Coral Reefs (2002) 21: 245–251 DOI 10.1007/s00338-002-0241-x
R EP O RT
Elizabeth A. Whiteman Æ Isabelle M. Coˆte´ John D. Reynolds
Do cleaning stations affect the distribution of territorial reef fishes?
Received: 18 February 2001 / Accepted: 22 January 2002 / Published online: 18 June 2002 Springer-Verlag 2002
Abstract We investigated the role of cleaning stations in determining the distribution of territorial reef species. Cleaner fish reduce their clients’ ectoparasite loads and, therefore, proximity to cleaning stations should be advantageous for territorial fish. We focused on five damselfish species which hold permanent territories and cleaning stations occupied by cleaning gobies (Elacatinus spp.) on a Caribbean reef. Contrary to our predictions of higher densities near cleaning stations, we found that bicolor damselfish were less abundant near cleaning stations than at ecologically similar points without cleaning gobies whereas no effects were seen for longfin, dusky, yellowtail, and threespot damselfish. In addition, although damselfish densities were higher in the immediate vicinity of cleaning stations than 1.5–3 m away for most species, this was also the case at points without cleaners. Because cleaning stations are usually located on prominent coral heads or sponges, the overall significant attraction of damselfish to such structures, whether occupied by cleaning gobies or not, could reflect attraction to past or potential cleaning stations. However, it is more likely that interspecific competition and/or the low benefits of being cleaned at our study site prevent aggregation around cleaners. Cleaning stations may play only a minor role in determining the distribution of territorial reef fishes. Keywords Damselfish Æ Habitat selection Æ Cleaning symbioses Æ Territoriality Æ Cleaning gobies
E.A. Whiteman Æ I.M. Coˆte´ (&) Æ J.D. Reynolds Centre for Ecology, Evolution and Conservation, School of Biological Sciences, University of East Anglia, Norwich NR4 7TJ, UK E-mail:
[email protected] Tel.: +44-1603-593172 Fax: +44-1603-592250
Introduction Most coral reef fish exhibit non-random adult distributions which have been related to various factors such as substratum type, habitat complexity and fish densities (reviewed in Williams 1991). Habitat selection by individuals has been shown to influence both growth and survival (Jones 1988; Wellington 1992). There should thus be strong selection on individuals to choose the appropriate habitat at, or soon after, settlement. One habitat feature which could affect reef fish distribution is the presence of cleaning stations. These traditional sites are usually located on prominent coral heads and occupied by cleaner fish which remove ectoparasites and other items from the body surface of larger fishes (known as clients; Feder 1966). Evidence is mounting that cleaner fish significantly reduce the ectoparasite burden of their clients. Grutter (1999) found a 4.5-fold decrease in the number of parasitic gnathiid isopod larvae on clients having access to blue-streaked cleaner wrasse Labroides dimidiatus, compared to clients without such access. Similarly, Caribbean damselfish that often visited cleaning stations operated by the cleaning gobies Elacatinus evelynae and Elacatinus prochilos had fewer gnathiids than less frequent visitors (Cheney and Coˆte´ 2001). However, client access to cleaners appears to be limited by the cost of travelling to cleaning stations. Cheney and Coˆte´ (2001) found that damselfish living more than 2 m away from cleaning stations rarely visited these. Moreover, several experimental removals of cleaners from reefs have failed to result in movements of clients to adjacent reefs with cleaners (Youngbluth 1968; Grutter 1997), suggesting that the costs of travelling outweigh the benefits gained from being cleaned. Proximity to cleaning stations may therefore be an asset to fish settling on a reef. We investigated the significance of cleaning stations in determining the distribution of territorial species on Caribbean coral reefs. We focused on damselfish (Pomacentridae) because they are among the most fre-
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quent visitors to cleaning stations (Arnal and Coˆte´ 1998), and the costs and benefits of cleaning symbioses have been elucidated for at least one species (Cheney and Coˆte´ 2001). Most damselfish are highly aggressive herbivores which occupy virtually permanent territories (Robertson 1984). We can envisage three ways in which damselfish may aggregate their territories around cleaning stations if these represent high-quality resources. First, juvenile damselfish may settle preferentially in good habitat (e.g. Jones 1988; Booth 1992; Wellington 1992). Second, if the best habitat is not available at settlement, damselfish may still move as subadults or adults and take over vacant territories some distance from the initial territory (Doherty 1983; Itzkowitz 1985; Robertson 1988, 1995). Finally, even where habitat is saturated with damselfish territories, there may be scope for territory compression, and hence higher densities, around favourable sites. Although such territorial compression has not yet been documented in damselfish, this phenomenon is common in other fish species (Iguchi and Hino 1996; Praw and Grant 1999; Keeley 2000). We compared the abundance of territorial damselfish at points with and without a cleaning station, and also at increasing distance from cleaning stations. We predicted (1) a higher abundance of territorial damselfish near cleaning stations than at ecologically similar points without a station, (2) decreased abundance with distance from a cleaning station, and (3) a relationship between the extent to which various species of damselfish aggregate around cleaning stations and their frequency of visits to cleaners. Visit rate to cleaning stations correlates well with ectoparasite load on clients (Arnal and Morand 2001). As a control, we also recorded the distribution of a territorial herbivorous species, the redlip blenny Ophioblennius atlanticus, which does not visit cleaning stations (Arnal and Coˆte´ 1998). Finally, we measured a range of abiotic and biotic habitat variables which could potentially confound patterns of damselfish distribution caused by the presence of a cleaning station.
Methods Field site and study species The study was carried out in Barbados (1310¢N, 5930¢W), West Indies, in November 1999. All observations were made in the Barbados Marine Reserve, a 2.2-km stretch of coast containing fringing reefs, on the west coast of the island. Sampling points were located on the Bellairs reef, an area of continuous habitat with depths varying between 0.9 and 6.25 m. Two species of cleaning gobies, E. evelynae (Bo¨hlke & Robins) and E. prochilos (Bo¨hlke & Robins), are present on the reef. Both species are small (1) which were subsequently used as covariates in the ANCOVAs. First, multivariate ANCOVAs were performed to incorporate potential interactions between species. Second, a paired univariate ANCOVA design was generated by ranking the density of each fish species such that paired cleaning and non-cleaning points (see Data collection) or the inner circle and outer ring of a sampling point were assigned the same rank. The ranking was then entered as a factor in the univariate ANCOVAs. For each species, we used a backward stepwise procedure, dropping the least significant variable at each step until only significant (P0.05 in all cases). Data for each substratum were therefore combined in subsequent analyses.
Table 1. Results of analyses of covariance testing for the effects of the presence or absence of a cleaning station (factor: cleaner) and habitat covariates (factors: PCA 1–3) on damselfish and redlip blenny densities. The factor Pair matches ecologically equivalent cleaning and non-cleaning points (see Methods for further details). For each species, a fully significant model achieved by stepwise (backwards) regression is presented. Dashes indicate that no factor explained a significant amount of variance in density Factor
F
Longfin and dusky damselfish PCA 1 7.03 Yellowtail damselfish Pair 3.67 PCA 2 4.85 Bicolor damselfish Cleaner 6.11 Pair 6.40 PCA 1 14.01 PCA 3 13.41 Threespot damselfish – – Redlip blenny PCA 3 5.60
D.f.
B
P
1
3.33
0.016
9 1
0.65
0.033 0.055
1 9 1 1
–4.27 –4.56 –4.38
0.043 0.012 0.007 0.008
–
–
–
1
–0.94
0.029
Fish density at cleaning vs. non-cleaning points Contrary to our hypothesis, there were no significant differences between cleaning points and non-cleaning points in the density of any of the species censused (paired t-tests: longfin/dusky: t=1.86, d.f.=9, P=0.10; yellowtail: t=0.32, d.f.=9, P=0.76; bicolor: t=1.44, d.f.=9, P=0.18; threespot: t=0.34, d.f.=9, P=0.74; redlip blenny: t=0.13, d.f.=9, P=0.90). In fact, the total density of damselfish was significantly greater at noncleaning points (paired t=2.77, d.f.=9, P=0.022). Three PCA factors were generated which together explained 74.3% of the variation in habitat characteristics. Factor 1, which accounted for 43.9% of the variation, represented a decreasing proportion of bare substratum, increasing proportion of algal turf and reef, and decreasing amount of rubble. Factor 2 (18.7%) represented mainly decreasing sand cover, whereas factor 3 (11.7%) represented increasing live cover, including fleshy macrophytes and live coral. When using the PCA factors to control for abiotic and biotic habitat variation, damselfish densities were not significantly affected by the presence of a cleaning station (Pillai’s Trace, P>0.05). Overall, higher damselfish densities were found in areas with high algal turf cover (PCA 1; Pillai’s Trace, F4, 13=3.392, P=0.041). Considering each damselfish category separately, the presence or absence of a cleaning station explained a
Fig. 1. Mean density (number per census area ± 1 SE) of each damselfish species and redlip blennies at cleaning (dark bars) and non-cleaning points (light bars), adjusted for habitat covariates. Means were derived from a full model prior to stepwise (backwards) regression. * Significant difference (P0.5 in all cases). Fish density at increasing distance from cleaning stations Additional control over variation among sampling sites was provided by comparing fish densities in the inner circle with those in the outer ring of each sample point. Principal component analyses generated three factors which incorporated 75.5% of the variation in habitat at cleaning stations and 80.4% at non-cleaning points. The ecological meaning of these factors was largely similar to that of the factors presented above. At cleaning and non-cleaning points, factor 1 (cleaning points: 42.1%, non-cleaning points: 48.1%) represented a decreasing proportion of bare substratum and rubble and an increasing cover of reef and algal turf, whereas factor 2 (cleaning points: 19.2%, non-cleaning points: 19.2%) represented increasing sand cover. At cleaning points, factor 3 (13.9%) represented an increasing proportion of fleshy macrophytes and a decreasing proportion of encrusting coralline algae. At non-cleaning points, factor 3 (13%) represented an increasing proportion of live cover and a decreasing proportion of algal turf. At both cleaning and non-cleaning points, the density of all damselfish was significantly higher in the inner circle than in the outer ring (Pillai’s Trace: cleaning points: F4, 14=5.56, P=0.007; non-cleaning points: F4,12=5.40, P=0.01). At cleaning stations and noncleaning points, this pattern held for longfin and dusky damselfish as well as redlip blennies (Fig. 2a, b). Variation in the density of yellowtail and threespot damselfish was explained neither by habitat factors nor by distance from a cleaning station (Table 2). At cleaning points, fish densities were generally not related to habitat variables, perhaps due to the limited variation in habitat characteristics within a sampling point. However, as observed above, at non-cleaning points overall damselfish densities and longfin/dusky densities increased with increasing algal turf cover and a decreasing proportion of bare substratum and rubble (PCA 1; Pillai’s Trace, F4, 12=6.48, P=0.005, Table 2). Densities of bicolor damselfish increased in areas of bare substratum and sand (Table 2).
Fig. 2a, b. Mean density (number m–2±1 SE) of each damselfish species and redlip blennies in the inner circle (dark bars) and outer ring (light bars) at a cleaning points, and b non-cleaning points. Means were derived from a full model prior to stepwise (backwards) regression. * Significant difference (P
