In the late 19th century, Frank (1885) introduced hypotheses on the mutualistic nature of mycorrhizal networks. Mycorrhizae are fungi that form partnerships with plants, in which the fungi typically supply the plant with nitrogen, phosphate, water, and microbial defenses in exchange for photosynthate. These hypotheses were considered a challenge to conventional biological understanding when introduced and were therefore highly contested (Trappe, 2005). This unconventional lens was also applied to the fundamental association of fungi and algae in lichen biology, with mycologists such as Anton de Bary and Simon Schwendener arguing for a new framework for understanding this dynamic (Plitt, 1919; Kaishian and Djoulakian, 2020). More than a century later, these ideas are only just becoming well-integrated into scientific literature and lexicon, and remain poorly understood and under-recognized outside of mycology (Trappe, 2005).
With parasitism being understood as the other end of the symbiotic spectrum, the term parasite therefore refers to a loose group cheekily defined by Brooks and McLennan (1993) as “organisms studied by parasitologists.” Edward O. Wilson (2014) attempted to quantify the definition of parasite by saying, “parasites eat prey in units less than one.” Alternatively, parasites can be defined as organisms that “find their nourishment and habitat on other living organisms, without destroying it as predators do prey” (Brooks and McLennan, 1993). While that definition may seem appropriate at first blush, there are a number of organisms that do not fit that definition but have been traditionally considered parasites, such as Oxyruida nematodes (pinworms) that feed on intestinal bacteria and protozoa rather than host tissue (Adamson, 1994). Or, alternatively, there are a number of organisms that meet this definition but have not traditionally been considered parasites, such as vampire bats, mosquitoes, and perhaps most strikingly, herbivores. For instance, is a chrysomelid (leaf beetle) living on and eating a plant leaf parasitic? Conventional wisdom would say no.
In order to understand this dilemma, it is useful to consider the origins of the discipline of parasitology, which are situated in the context of disease biology. In addition to the social origins of the word discussed above, parasitology emerged around the same time as bacteriology, linking with research of pathogenicity and widely viewed within a non-Darwinian framework (Brooks and McLennan, 1993). Thus, parasites were historically approached and understood as unwanted, harmful organisms that disrupted the “natural” order of otherwise discrete and independent individuals. For example, nematodes are a ubiquitous group that fills a vast array of niches. The aforementioned pinworms living in the gastrointestinal tract of mammals, feeding not on host tissue but on bacteria and protozoa are, by definition, commensals. However, their nature as worms predisposes humans to view them as “lesser than,” and their presence within the bodies of mammals is understood negatively, and they are thus often considered parasites (Fig. 1).

The red-billed oxpecker: mutualist or parasite?

An interesting example of shifting definitions exists in the tension between the biology and perception of the red-billed oxpecker, Buphagus erythrorhynchus (Fig. 4). These birds live on the bodies of large African mammals, such as giraffes, rhinos, and zebras, feeding on ticks, dry skin, and exudates such as sweat and mucus (Weeks, 2000). Because ticks are understood to be harmful to their hosts, causing disease, infection, and metabolic drag, the relationship between the red-billed oxpeckers and the mammals was long thought to be mutualistic: the mammals benefit from having the ticks removed and in turn, the birds benefit with a meal. Birds—due to their status as popular, beloved organisms—are not typically associated with parasitism. Therefore, the red-billed oxpecker’s positive status as “mutualist” in this system went widely reported but uninterrogated in the literature. However, Weeks (2000) conducted the first quantitative study of the relationship between oxpeckers and ticks on host cattle, and found that adult tick loads on the cattle are not impacted by the presence or absence of the birds. Moreover, the presence of the birds actually prolong the healing time of wounds on cattle. Then again, a recent study by Plotz and Linklater (2020) added one more piece of the puzzle by showing experimentally that rhinos use oxpeckers alarm calls to detect and evade humans undetected. These findings significantly complicate the categorization of the red-billed oxpecker as either or. It becomes evident that these interactions are complex and multi-faceted.