Cleaning symbiosis is a mutually beneficial
association between individuals of two species,
where one (the cleaner) removes and eats parasites
and other materials from the surface of the
other (the client). Cleaning symbiosis is
well-known among marine fish, where some small
species of cleaner fish, notably wrasses but
also species in other genera, are specialised
to feed almost exclusively by cleaning larger
fish and other marine animals. Other cleaning
symbioses exist between birds and mammals,
and in other groups.
Cleaning behaviour was first described by
the Greek historian Herodotus in about 420
BC, though his example (birds serving crocodiles)
appears to occur only rarely.
The role of cleaning symbioses has been debated
by biologists for over thirty years. Some
believe that cleaning represents selfless
co-operation, essentially pure mutualism,
increasing the fitness of both individuals.
Others such as Robert Trivers hold that it
illustrates mutual selfishness, reciprocal
altruism. Others again believe that cleaning
behaviour is simply one-sided exploitation,
a form of parasitism.
Cheating, where either a cleaner sometimes
harms its client, or a predatory species mimics
a cleaner, also occurs. Predatory cheating
is analogous to Batesian mimicry, as where
a harmless hoverfly mimics a stinging wasp,
though with the tables turned. Some genuine
cleaner fish, such as gobies and wrasse, have
the same colours and patterns, in an example
of convergent evolution. Mutual resemblance
among cleaner fish is analogous to Müllerian
mimicry, as where stinging bees and wasps
mimic each other.
== History ==
In his Histories (book II), the ancient Greek
historian Herodotus wrote:
As [the crocodile] lives chiefly in the river,
it has the inside of its mouth constantly
covered with leeches; hence it happens that,
while all the other birds and beasts avoid
it, with the trochilus it lives at peace,
since it owes much to that bird: for the crocodile,
when he leaves the water and comes out upon
the land, is in the habit of lying with his
mouth wide open, facing the western breeze:
at such times the trochilus goes into his
mouth and devours the leeches. This benefits
the crocodile, who is pleased, and takes care
not to hurt the trochilus.
Herodotus thus claimed (circa 440 BC) that
Nile crocodiles had what would now be called
a cleaning symbiosis with the bird he called
the trochilus, possibly a sandpiper; but while
he was right about the existence of cleaning
symbioses, there is little evidence for it
in crocodiles. In 1906 Henry Scherren quoted
John Mason Cook, son of travel agent Thomas
Cook, as reporting from Egypt that he had
seen some spur-winged plovers approach a crocodile,
which opened its jaws for them:
Mr. J. M. Cook, of the celebrated tourist
agency, when in Egypt in 1876, "watched one
of these birds, and saw it deliberately go
up to a crocodile, apparently asleep, which
opened its jaws. The bird hopped in, and the
crocodile closed its jaws. in what appeared
to be a very short time, probably not more
than a minute or two, the crocodile opened
its jaws, and we saw the bird go down to the
water's edge." There were several of these
birds about, and Mr. Cook shot two of them,
which Dr. Sclater identified as Spur-winged
Plovers; so that the question as to what bird
enters the mouth of the crocodile is now set
at rest.
MacFarland and Reeder, reviewing the evidence,
found that
Extensive observations of Nile crocodiles
in regular or occasional association with
various species of potential cleaners (e.g.
plovers, sandpipers, water dikkop) ... have
resulted in only a few reports of sandpipers
removing leeches from the mouth and gular
scutes and snapping at insects along the reptile's
body.
== A disputed relationship ==
Cleaning symbiosis is a relationship between
a pair of animals of different species, involving
the removal and subsequent ingestion of ectoparasites,
diseased and injured tissue, and unwanted
food items from the surface of the host organism
(the client) by the cleaning organism (the
cleaner). Its status has been debated by biologists,
with viewpoints ranging from pure mutualism
through to a form of exploitative parasitism
by the cleaner.Marine biologist Alexandra
Grutter explains:
Cleaning associations involve cleaner organisms
that remove ectoparasites and other material,
such as mucus, scales and skin, from the body
surfaces of other apparently co-operating
animals. The latter are often referred to
as hosts, customers, or clients. Cleaning
behaviour is one of the most highly developed
inter-specific communication systems known,
with clients striking elaborate postures which
have generally been assumed to make ectoparasites
more accessible to cleaners.
=== Selfless co-operation ===
Grutter and her colleague Robert Poulin, reviewing
over thirty years of debate by biologists
on cleaning symbioses, argue that "Cleaning
symbioses may not be mutualistic associations
but rather one-sided exploitation. However,
one must then ask why no counter-adaptation
has evolved in clients to free them from this
exploitation. If clients are the puppets of
cleaners, then the fitness consequences of
being exploited must be small". They quote
as an example of an early position, C. Limbaugh
writing in 1961: "From the standpoint of the
philosopher of biology, the extent of cleaning
behavior in the ocean emphasizes the role
of co-operation in nature as opposed to the
tooth-and-claw struggle for existence".
=== Mutual selfishness ===
In 1971, mathematical biologist Robert Trivers
wrote more carefully "Cleaner organisms and
their hosts meet the preconditions for the
evolution of reciprocally altruistic behavior.
The host's altruism is to be explained as
benefiting him because of the advantage of
being able quickly and repeatedly to return
to the same cleaner" (i.e. mutual selfishness).
=== One-sided exploitation ===
By 1987 G. S. Losey wrote less optimistically
"Cleaners are nothing but very clever behavioral
parasites ... that have taken advantage of
the rewarding aspects of tactile stimulation,
found in nearly all vertebrates." Poulin and
Grutter remark that "Over the last few decades,
... the opinion of scientists regarding cleaning
symbioses has changed, from selfless cooperation,
to a mutually beneficial interaction, and
finally to a one-sided exploitation."
== 
Biological range ==
Cleaning symbiosis is known from several groups
of animals both in the sea and on land (see
table). Cleaners include fish, shrimps and
birds; clients include a much wider range
of fish, marine reptiles including turtles
and iguanas, octopus, whales, and terrestrial
mammals. Cleaning symbioses with reptile clients
include fish cleaning the teeth of American
crocodiles (Crocodylus acutus), geckos eating
mosquitoes on Aldabra giant tortoises (Geochelone
gigantea) and scarlet crabs (Grapsus grapsus),
and three species of Galapagos finches removing
ticks from marine iguanas (Amblyrhynchus cristatus).
The best known cleaning symbioses are among
marine fishes, where several species of small
fish, notably of wrasse, are specialised in
colour, pattern and behaviour as cleaners,
providing a cleaning and ectoparasite removal
service to larger, often predatory fish. Cleaner
species, as shown in the table, vary widely
in their degree of dependence on their clients.
Some are essentially pure obligate symbionts
like the cleaner wrasse; some are opportunistic
or facultative symbionts, like the orange
chromide or some cleaner shrimps; and some,
like the oxpeckers, combine a little eating
of parasites (beneficial to client) with taking
of blood (harmful to client), their favoured
food.
== Mimicry among cleaner fish ==
=== 
Mutual mimicry among cleaner fish ===
Many cleaner fish in different families, such
as the Caribbean neon goby (Elacatinus evelynae)
and the Indo-Pacific cleaner wrasse (Labroides
dimidiatus) share the distinctive combination
of a long narrow body, a longitudinal stripe,
a blue colour, and small size. "Convergent
signalling among cleaners, using size, stripes
and colour, should facilitate their recognition
by fish clients." This is analogous to Müllerian
mimicry where genuinely aposematic species
(such as wasps) mimic each other's warning
colours.
=== Aggressive mimicry of cleaner fish by
blennies ===
The sabre-toothed blenny (Aspidontus taeniatus)
is a predatory blenny, an aggressive mimic
which accurately resembles the bluestreak
cleaner wrasse, not only in colour and pattern,
but also in the ritualised dance the cleaner
wrasse makes when potential client fish swim
nearby. However, instead of providing the
cleaning service that it signals, it bites
off pieces of healthy skin, scales and mucus
from the host and then swims rapidly away
to safety.
The effect of aggressive mimicry in a cleaning
symbiosis is analogous to Batesian mimicry,
where a harmless "edible mimetic species copies
the warning signal of a noxious, aposematic
model species, thereby gaining protection
from predators". As in Batesian mimicry, the
rate of successful attacks on cleaning clients
by the bluestriped fangblenny (Plagiotremus
rhinorhynchos), which like the sabre-toothed
blenny mimic the bluestreak cleaner wrasse
(Labroides dimidiatus), is frequency-dependent,
meaning that the mimicry is more effective
when the cheating fangblenny is rare compared
to the cleaner wrasse. The difference, however,
is that the aggressive mimic is inserting
itself into a co-operative relationship (between
cleaner and client), whereas "Batesian mimics
insert themselves into an antagonistic predator–prey
interaction (where the models are the unpalatable
prey)." The fangblenny has evolved an opioid-containing
venom which dulls pain and lowers blood pressure,
confusing the bitten host and giving the cheating
mimic time to escape
