EXPERIMENTAL ANALYSIS OF THE ASSOCIATION BETWEEN INVERTEBRATES and UNICELLULAR ALGAE

Summary Intracellular association with unicellular algae is almost entirely confined to invertebrates which digest intracellular. The mode of establishment must have varied according to whether the animal was herbivorous (or omnivorous) or a specialized carnivore. In the former a specialization of the algae to resist digestion would be the essential preliminary; stages in the establishment of such an association are indicated by conditions in the Spongillidae, Fronlonia, Paramecium bursaria and Foraminifera (and possibly also Radiolaria). The more numerous cases of association with carnivores demand prior specialization of the animal to ingest and tolerate the algae; there is evidence that the initial stages were those of parasitism by the algae, indicated by conditions in various Hydrida. In Chlorohydra viridissima and the turbellarian Dalyellia viridis a balanced association has been attained. Further developments are represented by the animal becoming dependent on the plant (Convoluta roscoffensis), the plant on the animal (zooxanthellae of Coelenterata, etc.) and interdependence of the two (Xeniidae and other Alcyon‐acea). Infection by algae already specialized for life within other animals may explain the origin of the association in certain Gastropoda (e.g. Aeolidiella alderi), the Tridacnidae and some compound ascidians. Association may modify both partners in structure, physiology and habits. These may affect the individual or the race. The zooxanthellae are the most modified of the algae; the structure and habits of Convoluta roscoffensis, C. paradoxa and the Tridacnidae are most strikingly affected amongst the animals. The significance of the association varies widely. Only rarely is it balanced, i.e. a true symbiosis. The algae gain protection and also inorganic food salts, notably those containing available nitrogen and phosphorus. The animals acquire an additional source of oxygen, but the value of this is uncertain. In some cases food in the form of organic matter is passed from the algae (e.g. Paramecium bursaria, Convoluta paradoxa and (in early life) C. roscoffensis) or the animal digests dead or living algae (instances of the former are somewhat uncertain but of the latter include the Spongillidae, C. roscoffensis in later life, Xeniidae and Tridacnidae). The great majority of coelenterates never digest associated zooxanthellae. The waste products of animal metabolism are always automatically removed by the algae. It is possible that the consequent gain in metabolic efficiency may be a significant factor in the great powers of growth and repair possessed by reef‐building corals. Cases of experimental symbiosis illustrate the mutual advantage of the interrelationship. But the association ceases to be truly symbiotic when one party exploits the other, e.g. in C. roscoffensis (with eventual death of the animal) and, most efficiently of all because the animal continues to feed holozoically, in the Tridacnidae. Algae are so frequently associated with tropical invertebrates as to constitute ‘imprisoned phytoplankton’ which, by tapping important sources of nitrogen and phosphorus, probably materially reduce the free phytoplankton of surrounding waters. The frequency of association in tropical waters may be attributed to the great competition there for the limited supplies of nutrient salts on the part of the plants, and to the greater survival value owing to increased nutriment (Tridacnidae, Xeniidae, Foraminifera, Radiolaria) or increased metabolic efficiency (Madreporaria and other Coelenterata) conferred on the animal.