Interactions between Plagiotremus spp., Labroides dimidiatus and their clients: evidence for behavioural niche partitioning

This study employed community analysis and behavioural field observations to explore the inter‐specific interactions between fangblenny species (Plagiotremus spp.), the cleaner wrasse Labroides dimidiatus and their target species and found that the presence of Plagiotremus spp. did not affect the total amount that L. dimidiatus cleaned but it did reduce the amount L. dimidiatus cleaned key prey species of the Plagiotremus spp. The behavioural interactions between adult L. dimidiatus and their clients changed in response to the presence of Plagiotremus spp., but the results suggested the potential cost of Plagiotremus spp. on L. dimidiatus may be offset by behavioural niche partitioning.     

Caribbean Cleaning Gobies Prefer Client Ectoparasites Over Mucus

If cooperation often involves investment, then what specific conditions prevent selection from acting on cheaters that do not invest? The mutualism between the Indo‐Pacific cleaner wrasse Labroides dimidiatus and its reef fish clients has been a model system to study conflicts of interest and their resolution. These cleaners prefer client mucus over ectoparasites – that is, they prefer to cheat – but punishment and partner switching by clients enforce cooperative behaviour by cleaners. By contrast, clients of Caribbean cleaning gobies (Elacatinus spp.) do not to use punishment or partner switching. Here, we test the hypothesis that the behavioural differences between these two cleaner fish systems are caused by differences in cleaner foraging preferences. In foraging choice experiments, we offered broadstripe cleaning gobies Elacatinus prochilos client‐derived parasitic isopods, client mucus and a control food item. The cleaning gobies significantly preferred ectoparasites over mucus or the control item, which contrasts with cleaner wrasses. We propose that the low level of cleaner–client conflict arising from cleaning goby foraging preferences explains the observed lack of strategic partner control behaviour in the clients of cleaning gobies.     

Cleaning by the wrasse Thalassoma noronhanum, with two records of predation by its grouper client Cephalopholis fulva

The Noronha wrasse Thalassoma noronhanum was recorded cleaning 19 client fish species at Fernando de Noronha Archipelago, o. north–eastern Brazil. The preferred clients were non–dangerous, mostly planktivorous species, whereas the potentially dangerous, predatory species were rarely cleaned. T. noronhanum acts as a cleaner in two distinct ecological situations, at and outside the cleaning stations, and attends different client species in each of them. Potentially dangerous clients were mostly attended outside the cleaning stations. Many attacks and two instances of predation on the cleaner wrasse by the grouper client Cephalopholis fulva were recorded. The attacks occurred on individual wrasses foraging near the bottom outside the cleaning stations.     

Multiple cleaner species provide simultaneous services to coral reef fish clients

Cleaning symbioses on tropical coral reefs are typically documented between two species: a single client fish and one or more conspecific cleaners. However, multiple cleaner species living sympatrically in the Caribbean have been anecdotally reported to simultaneously clean the same client. Nothing is known about the patterns and processes driving these interactions, which may differ from those involving a single cleaner species. Here, we used remote underwater videography on three reefs in Honduras to record simultaneous cleaning interactions involving Pederson''s cleaner shrimp (Ancylomenes pedersoni) and cleaner gobies (Elacatinus spp.). A pilot study on adjacent shrimp and goby stations found interactions were always initiated by shrimp. A larger, multi-year dataset shows cleaner gobies joined 28% of all interactions initiated at A. pedersoni cleaning stations with cleaner gobies residing nearby. Client body size significantly predicted simultaneous cleaning interactions, with 45% of interactions simultaneous for clients greater than 20 cm total body length compared with only 8% for clients less than 20 cm. We also found that simultaneous cleaning interactions lasted over twice as long as shrimp-only interactions. We propose these novel multi-species interactions to be an ideal model system to explore broader questions about coexistence, niche overlap and functional redundancy among sympatric cleaner species.     

Temporal Variation in Cleanerfish and Client Behaviour: Does It Reflect Ectoparasite Availability?

We tested the importance of ectoparasites as the proximate cause of cleaning interactions by comparing the activity of Caribbean cleaning gobies (Elacatinus evelynae) and of their clients during three daily periods (early morning, midday, and late afternoon) in which ectoparasite availability varied naturally. Emergence from the benthos of gnathiid isopod larvae, the main target of cleaning goby predation, was higher at night, when cleaners were inactive, than during the day. As a result, overall ectoparasite loads on client fish tended to be higher in the morning. Inspection bouts by cleaning gobies were longest in the morning, but also at midday when ectoparasite availability on clients was lower. Client fish were observed at cleaning stations most often in the afternoon, when they harboured few ectoparasites, but they were more likely to adopt incitation poses, which increase the likelihood of being cleaned, in the morning than later in the day. Most cleaner and client behaviours therefore did not change predictably in response to natural diurnal variation in ectoparasite availability. Our study suggests that the ultimate and proximate causes of cleaning behaviour need not necessarily coincide.     

Cleaning Activity of Juvenile Angelfish, Pomacanthus paru, on the Reefs of the Abrolhos Archipelago, Western South Atlantic

Studies on fish cleaning symbiosis in the tropical western Atlantic concentrate on specialized cleaner gobies and wrasses. On the reefs of the Abrolhos Archipelago, off the eastern Brazilian coast, juvenile french angelfish, Pomacanthus paru, clean a rich and varied community of fish clients. We recorded 31 reef fish species, including large predators such as groupers, jacks, and morays, being serviced by the french angelfish on cleaning stations situated mostly on seagrass flats. The angelfish performs a characteristic fluttering swimming at the station and, during cleaning events, touches the body of the clients with its pelvic fins. Frequency of encounters between the cleaner and its clients do not reflect the local abundance of client species; most of these move from the reefs to the sand flats to be cleaned. We found no correlation between client size and duration of cleaning events. The conspicuous black and yellow pattern, the fluttering swimming, the tenure of cleaning stations, the physical contact with the client, and the varied community of clients, qualify the juveniles of P. paru as specialized cleaners comparable to the gobies of the genus Elacatinus.     

Cleaning behaviour of the cichlid Mesonauta festivus in the Pantanal wetlands: evidence of a potential freshwater cleaning station

Cleaning interactions are known among several groups of fishes, with a higher number of records for marine fish species. These temporary associations occur between one species that acts as the cleaner and the other species as the client. The interaction usually takes place within the boundaries defined by the cleaner. This site, known as the cleaning station, allows the client fish to strike a typical pose allowing the cleaner to approach, such as wide-open fins and inclined, motionless body. Few studies have reported on the cleaning behaviour of freshwater fish species, and none has reported on behaviour that could be interpreted as establishing a cleaning station. Herein we present a new record of the cleaning interaction in the Neotropics, between the cichlid Mesonauta festivus as the cleaner and three species of anostomid (Leporinus macrocephalus, Leporinus friderici and Schizodon borellii) as clients on Pantanal wetlands, as well as the establishment of a defined cleaning station.     

Daily Cleaning Activity and Diversity of Clients of the Barber Goby, Elacatinus figaro, on Rocky Reefs in Southeastern Brazil

Gobies of the genus Elacatinus are regarded as the most specialised cleaner fishes in the western tropical Atlantic, yet there are no studies on these cleaners in the southern portion of West Atlantic. We studied the diversity of clients and the daily cleaning activity of the barber goby, Elacatinus figaro, on rocky reefs in southeastern Brazil (23–24°S). A total of 34 fish client species in 16 families were recorded over 484 cleaning events. The most frequent clients were damselfishes, Pomacentridae (37.9% of cleaning events) and grunts, Haemulidae (16.9%). Planktivores were the most frequently attended trophic category, and two species in that category accounted for about a half (44%) of the total cleaning events. Size of clients ranged 4.5–55cm and most individuals were medium-sized (12–30cm); as the barber goby ranged 2–4.5cm, clients were 1.5 to 15 times larger than the cleaner was. Cleaning activity started at dawn and ended shortly before nightfall, the highest frequency of interactions occurring at early morning (nocturnal clients) and mid-afternoon (diurnal clients). By midday the frequency of cleaning events decreased and their duration increased. A total of 109±3 cleaning events and 30±1min of cleaning activity were estimated per cleaning station per day, both figures low when compared to those recorded for cleaner fishes in tropical areas of the western Atlantic and Indo-Pacific.     

Cleaning behavior ofBodianus rufus,Thalassoma bifasciatum,Gobiosoma evelynae,andPericlimenes pedersoni along a depth gradient at Salt River Submarine Canyon,St. Croix

Synopsis Cleaning activity at specific cleaning stations was monitored over a depth range of 15–45 m at Salt River Submarine Canyon, St. Croix using the HYDROLAB underwater habitat. We observed over 4600 cleaning events involving 32 host species. Cleaners included the fishesGobiosoma evelynae (cleaning goby), juvenileBodianus rufus (Spanish hogfish) and juvenileThalassoma bifasciatum (bluehead wrasse) and the shrimpPericlimenes pedersoni, often active simultaneously at the same stations. Although cleaning was observed to depths of 30 m, the greatest density of cleaning fishes occurred at a sharp break in the bottom contour at 15 m.Clepticus parrae was the dominant fish cleaned by fishes (80% of events), and the graysby,Petrometopon cruentatum, was most frequently cleaned byPericlimenes. Cleaning was initiated byGobiosoma at 0600 to 0630 h and continued throughout the day as intense bouts of cleaning activity were interspersed with periods of relative calm.Bodianus patrolled areas of several meters and would sometimes rise over a meter above the substrate to initiate cleaning. In contrast, gobies were much more restricted in both lateral and vertical movements.Gobiosoma andBodianus cleaned 3104 and 1346 hosts during the study compared to only 207 forThalassoma. This study of a deeper reef area shows significantly more cleaning activity byBodianus and much less byThalassoma than has been reported from other studies in shallower water     

Cleaning interactions at the only atoll in the South Atlantic

In marine ecosystems, cleaning is a mutualistic relationship in which so-called cleaners remove ectoparasites, diseased tissue, or mucus from the body of their clients, and thus help to maintain a healthy reef community. In spite of its importance in many marine habitats, this interaction remains poorly understood, particularly at oceanic islands. Here, we present the first comprehensive study of cleaning interactions in a reef fish assemblage at Rocas, the only atoll in the South Atlantic. We recorded 318 cleaning events, in which six fish species, including two endemic ones, and two shrimp species acted as cleaners. The clients serviced by these cleaners were 21 bony fish species, one shark and one sea turtle. The cleaner wrasse Thalassoma noronhanum and the cleaner goby Elacatinus phthirophagus were the cleaners with the greatest number of events and species richness of clients. Additionally, 82% of clients in the cleaning events were non-piscivores, and the abundance of both cleaners and clients positively influenced the number of cleaning events (R² = 0.4; p < 0.001). Our results indicate that Rocas atoll has a high species richness of cleaner species despite its small size and highlight the importance of studies of cleaning symbiosis, even in isolated places with low species richness, for a better comprehension of this association in reefs.     

Mutualism promotes site selection in a large marine planktivore

1. Mutualism is a form of symbiosis whereby both parties benefit from the relationship. An example is cleaning symbiosis, which has been observed in terrestrial and marine environments. The most recognized form of marine cleaning symbiosis is that of cleaner fishes and their clients.
2. Cleaner species set up cleaning stations on the reef, and other species seek out their services. However, it is not well understood how the presence of cleaning stations influence movements of large highly mobile species. We examined the role of cleaning stations as a driver of movement and habitat use in a mobile client species.
3. Here, we used a combination of passive acoustic telemetry and in‐water surveys to investigate cleaning station attendance by the reef manta ray Mobula alfredi. We employed a novel approach in the form of a fine‐scale acoustic receiver array set up around a known cleaning area and tagged 42 rays. Within the array, we mapped structural features, surveyed the distribution of cleaner wrasse, and observed the habitat use of the rays.
4. We found manta ray space use was significantly associated with blue‐streak cleaner wrasse Labroides dimidiatus distribution and hard coral substrate. Cleaning interactions dominated their habitat use at this site, taking precedence over other life history traits such as feeding and courtship.
5. This study has demonstrated that cleaning symbiosis is a driver for highly mobile, and otherwise pelagic, species to visit inshore reef environments. We suggest that targeted and long‐term use of specific cleaning stations reflects manta rays having a long‐term memory and cognitive map of some shallow reef environments where quality cleaning is provided. We hypothesize that animals prefer cleaning sites in proximity to productive foraging regions.

     

Crime and punishment in a roaming cleanerfish

Cheating is common in cooperative interactions, but its occurrence can be controlled by various means ranging from rewarding cooperators to active punishment of cheaters. Punishment occurs in the mutualism involving the cleanerfish Labroides dimidiatus and its reef fish clients. When L. dimidiatus cheats, by taking scales and mucus rather than ectoparasites, wronged clients either chase or withhold further visits to the dishonest cleaner, which leads to more cooperative future interactions. Punishment of cheating L. dimidiatus may be effective largely because these cleaners are strictly site-attached, increasing the potential for repeated interactions between individual cleaners and clients. Here, we contrast the patterns of cheating and punishment in L. dimidiatus with its close relative, the less site-attached Labroides bicolor. Overall, L. bicolor had larger home ranges, cheated more often and, contrary to our prediction, were punished by cheated clients as frequently as, and not less often than, L. dimidiatus. However, adult L. bicolor, which had the largest home ranges, did not cheat more than younger conspecifics, suggesting that roaming, and hence the frequency of repeated interactions, has little influence on cheating and retaliation in cleaner–client relationships. We suggest that roaming cleaners offer the only option available to many site-attached reef fish seeking a cleaning service. This asymmetry in scope for partner choice encourages dishonesty by the partner with more options (i.e. L. bicolor), but to be cleaned by a cleaner that sometimes cheats may be a better option than not to be cleaned at all.     

Cleaning interactions at the southern limit of tropical reef fishes in the Western Atlantic

Cleaning associations are one of the most dynamic and complex mutualistic interactions of reef environments and are often influenced by local conditions. In the Western Atlantic (WE) most studies concentrate in tropical areas, with little attention to subtropical areas. We examined an assemblage of cleaner fish and their clients on the rocky reefs of the coast of Santa Catarina state, South Brazil, the southern limit of tropical reef fishes in the WE. We recorded 150 cleaning interactions, in which four fish species and one shrimp species acted as facultative cleaners. The grunt Anisotremus virginicus and the angelfish Pomacanthus paru serviced most clients. Fifteen fish species acted as clients, among which the most frequent was the planktivorous grunt Haemulon aurolineatum (31%). Cleaning interactions occurred mostly (87%) with non-carnivorous clients and the number of interactions was not related to the abundance of the species involved. The absence of dedicated cleaner fishes at the study sites and the replacement of their roles by facultative cleaners may be related to local conditions, including cold currents and reduction of rock cover. Under these circumstances, clients take advantage of the services offered by facultative cleaners, a characteristic of temperate areas.     

To clean or not to clean: Cleaning mutualism breakdown in a tidal environment

The dynamics and prevalence of mutualistic interactions, which are responsible for the maintenance and structuring of all ecological communities, are vulnerable to changes in abiotic and biotic environmental conditions. Mutualistic outcomes can quickly shift from cooperation to conflict, but it unclear how resilient and stable mutualistic outcomes are to more variable conditions. Tidally controlled coral atoll lagoons that experience extreme diurnal environmental shifts thus provide a model from which to test plasticity in mutualistic behavior of dedicated (formerly obligate) cleaner fish, which acquire all their food resources through client interactions. Here, we investigated cleaning patterns of a model cleaner fish species, the bluestreak wrasse (Labroides dimidiatus), in an isolated tidal lagoon on the Great Barrier Reef. Under tidally restricted conditions, uniquely both adults and juveniles were part‐time facultative cleaners, pecking on Isopora palifera coral. The mutualism was not completely abandoned, with adults also wandering across the reef in search of clients, rather than waiting at fixed site cleaning stations, a behavior not yet observed at any other reef. Contrary to well‐established patterns for this cleaner, juveniles appeared to exploit the system, by biting (“cheating”) their clients more frequently than adults. We show for the first time, that within this variable tidal environment, where mutualistic cleaning might not represent a stable food source, the prevalence and dynamics of this mutualism may be breaking down (through increased cheating and partial abandonment). Environmental variability could thus reduce the pervasiveness of mutualisms within our ecosystems, ultimately reducing the stability of the system.     

Does Competition for Clients Increase Service Quality in Cleaning Gobies?

In a biological market, members of one trading class try to outbid each other to gain access to the most valuable partners. Competition within class can thus force individuals to trade goods or services more cheaply, ultimately resulting in conflict (e.g. cheating) over the value of commodities. Cleaning symbioses among fish appear to be good examples of biological markets. However, the existence and effect of outbidding competition among either types of traders (cleaners or clients) have never been tested. We examined whether increasing competition among cleaning gobies ( Elacatinus spp.) for access to clients results in outbidding in the form of provision of a better cleaning service. On reefs where fish clients visited cleaning stations less frequently, and thus competition among cleaners was higher, cleaning gobies ingested fewer scales relative to the number of ingested parasites, i.e. they cleaned more honestly. This shift in cleaner behaviour towards greater honesty is consistent with a greater market value of access to clients in the face of competition among cleaners. However, this pattern could have also arisen as a result of differences in ectoparasite availability across reefs and therefore in value of the commodity offered by clients. Experimental manipulations will be required to determine whether cleaning service quality by cleaning gobies was enhanced solely because of competitive outbidding.     

Roving and Service Quality in the Cleaner Wrasse Labroides bicolor

The cleaner wrasse Labroides dimidiatus occupies fixed ‘cleaning stations’ on coral reefs, which ‘client’ reef fish visit repeatedly to have parasites removed. Conflict arises because cleaners prefer to cheat by feeding on client mucus instead of parasites. Clients can prevent L. dimidiatus from always cheating using control mechanisms such as chasing and partner switching, which depend on repeated interactions. These control mechanisms would be undermined in the absence of frequent repeated interactions, if cleaners roved over large areas. Roving behaviour has been anecdotally described for the closely related cleaner wrasse Labroides bicolor. Here we report field data comparing these two species in Moorea, French Polynesia. Our results confirmed that L. bicolor home ranges are much larger than L. dimidiatus home ranges, and showed that cleaning interactions occurred all over the L. bicolor home range: home range of cleaning interactions increased with total home range size. Moreover, we found that cleaner initiation of interactions increased with home range size in L. bicolor, which would give L. bicolor with large home ranges additional leverage to increase cheating. In line with these results, we found that client jolt rate (used as a measure of cheating) was higher among clients of cleaners with large home ranges. Our results emphasise the importance of game structure and control over initiating interactions as parameters in determining the nature of interactions in mutualisms.     

The Meaning of Jolts by Fish Clients of Cleaning Gobies

Cooperative interactions offer the inherent possibility of cheating by each of the interacting partners. A key challenge to behavioural observers is to recognize these conflicts, and find means to measure reliably cheating in natural interactions. Cleanerfish Labroides dimidiatus cheat by taking scales and mucus from their fish clients and such dishonest cleaning has been previously recognized in the form of whole‐body jolts by clients in response to cleaner mouth contact. In this study, we test whether jolts may be a general client response to cheating by cleaners. We experimentally varied the ectoparasite loads of yellowtail damselfish (Microspathodon chrysurus), a common client of the cleaning goby Elacantinus evelynae, and compared the rates of jolts on parasitized and deparasitized clients. As predicted if jolts represent cleaner cheating, deparasitized clients jolted more often than parasitized clients, and overall jolt rates increased over time as client parasite load was presumably reduced by cleaning activity. Yellowtail damselfish in the wild jolted significantly less frequently than those in captivity, which is consistent with a loss of ectoparasites during capture. Our results suggest that jolts by clients of cleaning gobies are not related to the removal of ectoparasites. Client jolts may therefore be a generally accurate measure of cheating by cleanerfish.     

Role of ants in structuring the aphid community on apple

1. The aphids Dysaphis plantaginea Passerini, Aphis spp. (Aphis pomi De Geer and Aphis spiraecola Patch), and Eriosoma lanigerum Hausmann are commonly found together in apple orchards. Ants establish a mutualistic relationship with the myrmecophilous aphids D. plantaginea and Aphis spp. but not with E. lanigerum. 2. Field surveys and one experiment manipulating the presence of ants and the aphid species were conducted to test the hypothesis that ants play a role in structuring the community of these aphids on apple. 3. Ants tended D. plantaginea and Aphis spp. but not E. lanigerum colonies. In the field, D. plantaginea performed better in the presence of ants while no effect was observed in Aphis spp. Contrarily, populations of Aphis spp. in the manipulative experiment performed better in the presence of ants while no differences were observed for D. plantaginea. Such differences between field and manipulative conditions could be related to thermal tolerance, phenology, and life cycles. In contrast, populations of E. lanigerum were reduced in the presence of ants. 4. Ants also had a significant negative effect on the abundance of natural enemies, which could partially explain the benefits to the tended aphids. However, while ants did not provide a benefit to Aphis spp. when it was reared alone, in the presence of other species ant attendance increased Aphis abundance by 256% and simultaneously reduced E. lanigerum abundance by 63%. Therefore, ants benefited Aphis by reducing competition with other aphid species, which involves a different mechanism, explaining the benefit of ant attendance. Considering all the aphid species together, ants had a net positive effect on aphid abundance, which was consequently considered harmful for the plant. 5. Our results highlighted the role that ants play in structuring apple aphid communities and give support to the observed pattern that ants can benefit tended aphids while simultaneously reducing the abundance of untended herbivores.     

Application of Bacillus species in the control of root rot diseases of crop plants

Bio control potential of three Bacillus spp viz., Bacillus subtilis, B. thuringiensis and B. cereus, against soil borne root-infecting fungi on cowpea and mash bean plants were tested both in vitro and in vivo. All three species showed efficiency and produced nodules on mash bean and cow pea plants. In vitro dual culture plate method showed significant inhibition of Fusarium spp. by all these three species of Bacillus with the appearance of a prominent zone of inhibition while a maximum zone of inhibition of Fusarium spp. was observed by B. thuringiensis, whereas in case of Macrophomina phaseolina and Rhizoctonia solani, the highest zone of inhibition was observed by B. subtilis. Bacillus spp. used as seed dressing and soil drenching showed a significant increase in shoot length, shoot weight, root length and root weight in cow pea and mash bean plants. Maximum shoot length was observed in cow pea plants where Bacillus spp. were drenched in soil, whereas maximum root length and root weight in cow pea was observed when B. thuringiensis used as seed dressing. Seed dressing and soil drenching with species of Bacillus viz., B. subtilis, B. thuringiensis and B. cereus, were found to be an effective method for the control of soil borne root-infecting fungi like M. phaseolina, R. solani and Fusarium spp., on cow pea and mash bean plants.     

Morphometric discrimination of two allozymically diagnosed sibling species of the <Emphasis Type="Italic">Echinorhynchus gadi</Emphasis> Zoega in Müller complex (Acanthocephala) in the North Sea

Allozyme electrophoresis was used to detect biological species of the E. gadi complex from gadids from the northern North Sea. A fixed difference at one of nine enzyme loci surveyed confirmed the existence of two reproductively isolated, sympatric species. Mixed infections of two E. gadi spp. (termed A and B) were observed in Gadus morhua and Pollachius virens. E. gadi sp. B was also found in Melanogrammus aeglefinus and Merlangius merlangus. The presence of gravid females of E. gadi spp. A and B in the same host species, P. virens, and sometimes in the same host individual, indicates that neither differential host-specificity nor seasonal differences in mating time are responsible for their reproductive isolation. Morphological study of probosces from electrophoretically identified specimens demonstrated that the two species can be discriminated in graphical and cluster analyses of hook morphometrics. E. gadi sp. I (of Väinölä etal., 1994) and E. gadi sp. A are probably conspecific.