Cleaning symbiosis

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Cleaning symbiosis
Flickr - Rainbirder - Yellow-billed Oxpecker (Buphagus africanus).jpg
Cleaning behaviour of yellow-billed oxpecker (Buphagus africanus) on the back of a large mammal

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.

Contents

Cleaning behaviour was first described by the Greek historian Herodotus in about 420 BCE, 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

Herodotus asserted that the trochilus bird, possibly a sandpiper, was able to enter the mouth of the Nile crocodile in what would now be called a cleaning symbiosis. Drawing by Henry Scherren, 1906 PloverCrocodileSymbiosis.jpg
Herodotus asserted that the trochilus bird, possibly a sandpiper, was able to enter the mouth of the Nile crocodile in what would now be called a cleaning symbiosis. Drawing by Henry Scherren, 1906

In his Histories (book II), the ancient Greek historian Herodotus wrote: [1] [2]

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. [1]

Herodotus thus claimed (c.440 BCE) that Nile crocodiles had what would now be called a cleaning symbiosis with the bird he called the trochilus, possibly a sandpiper. 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: [3]

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. [3]

MacFarland and Reeder, reviewing the evidence, found that [4]

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. [4]

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). [5] Its status has been debated by biologists, with viewpoints ranging from pure mutualism to a form of exploitative parasitism by the cleaner. [6]

Marine biologist Alexandra Grutter explains: [7]

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. [7]

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". [6] 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". [6]

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). [6]

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." [6] 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." [6]

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. [7] 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). [4]

Examples of cleaning symbioses in different groups of animals
HabitatCleanerDescriptionClientImage
Freshwater lakes and streams Crayfish worms (Branchiobdellida)Leech-like worms live on crayfish and feed on microorganisms that colonize crayfish gills and exoskeleton Crayfish [8] Crayfish worm.jpg
Indian Ocean coral reefsCleaner wrasse ( Labroides )Small, longitudinally-striped, with blue; eats only ectoparasites at 'cleaning stations'Larger fish e.g. puffers, sweetlips, groupers [9] [10]
Western Atlantic coral reefsCleaning gobies ( Elacatinus )Different species small, longitudinally-striped, with blue, showing convergent evolution; eat ectoparasites but also small preyLarger fish [10] [11] Neon Blue Goby.jpg
Brackish water, South AsiaCichlid fish, orange chromide ( Pseudetroplus maculatus )Eats ectoparasites; preys on eggs, larvaeCichlid fish, green chromide ( Etroplus suratensis ) [12] [13]
Freshwater, Amazon basinJuvenile striped Raphael catfish (Platydoras armatulus)Only juvenile is strongly striped and eats ectoparasitesTrahira (Hoplias cf. malabaricus) [14] -
Caribbean and Indo-Pacific coral reefsSpecies of cleaner shrimp Eat ectoparasites at cleaning stations, scavenge; omnivorousFish of various species [6] [15] Lysmata amboinensis cleans mouth of a Moray eel.jpg
Caribbean and Indo-Pacific coral reefsCrab Planes minutus Eat ectoparasites while living on host Loggerhead sea turtle (Caretta caretta) [6] [16] Columbus crab on Loggerhead sea turtle.jpeg
Pan-tropical coral reefs: Western Atlantic, Pacific Decapod Stenopus hispidus ("banded coral shrimp")Waves antennae to advertise service; eats parasites, fungi, dead tissueFish of various species; [17] [18] hawksbill sea turtle [19] Stenopus hispidus (Banded cleaner shrimp).jpg
African plains, savanna Red-billed oxpecker (Buphagus erythrorhynchus)Eats blue ticks ( Boophilus decoloratus) and brown ear ticks ( Rhipicephalus appendiculatus) (up to 100 adults or 1000 larvae/day), blood: keeps skin wounds openLarge mammals, e.g. impala, rhinoceros, domestic cattle [20] Impala mutualim with birds wide.jpg
Brazilian open countryWattled jacana ( Jacana jacana ), shiny cowbird ( Molothrus bonariensis ), cattle tyrant ( Machetornis rixosa ), giant cowbird ( Molothrus oryzivorus ), yellow-headed caracara ( Milvago chimachima )Feed on ticks, horseflies, other parasites Capybara ( Hydrochoerus hydrochaeris ) [21] Capibara 1.jpg
North American deserts, forests, etc.Species of pseudoscorpions Eat packrat ectoparasitesSpecies of packrat (Neotoma) [22] Kaldari pseudoscorpion 01.jpg
Hawaii submerged lava platformCleaner fish, mostly yellow tang (Zebrasoma flavescens) and golden eye surgeon fish ( Ctenochaetus )Fish at cleaning stations forage on shells and skin of turtles Green sea turtle (Chelonia mydas) [23] Green turtle swimming over coral reefs in Kona.jpg
Kenya and Uganda Banded mongooses (Mungos mungo)Have been observed removing ticks and other parasites Warthog (Phacochoerus africanus) [24] [25] Banded Mongoose.jpg

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. [26] 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. [20]

Mimicry among cleaner fish

Small, long, blue-striped cleaner wrasse (Labroides dimidiatus) servicing a lunar-tailed bigeye (Priacanthus hamrur) Cleaner station komodo.jpg
Small, long, blue-striped cleaner wrasse ( Labroides dimidiatus ) servicing a lunar-tailed bigeye ( Priacanthus hamrur )
Small, long, blue-striped Caribbean cleaning goby (Elacatinus evelynae) strikingly resembles the unrelated cleaner wrasse of the Indo-Pacific in pattern and behaviour Elacatinus evelynae.jpg
Small, long, blue-striped Caribbean cleaning goby ( Elacatinus evelynae ) strikingly resembles the unrelated cleaner wrasse of the Indo-Pacific in pattern and behaviour
The blue-lined sabertooth blenny (Plagiotremus rhinorhynchos) is an aggressive mimic of the blue-striped cleaner wrasse (Labroides dimidiatus), copying its dance but then biting the duped client Plagiotremus rhinorhynchos.jpg
The blue-lined sabertooth blenny ( Plagiotremus rhinorhynchos ) is an aggressive mimic of the blue-striped cleaner wrasse ( Labroides dimidiatus ), copying its dance but then biting the duped client

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." [27] 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. [28] 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. [29]

Comparison of Batesian mimicry with aggressive mimicry of cleaner fish
Type of mimicryModelMimicDupeModel-dupe relationshipDupe's expectationEffect
Batesian mimicry Wasp Hoverfly Predatory birdAntagonistic predator-preyMimic looks noxious Mimic dupes predator into not eating the mimic
Aggressive mimicry Bluestreak cleaner wrasse Sabre-toothed blenny Client fishCo-operative cleaner-clientMimic looks to be a cleaner Mimic dupes client into allowing the mimic to bite

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". [30] 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)." [30] 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. [31]

Related Research Articles

<span class="mw-page-title-main">Symbiosis</span> Close, long-term biological interaction between distinct organisms (usually species)

Symbiosis is any type of a close and long-term biological interaction, between two organisms of different species. The two organisms, termed symbionts, can be either in a mutualistic, a commensalistic, or a parasitic relationship. In 1879, Heinrich Anton de Bary defined symbiosis as "the living together of unlike organisms".

<span class="mw-page-title-main">Reciprocal altruism</span> Form of behaviour between organisms

In evolutionary biology, reciprocal altruism is a behaviour whereby an organism acts in a manner that temporarily reduces its fitness while increasing another organism's fitness, with the expectation that the other organism will act in a similar manner at a later time.

<span class="mw-page-title-main">Mimicry</span> Evolutionary strategy

In evolutionary biology, mimicry is an evolved resemblance between an organism and another object, often an organism of another species. Mimicry may evolve between different species, or between individuals of the same species. In the simplest case, as in Batesian mimicry, a mimic resembles a model, so as to deceive a dupe, all three being of different species. A Batesian mimic, such as a hoverfly, is harmless, while its model, such as a wasp, is harmful, and is avoided by the dupe, such as an insect-eating bird. Birds hunt by sight, so the mimicry in that case is visual, but in other cases mimicry may make use of any of the senses. Most types of mimicry, including Batesian, are deceptive, as the mimics are not harmful, but Müllerian mimicry, where different harmful species resemble each other, is honest, as when species of wasps and of bees all have genuinely aposematic warning coloration. More complex types may be bipolar, involving only two species, such as when the model and the dupe are the same; this occurs for example in aggressive mimicry, where a predator in wolf-in-sheep's-clothing style resembles its prey, allowing it to hunt undetected. Mimicry is not limited to animals; in Pouyannian mimicry, an orchid flower is the mimic, resembling a female bee, its model; the dupe is the male bee of the same species, which tries to copulate with the flower, enabling it to transfer pollen, so the mimicry is again bipolar. In automimicry, another bipolar system, model and mimic are the same, as when blue lycaenid butterflies have 'tails' or eyespots on their wings that mimic their own heads, misdirecting predator dupes to strike harmlessly. Many other types of mimicry exist.

<span class="mw-page-title-main">False cleanerfish</span> Species of fish

The false cleanerfish is a species of combtooth blenny, a mimic that copies both the dance and appearance of Labroides dimidiatus, a similarly colored species of cleaner wrasse. It likely mimics that species to avoid predation, as well as to occasionally bite the fins of its victims rather than consume parasites. Most veiled attacks occur on juvenile fish, as adults that have been attacked in the past may avoid or even attack A. taeniatus.

<span class="mw-page-title-main">Blenniiformes</span> Order of fishes

Blenny is a common name for many types of fish, including several families of percomorph marine, brackish, and some freshwater fish sharing similar morphology and behaviour. Six families are considered "true blennies", grouped under the order Blenniiformes; its members are referred to as blenniiformids. About 151 genera and nearly 900 species have been described within the order. The order was formerly classified as a suborder of the Perciformes but the 5th Edition of Fishes of the World divided the Perciformes into a number of new orders and the Blenniiformes were placed in the percomorph clade Ovalentaria alongside the such taxa as Cichliformes, Mugiliformes and Gobiesociformes.

<span class="mw-page-title-main">Egyptian plover</span> Species of bird

The Egyptian plover, also known as the crocodile bird, is a wader, the only member of the genus Pluvianus. It occurs in a band across Sub-Saharan Africa from Senegal in the west to Ethiopia in the east and south to parts of the Democratic Republic of the Congo. It no longer occurs in Egypt. The species was formerly placed with the pratincoles and coursers in the family, Glareolidae, but is now regarded as the sole member of its own monotypic family Pluvianidae.

<span class="mw-page-title-main">Cleaning station</span> Location where aquatic life congregate to be cleaned

A cleaning station is a location where aquatic life congregate to be cleaned by smaller beings. Such stations exist in both freshwater and marine environments, and are used by animals including fish, sea turtles and hippos.

Cheating is a term used in behavioral ecology and ethology to describe behavior whereby organisms receive a benefit at the cost of other organisms. Cheating is common in many mutualistic and altruistic relationships. A cheater is an individual who does not cooperate but can potentially gain the benefit from others cooperating. Cheaters are also those who selfishly use common resources to maximize their individual fitness at the expense of a group. Natural selection favors cheating, but there are mechanisms to regulate it. The stress gradient hypothesis states that facilitation, cooperation or mutualism should be more common in stressful environments, while cheating, competition or parasitism are common in benign environments.

<span class="mw-page-title-main">Cleaner shrimp</span> Species of crustacean

Cleaner shrimp is a common name for a number of swimming decapod crustaceans that clean other organisms of parasites. Most are found in the families Hippolytidae and Palaemonidae, though the families Alpheidae, Pandalidae, and Stenopodidae each contain at least one species of cleaner shrimp. The term "cleaner shrimp" is sometimes used more specifically for the family Hippolytidae and the genus Lysmata.

<span class="mw-page-title-main">Cleaner fish</span> Fish that remove parasites and dead tissue from other species

Cleaner fish are fish that show a specialist feeding strategy by providing a service to other species, referred to as clients, by removing dead skin, ectoparasites, and infected tissue from the surface or gill chambers. This example of cleaning symbiosis represents mutualism and cooperation behaviour, an ecological interaction that benefits both parties involved. However, the cleaner fish may consume mucus or tissue, thus creating a form of parasitism called cheating. The client animals are typically fish of a different species, but can also be aquatic reptiles, mammals, or octopuses. A wide variety of fish including wrasse, cichlids, catfish, pipefish, lumpsuckers, and gobies display cleaning behaviors across the globe in fresh, brackish, and marine waters but specifically concentrated in the tropics due to high parasite density. Similar behaviour is found in other groups of animals, such as cleaner shrimps.

<span class="mw-page-title-main">Aggressive mimicry</span> Deceptive mimicry of a harmless species by a predator

Aggressive mimicry is a form of mimicry in which predators, parasites, or parasitoids share similar signals, using a harmless model, allowing them to avoid being correctly identified by their prey or host. Zoologists have repeatedly compared this strategy to a wolf in sheep's clothing. In its broadest sense, aggressive mimicry could include various types of exploitation, as when an orchid exploits a male insect by mimicking a sexually receptive female, but will here be restricted to forms of exploitation involving feeding. For example, indigenous Australians who dress up as and imitate kangaroos when hunting would not be considered aggressive mimics, nor would a human angler, though they are undoubtedly practising self-decoration camouflage. Treated separately is molecular mimicry, which shares some similarity; for instance a virus may mimic the molecular properties of its host, allowing it access to its cells. An alternative term, Peckhamian mimicry, has been suggested, but it is seldom used.

<span class="mw-page-title-main">Bluestreak cleaner wrasse</span> Species of fish

The bluestreak cleaner wrasse is one of several species of cleaner wrasses found on coral reefs from Eastern Africa and the Red Sea to French Polynesia. Like other cleaner wrasses, it eats parasites and dead tissue off larger fishes' skin in a mutualistic relationship that provides food and protection for the wrasse, and considerable health benefits for the other fishes. It is also notable for having potentially passed the mirror test, though this is not without controversy.

<i>Elacatinus</i> Genus of fishes

Elacatinus is a genus of small marine gobies, often known collectively as the neon gobies. Although only one species, E. oceanops, is technically the "neon goby", because of their similar appearance, other members of the genus are generally labeled neon gobies, as well. Except for a single East Pacific species, all reside in warmer parts of the West Atlantic, including the Caribbean and Gulf of Mexico. They are known for engaging in symbiosis with other marine creatures by providing them cleaning service that consists of getting rid of ectoparasites on their bodies. In return, Elacatinus species obtain their primary source of food, ectoparasites.

<span class="mw-page-title-main">Bluestriped fangblenny</span> Species of fish

Plagiotremus rhinorhynchos, commonly called the bluestriped fangblenny, is a species of combtooth blenny found in coral reefs in the Pacific and Indian Ocean. This species reaches a length of 12 centimetres (4.7 in) SL. It is also known as the bluestriped blenny, bluestriped sabretooth blenny, blunt-nose blenny, cleaner mimic, tube-worm blenny or the two-stripe blenny. They hide in deserted worm tubes or other small holes.

<i>Plagiotremus laudandus</i> Species of fish

Plagiotremus laudandus, the bicolour fangblenny, false harptail-blenny, poison-fang blenny mimic, yellow-tailed blenny or the yellowtail fangblenny mimic, is a species of combtooth blenny found in coral reefs in the western Pacific ocean. This species reaches a length of 8 centimetres (3.1 in) TL. This species is a Batesian mimic of Meiacanthus atrodorsalis.

<i>Ancylomenes pedersoni</i> Species of crustacean

Ancylomenes pedersoni, sometimes known as Pederson's shrimp and Pederson's cleaner shrimp, is a species of cleaner shrimp. It is part of the genus Ancylomenes and was described in 1958 by Fenner A. Chace Jr. as Periclimenes pedersoni. Ancylomenes pedersoni is found in the Caribbean Sea, often associated with a sea anemone, at depths of 1 to 15 metres. They are often found on the reefs off Bermuda.

<span class="mw-page-title-main">Hawaiian cleaner wrasse</span> Species of fish

The Hawaiian cleaner wrasse or golden cleaner wrasse, is a species of wrasse found in the waters surrounding the Hawaiian Islands. The fish is endemic to Hawaii. These cleaner fish inhabit coral reefs, setting up a territory referred to as a cleaning station. They obtain a diet of small crustacean parasites by removing them from other reef fish in a cleaning symbiosis.

In evolutionary biology, mimicry in vertebrates is mimicry by a vertebrate of some model, deceiving some other animal, the dupe. Mimicry differs from camouflage as it is meant to be seen, while animals use camouflage to remain hidden. Visual, olfactory, auditory, biochemical, and behavioral modalities of mimicry have been documented in vertebrates.

<span class="mw-page-title-main">Rock cook</span> Species of fish

The rock cook, or small-mouthed wrasse, is a species of marine ray-finned fish from the wrasse family Labridae which is found in the eastern Atlantic Ocean off the coasts of Europe.

<span class="mw-page-title-main">Trochilus (crocodile bird)</span> Legendary bird, first described by Herodotus

The trochilus or trochilos, sometimes called the crocodile bird, is a legendary bird, first described by Herodotus, and later by Aristotle, Pliny, and Aelian, which was supposed to have enjoyed a symbiotic relationship with the Nile crocodile: it was said to pick leeches from the crocodile's throat by Herodotus, and to pick the crocodile's teeth by Aristotle. The trochilus has subsequently been spuriously identified with several bird species endemic to the Nile valley.

References

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