated the effect of fishing on the behavior and abundance of the cleaner fish Labroides dimidiatus on the Great Barrier Reef, Australia, by comparing cleaner fish density (underwater visual census) and behavior (focal animal observations) at a fished and a no-take site. Cleaner fish density, as well as the number of individuals and specie...

In an interspecific cooperative context, individuals must be prepared to tolerate close interactive proximity to other species but also need to be able to respond to relevant social stimuli in the most appropriate manner. The neuropeptides vasopressin and oxytocin and their non-mammalian homologues have been implicated in the evolution of sociality...

Diet analyses and observations of cleaning behaviour of two cleaner fishes revealed that Labroides bicolor fed more on client mucus, but Labroides dimidiatus fed more on ectoparasites, and that L. bicolor interacted with fewer species (36 species) compared with L. dimidiatus (44 species). The client species which contributed most to the dissimilari...

Gnathia masca sp. nov. is described from material collected off Coconut Beach, Lizard Island, Great Barrier Reef, Australia. Males are characterised by a cephalosome with a shallow dorsal sulcus that stretches half its length, a slightly produced frontal border with two conical superior fronto-lateral processes and a conical inferior medio-frontal...

Joint group membership is of major importance for cooperation in humans, and close ties or familiarity with a partner are also thought to promote cooperation in other animals. Here, we present the opposite pattern: female cleaner fish, Labroides dimidiatus, behave more cooperatively (by feeding more against their preference) when paired with an unf...

Pygmy seahorses are a group of little-known miniature hippocampid fish that differ considerably in biology and ecology from their larger congeners. We estimated the population density, sex ratio and habitat of 2 sympatric, obligate gorgonian-associated pygmy seahorses, Hippocampus bargibanti and H. denise, in a 20 km long coastal marine protected a...

Here we report on intraspecific cleaning behaviour between two adult bluestreak cleaner wrasse Labroides dimidiatus of similar size on coral reefs surrounding Lizard Island, Great Barrier Reef, Australia. During a SCUBA dive, we observed these individuals posing and the resulting cleaning interactions. While aggression in this species is common bet...

In humans, physical stimulation, such as massage therapy, reduces stress and has demonstrable health benefi ts. Grooming in primates may have similar effects but it remains unclear whether the positive effects are due to physical contact or to its social value. Here we show that physical stimulation reduces stress in a coral reef fi sh, the surgeon...

Cleaning behaviour is considered to be a classical example of mutualism. However, no studies, to our knowledge, have measured the benefits to clients in terms of growth. In the longest experimental study of its kind, over an 8 year period, cleaner fish Labroides dimidiatus were consistently removed from seven patch reefs (61-285 m(2)) and left undi...