Cleaning Symbioses: The Importance of Cooperation

As indicated previously, the main benefit for cleaning gobies to participate in a cleaning relationship is the presence of an abundant food source. Gnathiid isopods are highly common tropical ectoparasites that can be transiently found on the surface of fish⁶. Cleaning gobies have a strong preference for these and other ectoparasites found on tropical fish and therefore their apparent ubiquity presents gobies with a seemingly never-ending food source, which they are able to tap during cleaning.

There is a theoretical disadvantage to cleaning for the goby, however. The relatively small size of the goby compared to the client and the proximity of the goby to the mouth of the client during cleaning could present a risk of predation. It has been shown that cleaning gobies do clean predators but generally at a faster rate than other clients. The rapid service could signal that the goby is a cleaner instead of prey and reduce the amount of time that the predator is in the vicinity of the cleaning station^{12, 13}. As a consequence of this, there has been no reported predation of cleaning gobies by predatory clients at cleaning stations¹². An additional potential disadvantage of cleaning is the possibility of infection¹⁴. The prolonged intimate contact between the cleaner and client required for effective cleaning may lead to the cleaner becoming infected with the very parasites that they are attempting to remove from the client⁶. Although theoretically a possibility, this is rarely a reality¹⁴, so it is generally agreed that the benefit of a constant food source without the risk of hunting is much greater than the potential disadvantages of predation and infection.

The main benefit for clients involved in a cleaning relationship is, predictable, the removal of ectoparasites¹⁵. As ectoparasites such as gnathiid isopods can cause skin irritation and blood disease¹⁰, it is unsurprising that the removal of these parasites by cleaning gobies confers a lower risk of disease on the clients and allows for the clients to grow larger and live longer than they would otherwise⁶.

There are, however, several disadvantages associated with cleaning relationships. If a client must travel a long distance to find a cleaning station, and especially if the cleaning station is outside of their territory, the client may receive injuries, lose energy, and may even be predated upon by other fish. Additionally, if the client is away from their territory for an extended period of time, as would be the case if the cleaning station was a long distance away, they may lose resources or even the entire territory to another fish¹⁴. Finally, it is not uncommon for cleaner fish to feed on scales and mucus of their clients as well as their parasites, which can be highly disadvantageous for the client¹⁵. However, as cleaning gobies tend to prefer ectoparasites to other food¹³ this disadvantage may be limited in this particular relationship. On the whole, the disadvantages for the client fish in a cleaning relationship can be quite high. It is therefore necessary for the client to balance the potential benefits of parasite removal with the disadvantages of being cleaned. This usually means that clients with a high abundance of parasites, typically but not exclusively large, schooling, and abundant fish¹¹, and those that live reasonably close to a cleaning station seek out cleaning more often than others as the benefits of cleaning outweigh the costs¹⁴.

The previous section highlighted that there are both benefits and costs for both the cleaner and the client in a cleaning relationship. In any relationship, especially ones between different species, it could be assumed that natural selection would favour the individual that maximises their own benefits and minimises their own costs, potentially at the expense of their symbiotic partner. Mutualisms (relationships in which both parties benefit) therefore seem destined to descend to commensalisms (relationships in which one party benefits and the other does not) or parasitisms (relationships in which one party benefits and the other loses). How do cleaning relationships maintain their mutualistic status?

As they are less likely to receive negative effects for a cleaning encounter, it is typically the cleaning goby which is most likely to attempt to exploit their clients. They do this by feeding on the scales and mucus of the client, as well as the parasites. Depending on the effect of this on the client, this indicates that the relationship has become commensal or parasitic as the client does not benefit from the removal of their scales or mucus while the cleaner does benefit from an additional food source¹⁴. It should be noted that, as previously discussed, cleaning gobies have a strong preference for parasites over client scales and mucus, so unlike with other cleaning fish such as cleaner wrasses which happily feed on their clients, cleaning gobies do not tend to cheat very often¹⁰. However, this does not mean that they do not cheat at all and the fact that the Caribbean, and especially Barbados, has a low abundance of ectoparasites means that cleaning gobies may feed on the more abundant mucus and scales when necessary⁹. As the cleaner is able to exploit the client, the client must have a way to maximise their own benefits from the encounter or prevent the exploitation, in order to maintain the mutualistic relationship.

The best way that the client can prevent exploitation by the cleaner is through partner sanctions. For obligate cleaners like the cleaning goby, it is essential that fish continue to come to the cleaning station so that they can feed on their parasites. Therefore, if a goby were to cheat and feed on a client’s scales and mucus, that client and others watching may be more resistant to approach this cleaner in the future and so the goby will lose food sources⁵. This is not very common in cleaning gobies due to their lower likelihood of cheating but is a possible sanction¹⁰. A more common partner sanction for cleaning gobies is restriction of cleaning time. If a client feels a cleaner feeding on their scales or mucus, they may jolt, signalling the end of the transaction, and move away from the cleaning station. This means that cleaners that commonly cheat will have shorter cleaning interactions and therefore less food⁴. Partner sanctions are not the only way in which clients can prevent exploitation, however. It is known that cleaners are less likely to cheat on clients with high parasite loads as the costs of partner sanctions outweighs the benefits of feeding on mucus and scales when there are abundant parasites. Therefore, clients may wait until they have a high enough parasite load before initiating a cleaning interaction in order to gain maximum benefit while incurring minimal cost from the interaction¹⁷.

In conclusion, it is not uncommon for cleaner fish to attempt to exploit their clients and move the cleaning relationship from mutualism to parasitism, but clients tend to have methods to prevent this. This shows how an unusual relationship that should not exist according to natural selection has evolved and is maintained.

The most obvious benefit for the cleaner in this relationship is, like for cleaning gobies, an abundant food source. Indeed, this benefit is even more pronounced for C. ingens as they do not need to wait for the client to approach them due to their presence on the crayfish client. The ectosymbiont nature of branchiobdellids means that an additional benefit of the relationship is the production of habitat that is relatively safe from predators. However, as the crayfish host may remove worms through grooming, as will be discussed later, the habitat may not be as safe as it appears.

The main disadvantage of the relationship for the branchiobdellid is that, due to the strong symbiotic nature of the relationship, they can only reproduce when they are on a live crayfish host. This tightly ties the success of the worm to that of the crayfish so that if crayfish populations decline, so will worm populations³.

Like the tropical fish in the previous example, C. charmodactylus may benefit greatly from being cleaned as, when fouling is high, such as in areas with low water flow, growth rates are decreased and mortality is increased due to sensory, respiratory and locomotor activities being compromised². Removal of this debris by C. ingens, especially from around the gills, has been shown to promote greater growth and longer life in crayfish³ indicating a direct benefit of the cleaning relationship. Interestingly, crayfish have natural anti-fouling mechanisms such as moulting so the precise benefit that they may receive from the cleaning relationship with branchiobdellids is context dependent⁴.

Similar to the previous example, low fouling and high C. ingens abundance has the potential to cause problems for the crayfish host as the worms may begin to feed on the crayfish itself due to scarce food availability³ and may even begin to prevent effective movement or vision due to high worm abundance².

As would be expected, the relationship between the cleaner branchiobdellids and their client crayfish is finely balanced and has the potential to move from positive to negative for the client, with the cleaner having the opportunity to exploit its host. This relationship is slightly more complex than the one described for tropical fish, however, as crayfish can actively clean themselves. When the crayfish is small, young, and in areas of low fouling, the grooming and moulting performed by the crayfish is usually efficient enough to remove debris from their surface and gills⁴. This means that there will typically be little to no benefit in allowing branchiobdellids to live upon them, and the relationship will be either commensal, due to no negative consequences for the client if low numbers of branchiobdellids that can be hosted on the small crayfish², or non-existent, due to the crayfish removing the ectosymbionts before they can cause any problems⁴.

As the crayfish grows older and larger, however, they moult less frequently and become less able to remove debris themselves so begin to experience greater benefits from hosting ectosymbionts like branchiobdellids⁴. Under high fouling pressures, this benefit is at its highest and therefore the relationship would typically be considered mutualistic. However, a consequence of growing size, increased debris abundance, and higher tolerance for branchiobdellid, is an increase in the abundance of branchiobdellids on the crayfish host¹⁷. As the number of ectosymbionts increases, so does the likelihood that their food source of debris will become limiting which will subsequently lead to an increase in feeding upon the tissue and blood-like fluid of the crayfish itself. Therefore, just like the previous marine example, this symbiotic relationship may become parasitic under specific conditions³. To prevent this slide to parasitism, the crayfish will remove branchiobdellids through grooming. A counter-characteristic has evolved in the branchiobdellid cleaners who may choose to attach to less accessible sites of the crayfish, typically away from the gills. Although these positions are not optimal for food acquisition, the branchiobdellids will at least avoid complete removal by the crayfish host which is beneficial, especially as branchiobdellids are completely dependent on crayfish for their survival and reproduction⁴. This is an example of not just how mutualism is maintained in a relationship but also how evolution can cause the production of strategies and counter-strategies to increase the benefits of a given relationship for an individual.

As for most cleaners, a major benefit of the cleaning relationship for oxpeckers is the abundant food source provided by their clients. Ticks, especially the blood-engorged ticks found on other animals, are an important food source for oxpeckers¹⁸, especially for nestlings²². Oxpecker breeding has been shown to occur at times when ticks are most abundant indicating that breeding is reliant on the cleaning relationship, especially as breeding occurs on the host²². This reliance may be a disadvantage of the relationship if client or tick abundance declines.

As red-billed oxpeckers spend all day and yellow-billed oxpeckers spend all day and night on their mammalian clients²⁰, an additional benefit of the relationship is the increased safety experienced by the cleaner²³. Incidentally, yellow-billed oxpeckers must nest on their clients as a way to maintain their food supply due to their smaller range of clients which may move away from the cleaner during the night²⁰, which indicates that yellow-billed oxpeckers are even more reliant on their clients than their red-billed cousins. This is disadvantageous if client populations decline.

Finally, red-billed oxpeckers commonly use hair²² and faeces²⁴ from their clients to build and maintain their nests, indicating an additional benefit to participating in a cleaning relationship.

Ticks feed on the blood of their hosts and can cause skin infections, tick toxicosis, lack of appetite and general energy loss^{18, 24}, so the main advantage for ungulate clients involved in a cleaning relationship is the removal of ticks and therefore the prevention of life-limiting complications. The extent to which oxpeckers remove ticks from their clients is under debate^{22, 25}, however it is likely to be of some advantage, especially in regions of high parasite abundance¹⁹. Furthermore, oxpeckers may feed on wounds on their clients which, although open for exploitation and may therefore become disadvantageous, may aid in the cleaning and healing of wounds¹⁹.

An interesting benefit for the client is the presence of an alarm system that enables the client to be made aware of dangers before they can see them. When an oxpecker detects danger, it makes a hissing call and flies off the client, alerting the client, which may have very poor eyesight, of the presence of a threat^{22, 25}. Although not a direct benefit from the cleaning portion of the relationship, this alarm system is nevertheless reliant on the presence of a relationship between oxpeckers and ungulates.

Just as with the aquatic examples, the cleaner appears to be the participant most able to exploit the cleaning relationship due to their ability to feed on either ectoparasites or client tissue thereby rendering the relationship mutualistic or parasitic⁷. Indeed, it appears that oxpeckers feed mostly on blood¹⁹ which may come from ticks or hosts wounds²³. When a client hosts a large amount of ectoparasites such as ticks it is likely that the cleaner will feed mostly on these parasites, effectively cleaning the client and ensuring that the relationship is either mutualistic, if ticks are removed prior to their feeding on the client, or commensal, if blood-filled ticks are removed. When a client hosts few parasites, it is more likely that the cleaner will ‘cheat’ and either feed on existing wounds or open new ones on the client. The latter situation will typically cause the relationship to be parasitic while the former situation may be mutualistic if the wound is cleaned and not made deeper, indicating an additional context that determines the nature of the relationship, i.e. the abundance of wounds on the host²⁶.

Like other client species, ungulates serviced by oxpeckers do appear to have some control over the relationship as shown by the lack of oxpeckers observed on elephants. Elephants generally lack high levels of parasites so they would receive little if any benefit and perhaps incur considerable costs from permitting oxpeckers to feed on them. It is therefore unsurprising that elephants have been observed using their ears, trunks, and tails to prevent oxpeckers landing on them²⁴. This is an example of rejection of the relationship to prevent parasitism, but it may also indicate that other species that have fluctuating parasite loads may have the ability to control how tolerant they are of their cleaner partners.