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Cleaning symbioses

Caribbean diving photographs compliments of Dr Karen Cheney, click to enter site Cleaning interactions provide an ideal model system to investigate the costs and benefits of mutualisms. Cleaning symbioses are heralded a textbook examples of mutualistic interactions in which one cleaning organism removes material from the body surface of a client individual.

Randall (1955, 1958) first found parasites in the gut of cleaners, suggesting a function for cleaning, and Limbaugh (1961) provided the first review of marine cleaning symbioses. Limbaugh (1961) also reported that after removing all cleaners from two small reefs in the Bahamas, he observed signs of declining health of reef fish. Fish remaining on the reef developed 'fuzzy white blotches, swelling, ulcerated sores and frayed fins'. This uncontrolled experiment led to a number of generalisations about cleaning symbioses, which long remained untested. In particular, it was perceived that cleaners were key organisms in determining the general patterns of distribution of other fish and, more important, that they played a crucial role in maintaining the health of their clients (Limbaugh 1961, Feder 1966). However, in the last three decades, the view of cleaning symbioses as a mutualistic interaction has been debated due to evidence suggesting that parasite loads of clients are often not affected by cleaner activity (Gorlick et al. 1987, Grutter 1996), that removal of cleaners often does not result in perceptible changes in fish communities (Losey 1972, Grutter 1997, Whiteman et al. 2002) and that cleaners remove not only parasites but mucus and scales from their clients (e.g. Gorlick 1980).

Caribbean diving photographs compliments of Dr Karen Cheney, click to enter site Such observations were also made in terrestrial cleaning systems. Weeks (2000), for example, found that red-billed oxpeckers did not affect tick loads on African cattle and that instead, the oxpeckers significantly prolonged the healing time of wounds. Cleaning may thus, at least in some instances, be closer to parasitism by cleaners than to mutualism (Poulin & Grutter 1996). An alternative hypothesis for cleaning symbioses suggests that inspecting cleaners are behavioural parasites that exploit their clients' propensity to seek rewarding tactile stimulation to gain access to food (Losey 1979, 1987). This hypothesis stems from studies showing that fish clients in captivity posed for painted wooden models resembling cleaners (Fricke 1966) and even for bare wire (Losey 1979), as long as physical contact between the object and the client occurred. Recently though, (Grutter 1999) showed a 4.5-fold reduction in ectoparasite load on the client Hemigymnus melapterus present on reefs with the cleaner wrasse Labroides dimidiatus compared to reefs without cleaners. Her results have reopened the debate about the mutualistic nature of cleaning symbioses, a debate which will only be resolved by considering the costs and benefits of cleaning and how consistent these are over temporal and spatial scales. This was the main goal of my thesis.


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Study Species

Caribbean diving photographs compliments of Dr Karen Cheney, click to enter site Such observations were also made in terrestrial cleaning systems. Longfin damselfish were ideal for this study. They are very abundant on shallow water reefs throughout the Caribbean. Their territorial nature allows multiple observations to be carried out on individuals and easy recognition of individuals through territory position. Their territories are also found at variable distances from cleaning stations which has an impact on their use of cleaning stations. The Caribbean cleaning goby (Elacatinus sp) are found at cleaning stations on coral heads or sponges. Clients will visit these cleaning stations and the goby will jump on these fish and glean material, such as ectoparasites from their surface and buccal cavity.

Costs and benefits of cleaning interactions

Caribbean diving photographs compliments of Dr Karen Cheney, click to enter site Such observations were also made in terrestrial cleaning systems. Longfin damselfish were ideal for this study. They are very abundant on shallow I investigated the benefit of being cleaned in terms of changes ectoparasite loads in relation to time spent by damselfish at cleaning stations of the Caribbean cleaning goby (Elacatinus sp.), and the costs of being cleaned, in terms of distance travelled, time spent away from territories and resources lost while the territory is unguarded (Animal Behaviour, 2001). This paper provides the first estimates of costs of being cleaned for any marine cleaning symbiosis. I also have linked the decrease in ectoparasite load associated with use of cleaners to one measure of fitness, i.e. male reproductive output (Behavioural Ecology, 2003).

Caribbean diving photographs compliments of Dr Karen Cheney, click to enter site Such observations were also made in terrestrial cleaning systems. I examined the relationship between longfin and cleaning gobies over the distributional range of these species to investigate how costs and benefits of the interaction change spatially and temporally with changing environmental factors such as ectoparasite availability (In review).

Ecological causes and consequences of cleanerfish distribution

Cleaning stations are prominent features on any coral reef, and interactions between cleaners and their clients are among the most common interspecific interactions of coral reef fish. Clients spend a large amount of time at cleaning stations every day (Grutter 1995), and cleanerfish can be visited by more than 120 clients every hour (personal observations). However, the few studies that have investigated the causes of cleaning station abundance and distribution (Johnson & Ruben 1988, Arnal et al. 2002) and the consequences of cleaning stations on client distribution, diversity and changes in reef fish behaviour around cleaning stations, have reported conflicting results which seem at odds with the apparent importance of cleanerfish.

Limbaugh (1961), for example, suggested that good fishing sites were situated around cleaning stations. Recent quantitative studies, however, have failed to find any effect of cleaner fish on the abundance or diversity of client reef fish (Youngbluth 1968, Losey 1972, Grutter 1997, Whiteman et al. 2002b). This failure to find effects on client diversity or abundance led to the conclusion that cleaners do not cause, but rather respond to patterns of client fish distribution (Johnson & Ruben 1988, Côté 2000). However, a closer examination of clients based on pattern of reef residency reveals visiting species that can move from reef to reef do abandon reefs from which clients have been removed (Grutter et al. 2003). Even resident species may be affected by changes in cleanerfish abundance but this effect occurs over long time periods (Bshary 2003).

I have attempted to answer questions about the ecological causes and consequences of cleanerfish distribution, such as the causes of cleanerfish abundance and ask whether ectoparasite loads, number of clients or habitat variables control the cleaning goby density on two spatial scales: among reefs within Barbados, West Indies, and among six islands spanning the Greater and Lesser Antilles (Mar-Ecol-Prog-Ser, 2003 ).

I have also quantified intersexual differences in longfin damselfish distribution which, combined with the non-random distribution of cleaning stations on reefs, results in sex-related patterns of cleaning stations use and ectoparasite load on damselfish .


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