The predator-prey relationship; a constant battle for the upper hand has produced some amazing natural methods of outsmarting, out-competing and ultimately surviving against the odds. Coral reefs may appear to humans as peaceful, tranquil and beautiful places but for the animals that live there, it is a cut-throat world of intense predator-prey interactions. Evolution has driven some incredible methods for survival of both predators and prey with a constant battle between both parties to gain the upper hand. Venoms used by predators to disable prey, toxins used by prey to ward off predators, size used by both predators and prey to gain the advantage in physical battle as well as evolving a physical appearance that makes both predators and prey more inconspicuous and undetected by other animals.

Antennarius sp.

Crypsis is the ability of an organism to avoid being seen by other organisms. This can be achieved either physically, by mimicry, camouflage or transparency, or behaviorally, by nocturnality or reclusive lifestyle (e.g. living in a cave or burrow). This article will focus on the physical forms, mimicry and camouflage, which are both similar mechanisms by which an organism copies other forms found in its natural environment. By definition, mimicry is the external resemblance to another organism, known as a model, while camouflage is concealment by resemblance to a non-living part of the environment. However, camouflage is often used as a blanket term which suggests an organism having a form in which it can blend in to its surroundings. Both forms can be used either defensively or as tools of ambush and are very common in the coral reef environment. There may be a blurred line between mimicry and camouflage where an animal mimics a plant, alga or sedentary animal such as sponge or coral. Technically, the animal resembles another organism or part thereof, therefore is a mimic, however, the model organism is a fixed part of the environment and it is usually considered that in these cases the resemblance is camouflage.

Mimicry is a common evolutionary solution to a range of problems facing marine organisms. It can be used to allow organisms to blend in to their surroundings, falsely advertise defense mechanisms or as a way too approach prey inconspicuously. One of the most common uses of mimicry is used by fishes which mimic species that have superior predator evasion skills or chemical defenses. These mimics rely on the knowledge of their predators that individuals which look like them are not easy meals. In many species mimicry is only displayed by juveniles and morphology and/or color will change at maturity as they become large enough to develop alternative defensive or evasive strategies.

Mimicry can be broken down into more distinct groups such as aggressive, defensive and automimicry. Defensive mimicry can be further split into sub-groups; Batesian mimicry, Müllerian mimicry, Mertensian mimicry and others. Mimicry has largely been described and classified based on insects and a lot of mimicry found in marine species does not fit the traditional mold.

Aggressive mimicry is where a predatory or parasitic species will mimic a less harmful model in order to get close to prey. The model in these cases is often the target species, allowing the mimic to move inconspicuously into a shoal where it can prey on smaller individuals or may be a beneficial symbiont to the prey such as a cleaner wrasse where the model can make sneak attacks before moving on to new prey.

Aggressive mimicry is a ploy used by several species of predators, especially in juvenile stages to allow them to blend in to shoals of planktivorous fish inconspicuously. Large juvenile and female slingjaw wrasses (Epibulus insidiator) are often a golden color and are found near congregations of the yellow damselfish, Pomacentrus molluccensis. Juveniles of the grouper Lutjanus bohar mimic a variety of Chromis species including C. margaritifer, C. iomelas and C. ternatensis. In both cases the coloration helps both with protection of juvenile individuals through safety in numbers but also allows them to get close enough to smaller individuals within the shoal in order to feed on them. In the case of E. insidiator, very small juveniles mimic Wetmorella spp. wrasses before changing color to mimic the damselfish (Kuiter, 1996). The reason for this is not known but it may be related to the fact the Wetmorella wrasses are much older at the same size and predators avoid chasing these small fish who are experienced at maneuvering through the reef. The aggressive mimicry exhibited by these predatory species is not limited to these two species and a similar ploy is used by other predators, especially juveniles of fishes from the serranid family who mimic small fish such as damselfishes and wrasses.

A similar method of mimicry is used by the coney, Cephalopholis fulva, where the model is a damselfish species, Chromis multilineata, but the prey species is a blenny, Malacoctenus sp., with no usual association with the damselfish. The idea here is that the Chromis is a harmless, non-threatening species with respect to the blenny and therefore their presence allows the blenny to feel confident in carrying out normal behaviors instead of hiding amongst rocks. As the school of damselfish passes an unsuspecting blenny, the ambush occurs with a relatively high success rate (Sazima et al, 2005).

The blenny genus Plagiotremus contains mimic species that use a number of methods of mimicry, both aggressive and defensive; the defensive mechanisms will be discussed later. Juveniles of the species P. rhinorhyncos mimic the cleaner wrasse Labroides dimidiatus and feed on flesh from unsuspecting fish that congregate around cleaning stations inhabited by the wrasse. The false cleaner wrasse, Aspidontus taeniatus, is another species of blenny which mimics the cleaner wrasse even more closely than P. rhinorhyncos and feeds in much the same manner. Aspidontus spp. possess fangs similar to those found in the fang blennies of the genus Meiacanthus although they are not venomous. It has been noted that in some areas P. rhinorhyncos will school with other fish species of fish from several families and intermittently making attacks on members of the aggregation (Russel et al, 1976).

Batesian mimicry is a form of defensive mimicry where the mimic resembles a model that is undesirable to predators by being unpalatable, venomous or elusive. This is especially common in marine fish given the number of toxic or venomous species that are potential models for mimics (Sewell, 2007). Almost all common examples of mimicry in marine fishes and most examples in marine organisms in general fall into this category. This type of mimicry is named after Henry Walter Bates who discovered it while studying butterflies in the Amazon rainforest in 1848.

One of the most interesting mimics in the marine world is the Indonesian mimic octopus, Thaumoctopus mimicus, which uses both color and behavior to mimic a variety of animals including sea snakes, lionfish and sole. Like all species of octopuses, T. mimicus has the ability to change the color and texture of its skin allowing an exceptional range of variation in its appearance in order to deceive potential predators. This species of octopus has shown the ability to mimic different animals based on which best suits the situation. One example of this is to retreat into a hole in rocks showing two arms and changing its color to black and yellow bands to mimic a species of venomous sea snake when under attack by damselfish. The diet of the sea snake being mimicked consists largely of damselfish so the mimicry displayed is highly appropriate. The mimicry of both lionfish and a species of banded sole is believed to be used to feign the venomous nature of both fish.

Reef Stonefish, Synanceia verrucosa.

The blenny genus Meiacanthus contains species of venomous fish that possess fangs that deliver a painful sting to potential predators and due to recognition by predatory fishes, are not often targeted as prey. Several other species of blennies have developed the same coloration to take advantage of this fact. Some species of mimics vary in color depending on local species of Meiacanthus such as found throughout the western Pacific mimic the coloration of Meiacanthus atrodorsalis whereas the subspecies P. laudandus flavus found in Fiji is yellow, mimicking M. oualanensis. Blennies from other genera, especially species from the genus Plagiotremus, mimic a variety of species of Meiacanthus blennies. However, mimicry of these venomous blennies is not restricted to members of this family and it has been shown that juveniles of the coral bream species Scolopsis bilineatus and S. margaritifera vary between locations to mimic a range of different species of Meiacanthus spp. while there are a few species of apogonids which also mimic these blennies. Like many mimic species, these mimics exhibit not only the coloration of the venomous blennies but also the behavior including swimming patterns and many of the Plagiotremus spp. keep their dorsal and anal fins displayed in order to mimic the body shape more closely.

Like the mimic blennies from the genus Plagiotremus, the mimic tang, Acanthurus pyroferus has a variety of model species which it mimics depending on its region of origin. This surgeonfish mimics species of angelfish from the genus Centropyge including C. vrolikii and C. heradli in the Western Pacific and C. flavissima in the Central and South Pacific. In the Indian Ocean, the western mimic tang, Acanthurus tristis, mimics the eibli angel, Centropyge eibli. In both species of surgeonfish, it is only the juveniles which exhibit the coloration of the angelfishes and it is believed the reason for this mimicry is the ability of dwarf angelfishes to evade predators. Often predators will target less evasive prey species after failed attempts at catching the dwarf angels. The surgeonfishes take advantage of this knowledge in the predators and by deceiving predators into believing they are dwarf angels and therefore difficult to catch, will be avoided as potential prey. The possible reason behind the advanced evasion techniques used by the Centropyge spp. compared to similar sized A. pyroferus or A. tristis is the size of the larvae at settlement. Larvae of the dwarf angels settle at 10-12mm while those of the mimic tangs settle at around 30-40mm. By the time the angelfishes reach the size of the settled tangs, they are familiar with their localized environment and have experience moving quickly through narrow sections of the reef (Kuiter and Debelius, 2001).

It is interesting to note the variety of models that may be used within a single genus of fish. An example of this is the Platax spp. batfishes, which all use camouflage or mimic techniques in the juvenile stages. While fish from this genus are generally considered to be unsuitable additions to the average home aquarium largely due to their size, they are often available to aquarists, collected and sold for their fascinating juvenile coloration. As juveniles, all fish from this genus stay close to the substrate and have evolved camouflage to suit this behavior. Most commonly available to aquarists is the pinnate batfish, Platax pinnatus, whose juvenile coloration mimics that of a toxic flatworm. Three other species within the genus, P. tiera, P. orbicularis and P. boersi, have a juvenile form that camouflages the fish as a piece of dead algae or a leaf, drifting across the bottom. In these species, the swimming behavior complements the coloration with the fish swimming slowly dragging the anal fin along the substrate as if it were being moved by the currents. The final species within the genus, P. batavianus, has a juvenile pattern of black and white uneven stripes not unlike a zebra which it uses to camouflage itself amongst crinoids. Like many fish mimics, batfish lose their cryptic coloration as they grow and rely more on their size for predator evasion.

Müllerian mimicry is an interesting method of mimicry where two species of toxic or unpalatable organisms develop similar coloration. The question was originally asked, “Why would a toxic species mimic another whose defenses are so similar?” The explanation is rather simple, if a predator attempts to feed on either species, the learned avoidance would benefit individuals of both species. While this is not a common form of mimicry in marine organisms a few examples may be found. In this type of mimicry, the model and mimic may be difficult to determine and the species may be regarded as “co-mimics”. Like Batesian mimicry, Müllerian mimicry was named after a biologist studying butterflies in the rainforests of Brazil. In this case it was German Johann Friedrich Theodor Müller who discovered this type of mimicry in 1878.

Many nudibranchs feed on toxic sponges, corals and anemones and store the chemicals which make them generally unpalatable in the repugnatorial glands found around the edges of the mantle. Mimicry is a common defense mechanism associated with nudibranchs, a ploy used by both nudibranchs and a number of nudibranch mimics. In many cases nudibranchs mimic coral or sponges while in others nudibranchs are mimicked by other organisms, most often flatworms from the order Polycladida (Phylum: Platyhelminthes, Class: Turbellaria). The vast number of cases are a mix of both Batesian and Müllerian mimicry since only some of the mimics possess unpalatable or toxic defenses. There are various examples of flatworm species from the genera Pseudoceros and Pseudobiceros that mimic nudibranchs from the genera Chromodoris, Glossodoris, Hypselodoris, Phyllidia and many others.

Mertensian or Emsleyan mimicry is an interesting phenomenon where a highly toxic species will mimic a moderately toxic or unpalatable species for the benefit of prey recognition. This form of mimicry was first described by Patel Emsley while describing reptilian mimicry. This was later elaborated on in a more comprehensive context by Wolfgang Wickler who named it after prominent biologist Robert Mertens. A predator species which feeds on a lethal species will not learn to avoid these as prey apart from the unlikely occurrence of seeing a conspecific die as a result of a failed attack. A predator that attacks a mildly toxic or unpalatable prey species will be unlikely to attempt to attack the same species again. This means a deadly species can gain the advantage of prey avoidance by mimicking a less toxic species. While there are many examples of Mertensian mimicry in the animal kingdom, including insects and venomous snakes, there is little evidence of this amongst marine organisms.

The comet grouper or marine betta, Calloplesiops altivelis, is an interesting mimic because its body does not at all resemble its model. This fish mimics the guineafowl or whitemouth moray eel, Gymnothorax meleagris, with its coloration and partially hides around rocks using its tail to mimic the head of the eel. The comet grouper has a false eye spot on the dorsal fin, above the caudal peduncle and when the fish hides its head amongst rocks, the posterior end of the body resembles the head of an eel emerging from the rocks. This allows this slow moving fish to safely move around openings in rocky reefs with a reduced risk of being attacked.

Like mimicry, camouflage is a ploy used both aggressively and defensively to allow species to blend into its environment. Camouflage is generally a physical attribute, though this is sometimes combined with behavioral characteristics such as digging beneath sand. Generally, in aggressive camouflage, predators will hide within the environment and ambush unsuspecting prey while in defensive camouflage, an individual will use their camouflage to evade predators, often feeding nocturnally to avoid movement during daylight hours.

An example of animals that uses both aggressive and defensive camouflage is octopuses. While this does not apply to all species, it is true for the majority. The soft muscular body of an octopus makes them ideal prey for a number of large animals. For this reason, most octopus species will use both camouflage and cryptic behavior to hide from potential predators. As mentioned earlier, octopuses possess the ability to change both the color and texture of their skin allowing them to easily blend into almost any part of their environment. Generally nocturnal hunters, octopuses will remain camouflaged during the day and may remain in the same place for hours at a time.

The closely related scorpionfish family, Scorpaenidae, and stonefish family, Synanceiidae, are notorious for their camouflage. These fish are a group of slow moving ambush predators which are also known for their venomous dorsal spines. Many species in these families lack swim bladders and their body structure means they are not especially well equipped for substantial movement. While the venomous spines of these fish generally protect them from predation, their camouflage assists them in hunting by keeping them hidden and allowing them to get close to their prey. Some of the most well known members of these families include the reef stonefish, Synanceia verrucosa, the Rhinopias scorpionfishes and the lionfishes from the Scorpaenid subfamily Pterionae. Many species within these families have bland coloration allowing them to blend in amongst sandy or rocky substrates, some have brilliant coloration allowing them to hide amongst corals and other benthic invertabrates while others, such as the lionfishes, have seemingly standout coloration which allows them to hide amongst larger invertebrates such as crinoids. This type of camouflage is common for many species of benthic ambush predators including frogfishes (also known as toadfishes) from the family Batrichoididae, flatheads from the family Platcephalidae and even larger predators such as angel sharks from the family Squatinidae. All these fish are built for predation, with a proportionally large head and small fins. This means these fish are not especially well equipped for swimming but are able to feed on relatively large prey.

Camouflage using coloration of rocky substrate is a common ploy used by various species of fish from many families. From small herbivorous fish such as blennies (Blennidae) and hawkfishes (Cirrhitidae) to moderately sized predators such as groupers (Serranidae) and even many species of benthic sharks. While camouflage is generally thought of as a defensive mechanism, the use of camouflage by marine organisms is well split between aggressive and defensive modes.

Camouflage is used by a plethora of marine invertebrates, in almost all cases in a defensive mode. From crustaceans to cephalopods and molluscs, camouflage is an important method of survival for small invertebrates. Many invertebrates have little in the way of physical protection such as shells or exoskeletons. Soft bodied animals such as nudibranchs, cephalopods and holothuroids are easy targets for for predators and must use alternate defense mechanisms. Many species use toxins or unpalatable chemicals to deter predators but the majority of vulnerable species use camouflage as their main form of defense.

As mentioned earlier, camouflage is not limited to visual defenses. One of the best examples of this is the physicochemical camouflage used by parrotfishes, Scaridae, which secrete a bag of mucous from a specialised gland on the side of the head that surrounds their body while they sleep. This prevents the scent of the fish from being picked up by potential predators. The moucous also contains a distasteful chemical that deters predators that do encounter them.

A very interesting phenomenon is the use of both mimicry and camouflage in some species such as the anglerfishes of the family Antennariidae. These fish are not especially mobile and lack the venomous spines possessed by similar ambush predators such as scorpionfishes and stonefishes. These fish use camouflage to evade predators amongst rocks, corals and sponges. This camouflage is also used to render them invisible to potential prey as well. On top of this, these fish have a modified first dorsal spine which mimics various species of small invertebrates such as worms or crustaceans. The spine is waved back and forth to mimic a wriggling animal that will attract small fish looking for food. As they approach, the anglerfish strikes with incredible speed, engulfing the small fish and swallowing it whole.

As mentioned, there is a grey area that falls between mimicry and camouflage, where animals will mimic living parts of their environment such as corals, sponges or algae. Often this also makes use of both aggressive and defensive mimicry, where a species lacks the ability to flee from predators but also uses its cryptic appearance to hunt. This is common on the reef and there are a number of families of fish that have become specialised in this area.

The Sygnathiformes, which include the families Sygnathidae (seahorses, pipefishes, pipe horses and sea dragons), Solenstomidae (ghostpipefishes) and Pegasidae (seamoths and dragonfishes) are all exceptionaly slow moving fish. They rely on their bony structure and their exceptional camouflage to evade predators. Many of these fish are temperate or subtropical species and hide amongst seaweed or seagrass beds, hiding from predators and preying on small crustaceans that are also seeking refuge amongst the weeds unaware of the danger that they are so often hiding amongst. Of the more well known of these animals are the Australian sea dragons, Phyllopteryx taeniolatus (weedy seadragon) and Phycodurus eques (leafy seadragon), rare in the aquarium trade but known globally for their impressive appearance. Other notable members of the group include the ornate ghostpipefish, Solenostomus paradoxus, which has a range of color forms including black, white, red and yellow and an impressive fin and spine structure that allows it to be completely hidden amongst crinoids and a similar species, the robust ghostpipefish, Solenostomus cyanopterus, which has green, yellow and brown color morphs to camouflage themselves amongst various seagrasses. Also, the pygmy seahorse, Hippocampus bargibanti, mimics 2 species of gorgonian, Muricella plectana and Muricella paraplectana with incomparable accuracy allowing groups of individuals to live within the same coral with little chance of being identified by predators. As a group, there are probably none better than the Sygnathiformes as masters of disguise in the marine world, hiding amongst a huge array of seagrasses, corals, algae, sponges and other living and non-living parts of their environment.

A number of other other marine fishes closely resemble seagrasses and algae including various species commonly encountered by aquarists and divers. These include such species as the dragon wrasse, Novaculichthys taeniourus, whose juvenile stage resembles a piece of drifting algae. Their behaviour aids in the illusion by swimming close to the substrate and swims like a piece of drifting algae. The closely related seagrass wrasse, Novaculichthys macrolepidotus, changes color during its life as it matures from juvenile form to adult form like many wrasses though both chromatic variations allow the fish to remain inconspicuous amongst algae and seagrasses.

Crypsis is a result of the evolutionary struggle between predator and prey, with species needing to find more and more advanced methods of outsmarting their rivals. As predators become more adept at catching prey, the prey must find novel ways of evasion and predators that have not evolved the speed and agility posessed by their prey, they must find more stealthy methods of hunting. This has culminated in an amazing array of methods of camouflage and mimicry that has given aquarists and divers some beautiful and unusual organisms to look at.

References

1. Kuiter, R. H. 1996. Guide to sea fishes of Australia: A comprehensive reference for divers and fishermen. Frenchs Forest, Australia. New Holland Publishers. 434pg.
2. Kuiter, R. H., H. Debelius. 2001. Surgeonfishes, Rabbitfishes and their relatives. Chorleywood, UK. TMC Publishing. 208pg.
3. Russell, B. C., G. R. Allen, H. R. Lubbock. 1976. New cases of mimicry in marine fishes. J. Zool. (Lond.) 180: 407-423
4. Sazima, I., J. P. Krajewski, R. M. Bonaldo, C. Sazima. 2005. Wolf in a sheep’s clothes: juvenile coney (Cephalopholis fulva) as an aggressive mimic of the brown chromis (Chromis multilineata). Neotrop. ichthyol. 3(2): 315-318
5. Sewell, A. 2007. Toxins, venoms and inhibitory chemicals in marine organisms. http://www.advancedaquarist.com/2007/9/aafeature1