#cooperation

In contrast to humans, the damselfishes have simpler agricultures... Hata and Kato have observed that species of the damselfishes maintain “dense stands of filamentous algae as algal farms.” In particular, the “territorial damselfish, Stegastes nigricans, maintains algal farms by excluding invading herbivores and weeding unpalatable algae from its territories”; it also carefully grazes its crops to stimulate the algae to remain in the rapid-growth, early-succession phase... Hata, Watanabe, and Kato, however, have noted that “this fish neither sows nor transplants the algae.” Further, Stegastes nigricans has not been observed to fertilize its crops or to use any type of pest control against crop parasites or diseases, and the damselfish does not use artificial selection or genetic engineering to improve its crops, unlike humans.

Of these [Lophotrochozoan agriculturalists], the limpet snails have the most complex agricultures, consisting of five of the 12 agricultural traits... Species of the scutellastrid limpets cultivate Ralfsia verrucosa algae in two types of gardens: periphery gardens (Scutellastra cochlear, S. flexuosa, S. mexicana, and others) and patch gardens (Scutellastra longicosta, S. laticostra, S. chapmani, and others). Periphery-gardening limpets cultivate algae in a zone around the periphery of a permanent home base... by rasping the coral surface, “and the alga within the garden area is restricted to the interstices of the rasped surface”. The more mobile patch-gardening limpets cultivate algae in larger patches over which the snails graze. Both types of gardening limpets fertilize their gardens, but in a different manner: by the release of nitrogenous excretions (ammonium and urea in their urine and feces) in the periphery gardeners, and by the spreading of nutrient-rich mucus in mucus trails from their feet by the patch gardeners... The patch-gardening snail Scutellastra longicosta has been demonstrated to weed its gardens... . The scutellastrid limpets also defend their crops from raiding herbivores

The nereidid polychaete annelid Platynereis dumerilii uses its own self-grown mucus-tube habitat as the substratum for its algal garden, according to Levinton, who has noted that some species of nereidids “attach pieces of sea lettuce (Ulva) to their tubes and maintain algal gardens”... The worms “live inside semi-permanent mucous tubes, that are generally attached to macroalgal thalli. . . . P. dumerilii generally feeds close to the tube entrance, to which worms attach small pieces of algae”. At the tube entrance, these pieces of algae are also in close proximity to the nitrogenous urine and feces of the polychaete and thus may be fertilized, even if inadvertently. Woodin has argued that the gardening behavior of Platynereis dumerilii is an adaptation to reduce the risk of predation... “searching for food, the worms are more vulnerable to potential predators.”

The nassariid whelk snail Bullia digitalis also has an agricultural technique that uses only three of the 12 agricultural traits, but they are not the same three... Bullia digitalis uses its own, self-grown calcareous-shell habitat as the substratum for its algal garden... the snail “frequently has an algal growth on the upper surface of its shell and especially on the last whorl”... Harris et al. further note that the garden consists of chlorophyte algae that bore into the shell material of the snail, that the snail periodically grazes on filamentous strands of the algae that protrude from its shell, and that the most commonly seen alga appears to be Eugomontia sacculata... the presence of “only a single species of alga”... argues for weeding behavior by the snail... and obviously the snail does not allow other species to graze its shell, thus defending its crop. Because the snail is mobile in high-energy sandy beaches it is unlikely that it fertilizes its crop with nitrogenous excretions... since these excretions would be quickly washed away...

The littorinid periwinkle snail Littoraria irrorata also has a simpler agricultural technique consisting of only four agricultural traits, but of overwhelming interest is that this periwinkle snail farms saprophytic fungi rather than photosynthetic algae. Thus, in its crop choice this agriculturalist marine species is convergent with the land-dwelling insect agriculturalists... Littoraria irrorata prepares the substrate for its garden by actively producing longitudinal wounds with its radula on the leaves of the salt marsh cordgrass Spartina alternifora; these wounds are then colonized by species of the ascomycete fungi Phaerosphaeria and Mycosphaerella... they have also been seen engaging in “selectively depositing hyphae-laden feces within wounded plant tissues to facilitate fungal establishment and growth”... The farmer is obligately dependent upon the presence of the fungal crop, but the fungal crop, although benefiting from the activities of the farmer species, is not obligately dependent upon it.

All three ecdysozoan [and terrestrial] agriculturalist animals farm fungi rather than plants, and all three have a two-way obligate relationship between the farming animals and their crops. The macrotermitine termites have an agricultural technique that uses eight of the 12... the relationship between the macrotermi- tine termites and their crops, species of Termitomyces fungi, is one of obligate mutualism... In addition to substrate preparation, crop planting, crop fertilization with organics, and protection and weeding of crops, Aanen also observed that “the termites ‘artificially’ select for high nodule production” to improve their Termitomyces crops and that “genetic screening of Termitomyces strain diversity happens in at least some of the genera either directly through active selection of symbionts or indirectly through interstrain competition for comb space.”

The leaf-cutter ants have an agricultural technique that uses ten of the 12 agricultural traits— an agriculture that is more complex than human agriculture in this analysis. Like humans, the ants use “chemical herbicides to combat pests,” but, unlike humans (as yet), the ants also use “disease-suppressant microbes for biological pest control”, in particular an “antibiotic produced by the Pseudonocardia bacterial symbiont” that is used against fungal parasites... whereas the fungal cultivars of the non-leaf-cutting “lower” attine ants are facultative symbionts, ants in the leaf-cutter genera Atta and Acromyrmex cultivate “higher attine” fungi (principally Leucoagaricus gongylophorus) that are incapable of living separately from their ant farmers. Like termites, ants practice artificial selection through the selection of variant fungal symbionts. Thus leaf-cutter ants are known to utilize all of the agricultural techniques used by humans in this analysis except two: the usage of artificially produced chemical fertilizers and genetic engineering to improve their crops. However, it is possible that the ants may even use genetic engineering—through the introduction of viruses and horizontal-gene transfer into their crops—but this remains to be proved.

Last, of the 11 independently evolved, fungus-farming lineages of ambrosia beetles, the Ambrosiodmus/Ambrosiophilus-clade ambrosia beetles utilize the most complex agricultural techniques. Their agricultures use seven of the 12 agricultural traits... the Ambrosiodmus/Ambrosiophilus-clade ambrosia beetles are obligate mutualists with their fungal crop species Flavodon ambrosius. [They] possess the general agricultural traits of substrate preparation, crop planting, crop protection, and crop weeding. Like the ants, they use microbes for biological pest control, but they are not known to fertilize their crops... “Several Asian species within the genus Ambriosiophilus engage in another inter-specific interaction—fungus stealing (mycocleptism). Instead of making their galleries in uninhabited wood, these parasitic Ambrosiophilus species search for galleries established by the much larger ambrosia beetles in the genus Beaverium and excavate their galleries immediately next to the existing tunnels. The fungus established by Beaverium spp. therefore immediately grows in the gallery of Ambriosiophilus spp.” (Kasson et al. 2016, 94).