14.7: Associations

Until relatively recently, competition was viewed as the dominant force shaping marine ecosystems. According to this view, ecosystems sustain a number of species, each of which competes with all others for food and living space. However, we now know that many species enter into associations with other species as an essential part of their life cycles and that these associations are critically important to the functioning of marine ecosystems and species evolution. 

Associations between species, called symbiosis, can take a bewildering variety of forms but are of three basic types: parasitism, whereby one species benefits from the association and the other is disadvantaged; mutualism, whereby both species (or all species if more than two species are involved) benefit from the association; and commensalism, whereby one species benefits and the other does not benefit but suffers no disadvantage from the association. It is often difficult to determine what, if any, advantage or disadvantage the partners receive in a given association. Many microbial species, including bacteria and archaea, are associates of other larger species but little is yet known about all but a very few of such associations so the examples of associations in this chapter are but a tiny fraction of the very large number that exist in marine ecosystems. Indeed it is likely that all non-microbial species live with a variety of associated microbial species. 

A parasite lives in or on, or frequently visits, another organism (the host) and feeds on the host’s tissues or steals the host’s food, thereby disadvantaging, without destroying, the host. A tremendous variety of parasitic species are present in the oceans, including marine worms, crustaceans, and snails. The majority are small and most live inside their host’s body. Some, however, such as the fish and sea star parasites shown in Figure 14-32, are partly or fully external to their hosts. Fish parasites are abundant. As scuba divers can observe on a coral reef, several species of small fishes and shrimp make their living by eating parasites off larger fishes’ bodies (Fig. 14-17e). The larger fishes seek out the cleaner, which often establishes a cleaning station to which its customers return for periodic service.

Figure 14-32. Parasites of fishes. (a) This whip goby (Bryaninops yongei, Indonesia) has a large parasite, a copepod crustacean, on its body. (b) A large black isopod parasite (a crustacean of the family Cymothoidae commonly known as a “fish doctor”) on a lemon damsel (Pomacentrus moluccensis, Papua New Guinea). There are two parasites. Look carefully and you might be able to see the much smaller male just under the large female. (c) Fish doctor parasites are common on many species of fishes, including this flasher scorpionfish (Scorpaenopsis macrochir, Indonesia). (d) This parasitic snail (Thyca crystallina, Indonesia) is apparently found only on this one sea star species (Linckia laevigata).

Because they live either in or on another organism, many parasitic species do not need sensory, locomotory, or skeletal organs. Consequently, many have become degenerate and lack such organs. Many species are little more than a digestive and reproductive system. The reproductive system is generally large because the parasite must normally produce enormous numbers of larvae so that a few of these larvae can encounter suitable hosts. Host location is a major problem for parasites, many of which are parasitic on only one host species. Accordingly, parasite life cycles are often very complex, with one or more intermediate hosts (Fig. 14-33).

Figure 14-33. The life cycles of parasites are often complex. The adult fish fluke lives in the gut of its fish host (a). It produces very large numbers of eggs that are discharged with the host’s feces and hatch into a juvenile stage called a “miracidium.” Although most of the miracidia do not survive, a very small number enter a bivalve mollusk (b), which acts as an intermediate host for the parasite. While in the bivalve, the miracidium develops into a larval form (c), which in turn develops a large number of another life stage, called a “cercaria” (d). The cercariae are released to the water, and a very small number of these cercariae eventually enter a second intermediate host, a brittle star (e). Inside the brittle star, the cercariae develop into yet another life stage, the metacercaria (f). If this intermediate host is eaten by a fish (g), the metacercaria develops into an adult fish fluke parasite. At each stage in its life cycle, only an extremely small fraction of the individuals survive to reach the next host. This is true because many parasites, such as the fish fluke, can use only a single species or only a very small number of species as host for one or more of their life stages.

Commensal or mutual associations can provide various benefits to the cooperating species. These include ready availability of food, avoidance of predators or parasites, easy transportation, and suitable living surfaces.

The association between anemonefishes and their anemones (Fig. 14-20) has major benefits for the anemonefishes. Hiding in the anemone’s stinging tentacles protects an anemonefish from potential predators. In addition, laying eggs under the anemone where they are protected from predators reduces the numbers of eggs needed. Anemonefishes may use the anemone for food in times of need, eating mucus, food scraps, and even anemone tentacles. They may also benefit by having external parasites stung to death and removed by the anemone.

Because many anemones are found without anemonefishes but anemonefishes are never found without an anemone, the benefits of the association to the anemone are less obvious. The anemone does benefit by being cleared of dead tissue, mucus, food wastes, and parasites by the anemonefish. The anemonefish also protect the anemone from its few predators. Without the anemonefish, the anemone could be consumed by certain butterflyfishes and might have to defend its delicate tentacles from such predators by closing up if the anemonefish were not present. Because the anemone cannot feed when closed, the freedom to remain open when predators are nearby is undoubtedly a benefit of the anemonefish association. In some cases, the anemone may benefit by being fed by the anemonefish, which, on occasion, have been seen to carry food to the anemone.

Many other associations also involve a mobile species that uses a nonmobile or less mobile host for protection and food. Examples are associations in which a variety of crabs (Figs. 14-34a-e), small fishes (Figs. 14-34f,g), shrimp (Figs. 14-34h-q, 14-35e), scale worms (Fig. 14-34r), and mollusks (Fig. 14-34s) live on crinoids (Fig. 14-16a,b), corals (Fig. 14-16g,h,j,k), sea stars (Fig. 14-16l), and sea fans (Fig. 14-11b). In most of these associations, the small lodger is well camouflaged or hidden within the host. The lodger eats mucus, dead tissue, parasites, the host’s body parts or food supply, or any combination thereof. Generally, the host benefits by being cleaned of mucus, dead tissue, and/or parasites.

Figure 14-34. Examples of the many associations between species. (a) The arrowhead crab (Huenia heraldica, Papua New Guinea) shown here not only blends into the algae (Halimeda sp.) that it lives on, but usually carries pieces of the algae around with it, as this one is doing, to further enhance its camouflage. (b) Many small crabs live in or on a larger invertebrate for camouflage, to hide and sometimes to steal the host’s food or feed on the host itself. Many species, such as the Xenia swimming crab (Caphyra sp.) shown here on a soft coral, are poorly studied and difficult to identify (Indonesia). (c) This tiny spider crab (Xenocarcinus tuberculatus, Indonesia) lives on a coral whip, usually just one pair per whip. (d) The porcelain crab (probably Porcellanella triloba, Indonesia) lives on a sea pen, even when the sea pen withdraws into the sand for protection. (e) Another tiny porcelain crab (probably Porcellanella sp., Indonesia) lives on a whip coral. (f) The weed cardinalfish (Foa brachygramma, Papua New Guinea) spends its life hidden in weeds or, as in this case, in a crinoid where it cannot be seen or reached by predators. (g) The crinoid clingfish (Discotrema crinophila, Papua New Guinea) lives and hides in a crinoid and usually has a body color that matches the crinoid. 

Figure 14-34. Examples of the many associations between species. (h) Emperor shrimp (Periclimenes imperator, Papua New Guinea) like the pair shown here live on a variety of hosts, including nudibranchs and sea cucumbers. (i) Sea star shrimp (Periclimenes soror, Indonesia), live on sea stars and match their body color to blend in with the host’s body. (j) This sea star commensal shrimp (Zenopontonia noverca, Indonesia) is partially transparent, and with its spots it blends in so well with its background when it is on some parts of the sea star’s body that we had to wait for the shrimp to move before getting a photograph in which the shrimp is more visible. (k) A pair of Coleman’s shrimp (Periclimenes colemani, Papua New Guinea) living protected on their venomous fire urchin host (Asthenosoma varium). (l) Many species of shrimp, like this one (Ancylomenes cf. venustus, Indonesia), live in anemones. (m) Many small commensal shrimp species, including this one (Periclimenes cf. tosaensis, Indonesia), have mostly transparent bodies, so they can blend in with several different hosts. This individual is living in a bubble coral, and the eggs that it’s carrying can be seen as a pink egg mass through its transparent body. (n) This species of coral shrimp (Vir philippinensis, Indonesia) lives only in bubble corals. 

Figure 14-34. Examples of the many associations between species. (o) A humpbacked shrimp (Hippolyte commensalis, Indonesia) can hardly be seen when it withdraws into its soft coral host. (p) This tiny urchin shrimp (Gnathophylloides mineri, Indonesia) is also virtually impossible to see when it hunkers down among the spines of its urchin host where it normally hides. (q) This saw blade shrimp (Tozeuma armatum, Indonesia) has an unusually elongated body so that it can lie flat against the strands of black coral on which it lives. (r) Scale worms, including this species (Gastrolepidia clavigera, Vanuatu), have flattened bodies and coloration to match their host, usually a sea cucumber, as seen here. (s) This egg cowrie (Pseudosimnia sp., Red Sea) lives on and probably eats soft corals such as the one shown here (Dendronephthya sp.).

Even if it is eaten by its partner species, the host may gain. Many species that feed on their host are present as only a single pair on their much larger host. This pair nourishes itself from the host’s tissues but eats the host only at a rate that can be replaced by normal growth. The resident pair aggressively protect their host against colonization by others of their species, parasites, and other species that would also consume the host. Thus, although it loses some tissue to the associate species, the host is better protected.

Many associations involve a normally nonmobile species that lives on a mobile host. Examples are the associations formed by the decorator crab (Fig. 14-16f) and the anemone crab (Fig. 14-35a). The decorator crab gains camouflage and protection from its covering of algae, hydroids, and sponges, which are unpalatable and rarely attacked by predators. The immobile associates may gain by being transported through the water, which increases their chances of obtaining food or dissolved nutrients, and by using the host as a substrate on which to grow. In similar associations, the sponge may be an indifferent partner removed from its home on the reef and carried on the crab’s back by a pair of specially adapted legs. The anemone hermit crab is well protected by the adopted mollusk shell in which it lives, but it is further protected by the stinging anemones that it attaches to the shell (Fig. 14-35a). The anemone gains by being transported through areas where food can be obtained, including scraps of food released as the hermit crab feeds by tearing apart its prey. This association, like many others, is highly specific. The association usually involves the same species of anemone and hermit crab, and the shell of the same species of mollusk. Some species of decorator crabs also cover themselves with sponges (Fig. 14-16f) or carry an urchin on their backs (Fig. 14-35b) to afford them protection.

Figure 14-35. Additional examples of associations. (a) This anemone hermit crab (Dardanus sp., Papua New Guinea) has found a strong gastropod mollusk shell to live in and has attached several anemones on the shell to further discourage potential predators. (b) This crab (Dorippe frascone, Indonesia) has a pair of legs that are modified to carry an urchin, in this case Astropyga radiata, on its back. The urchin’s toxic spines protect the crab from predators. (c) This tiger pistol shrimp (Alpheus bellulus, Indonesia) lives in a single burrow with the yellow shrimp goby (Cryptocentrus cinctus). The shrimp digs and maintains the burrow. The goby warns the shrimp, which is blind, when a predator approaches, and they both disappear into the burrow. (d) A giant clam (Tridacna gigas, Papua New Guinea). (e) This small pistol shrimp (Synalpheus sp., Papua New Guinea) lives in its host crinoid.

The remora (Fig. 14-26g) is an example of a species that is mobile but hitches a ride on a larger swimming animal. In some cases, remoras gain by stealing food from their host. However, the major advantage to the remoras is probably transportation, since they often ride on manta rays, which feed on plankton. It is not clear whether sharks or manta rays gain anything from a remora’s presence, but these hosts apparently are not harmed by carrying the passenger.

The association between gobies and shrimp is clearly beneficial to both partners. A goby and a shrimp live together in a common sand burrow, where they can retreat to safety from predators. The shrimp is blind, and the fish is incapable of digging its own burrow. The shrimp therefore digs and maintains the common burrow, but it is vulnerable to predators when it pushes excavated sand out of the hole. The goby repays the shrimp for its digging by sitting at the burrow entrance watching for predators (Fig. 14-35c). With one of its long, sensitive antennae, the shrimp maintains contact with the goby’s caudal fin. If a predator approaches, the goby wiggles its fin to warn the shrimp, which immediately withdraws into the burrow. If danger increases, the goby itself darts into the burrow.

The few associations described here are all relatively easy to observe and study, but most associations are much more subtle. For example, coordinated feeding by two or more fish species that benefits both species does occur but may be infrequent and difficult to observe. In addition, many associations are difficult to study because one species is well hidden inside the other or because one or both partners are microscopically small. For example, the giant clam, Tridacna (Fig. 14-35d), has a mutually beneficial association with zooxanthellae. The algae live inside the soft mantle tissues of the clam and give this part of the clam its often brilliant coloration. The algae benefit from a secure location within the clam’s tissues, where they also receive a steady supply of carbon dioxide and nitrogenous waste products from the clam, which the algae use for photosynthesis. There, the algal cells can obtain needed sunlight when the clam is open, and they are protected from settling of other benthic organisms that might otherwise overgrow them. In addition, the clam closes when threatened, protecting both itself and its algae. The clam benefits from the association by using the algae’s by-products as a supplemental food supply. Thus, the algae are essentially a carefully cultivated garden that supplements the clam’s food so that it does not have to filter extremely large volumes of water. This feeding arrangement is very energy-efficient and probably accounts for the giant clam’s ability to grow to its huge 1- to 2-m size. Hard corals have a similar association with zooxanthellae (Chap. 15).