Mutualism or parasitism: Partner abundance affects host fitness in a fish reproductive interaction

Abstract

Mutualisms are ubiquitous in nature but are understudied in freshwater ecosystems. Mutualisms can be unstable, shifting to commensal or even negative outcomes with context. Quantifying context dependency in mutualisms is critical for understanding how biotic interactions will shift along disturbance gradients in freshwater systems. A common reproductive interaction among stream fishes, nest association occurs when individuals of one species spawn in nests constructed by a host fish. Hosts benefit from a dilution effect: high proportions of associate eggs decrease the odds of host brood predation. Thus, partner abundance can be an important source of biotic context influencing the outcome of an association. We conducted a large in situ experiment manipulating abundance of partner yellowfin shiner (Leuciscidae: Notropis lutipinnis) (absent, low, high) at constant abundance of host bluehead chub (Leuciscidae: Nocomis leptocephalus), and quantified chub reproductive success using genetic tools. Evidence suggests that the nest association switched from mutualistic to parasitic outcomes as shiner abundance decreased. Chub reproductive success was highest at high shiner abundances. However, chub reproductive success was actually higher in the complete absence of shiners than at low shiner densities. This study shows that outcomes of biotic interactions in freshwater systems are context‐dependent, and that partner abundance can be a key source of context‐dependency in nest associations. We encourage future studies on freshwater mutualisms, which are thus far largely overlooked, relative to competition and predation.

Positive biotic interactions in freshwaters: A review and research directive

“…The fitness outcomes observed along a continuum of partner abundance are likely to differ between studies. Silknetter et al () identified parasitism at low partner abundances and mutualism at high abundances and this result is likely to be the result of novel resource trade; spawning substrate/parental care provided by the host in exchange for brood dilution. In contrast, Brown et al, () observed a mutualistic outcome at moderate partner densities but parasitism at high partner densities.…”

“…Stoll et al, ). The dashed black line indicates a relationship in which low symbiont densities are actually detrimental to the host, and do not benefit host fitness until a critical mass has been reached (sensu Silknetter et al, )…”

“…In other interactions, a critical mass of participants is needed for an interaction to benefit all species. For example, Silknetter et al (2019) found that increased partner density caused nest association to switch from parasitism to mutualism: low densities of partners made nests more conspicuous (attracting predators) without providing a beneficial dilution effect, and chubs were better off spawning without partners than with them at low densities. To manage these conflicting interests, some hosts punish over-exploitation by partners (Creed & Brown, 2018;Farrell et al, 2014;Frost & Elias, 1990), whereas others appear to have no defences for over-exploitation (Stoll et al, 2017) or over-exploitation is not predicted to occur (Peoples & Frimpong, 2016a).…”

The enemy of my enemy is my friend: Nematode infection of pollinating and non-pollinating fig wasps has net benefits for the fig-fig wasp pollination mutualism

“…However, theoretical works estimating negative (Ferriere et al 2002, Mougi and Kondoh 2014, Bachelot and Lee 2020 and neutral (Arizmendi et al 1996, Bronstein 2001) effects also exist, showcasing a presumable role for context-dependence in the diversity of community assemblages. The body of empirical research evaluating the role of community-interactions on mutualism fitness is limited, but growing (Bronstein 1991, Thompson and Fernandez 2006, Silknetter et al 2018, Song et al 2020. One impediment to investigating the effects of community-level antagonism on mutualism fitness is that lifetime fitness in many systems is difficult to quantify (West et al 1996, Bronstein 2001.…”

Positive co‐occurrence between feeding‐associative savannah fishes depends on species and habitat

“…the environment in which the interaction occurs) factors at the time of the interaction (Bronstein, 1994). Understanding context dependency in biotic interactions is key to predicting species response to environmental change (Chamberlain, Bronstein, & Rudgers, 2014), and a growing body of research is identifying the role of context dependency in freshwater systems (Brown et al, 2012;Peoples & Frimpong, 2016b;Silknetter et al, 2018). Moreover, a key debate in the general ecology literature centres on whether facilitation is necessary in benign habitats or is only relevant in stressful habitats (Holmgren & Scheffer, 2010).…”