Our findings supported two of the three hypothesized behavioral mechanisms to increase reproductive success of co-breeding males. Larger males invested more effort on a given nest than smaller males, and consequently were more reproductively successful. Thus, within-nest measures of effort were a correlate of male reproductive success. In addition, male reproductive success varied by nest. Reproductive success was higher for males who constructed larger nests together with more co-breeding males but constructing more nests did not increase reproductive success. These results show that reproductive success of co-breeding males increases due to multiple behavioral mechanisms.
Positive relationships between male body size and reproductive success are commonly reported in co-breeding species (Friedl and Klump 2000; Theuerkauf et al. 2009) and others (Lehtonen et al. 2007; Barber 2013; Bose et al. 2018). Agonistic behavioral interactions occur on nests and their outcomes depend on body size (Soler et al. 1998; Hellmann et al. 2020). Larger males of bluehead chub at times displayed aggressive behavior toward smaller males occupying the same nest in this study (S. Kim, pers. obs.) and others (Wallin 1989; Sabaj et al. 2000; Kim et al. 2020b). Males guarded their own spawning pits aggressively, while other males spawned simultaneously on the same nest by displaying a mutual tolerance as co-breeders (Fig. 1). Sneaking behavior was not observed in bluehead chub (Kim et al. 2020b). Accordingly, larger males did not solely own nests, resulting in positively size-dependent patterns of reproductive effort and success. Bluehead chub are short-lived (< 3–4 years) but iteroparous with 2–3 potential years of spawning (Lanchner 1952; Marcy Jr et al. 2005). Given the few annual opportunities to reproduce, we speculate that larger and presumably older males maximize reproductive effort in the current breeding season, but smaller, younger males balance current reproductive effort and its effects on subsequent survival and reproductive success while subject to the current constraint imposed by larger males due to their agonistic behavior (Taborsky 2001; Gross 2005).
Earlier, we reported that body size of males did not affect their reproductive success in the study stream (Kim et al. 2020b). The discrepancy between the earlier and current studies is likely due to three reasons. First, the current study used a subset of data reported by Kim et al. (2020b) by focusing on males detected by PIT antennas at the nests. A total of 64 males were marked with PIT tags between January and June 2017, but only 34 of them were detected on the 18 nests in the current study. We cannot know with certainty the fate of the males not detected by the antennas, whether it is mortality or emigration. It is plausible that body size differently affects reproductive success of males once they are on the nests versus survival during the few months leading up to breeding. Second, the current analysis explicitly accounted for variation in male reproductive success among nests, in contrast to Kim et al. (2020b). The male body size effect on reproductive success is indeed not readily discernable on a biplot (Fig. 5). By incorporating that male reproductive success varies among nests, our current analysis showed that male body size mattered relative to the size of other males on a given nest. Furthermore, our current approach assumed that reproductive success among males on the same nest is partitioned based on their relative effort measured by the time spent on the nest by each male. Third, larger males were detected earlier in the spawning season than smaller males, but Kim et al. (2020b) did not incorporate this seasonal pattern. By incorporating the nest random effect in the hierarchical model, the current analysis was able to account for the seasonal pattern indirectly. Overall, the current result updates our previous knowledge and provides a novel insight that male body size is indeed a predictor of reproductive success among males occupying the same nest.
Perhaps not surprisingly for a co-breeding species, construction of nests with more males led to larger nests and higher reproductive success. It is noteworthy that the 5 most reproductively successful males (range = 13–33) constructed the largest nest. Nest size is an indicator of male quality, thus it influences mate choice and reproductive success in many nest-building species (Soler et al. 1998; Barber 2013; Bose et al. 2018). Likewise, larger nests attracted more female bluehead chub so that males could increase encounter with their potential mates (Kim et al. 2020b). Larger nests were also visited and used for spawning by larger groups of yellowfin shiner in streams nearby, which would dilute predation effects on bluehead chub eggs (Silknetter et al. 2019; Kim et al. 2020a). Because constructing more nests did not increase male reproductive success in the current study, our data indicated that males could best increase reproductive success by constructing certain nests (i.e., larger nests) and spent more effort on those nests.
Our data did not support one hypothesis that constructing more nests would increase male reproductive success. We considered that this behavior would function as a bet-hedging strategy in a stochastic environment where high flows due to precipitation mobilize substrates that make up nests (i.e., nest failures) based on our previous studies (Kim and Kanno 2020; Kim et al. 2020a). In the current study, precipitation was recorded frequently in April (i.e., prior to the onset of the spawning season) but was recorded less frequently afterward (Appendix S2). Perhaps a bet-hedging strategy might be more effective in a hydrologically less stable condition. This idea could be tested in a longer-term study with contrasting summer precipitation regimes (i.e., dry versus wet summers) or in a design that incorporates space-for-time substitution (i.e., free-flowing versus flow-regulated rivers). A longer-term study to keep track of the same individuals in multiple years would also show whether nesting behaviors, such as number of nests to build in a single spawning season and number to males to build nests with, would change through ontogeny.
We were challenged to analyze this complex data set because the nest from which YOY originated could not be identified via the genetic assignment method, given that males were commonly recorded on multiple nests by the PIT antennas. An alternative approach would have been to collect eggs from nests (Silknetter et al. 2019). This requires lethal sampling and is logistically difficult because eggs of nest associates outnumber greatly those of bluehead chub on nests (Cashner and Bart 2010; Silknetter et al. 2019). We also experimentally tested the effect of male body size on reproductive success, but with equivocal results (Kim 2019), reflecting the difficulties of controlling body size and number of males in a manipulative experiment in the wild. Sampling YOY in the current study integrates nest origin and survival in the subsequent few weeks, an approach suitable for measuring animal reproductive success (Westneat and Fox 2010). Ultimately, we devised a model-based solution by accounting explicitly for memberships of males to nests and reproductive effort of each male relative to others on each nest.
In conclusion, effort within nests was a stronger determinant of male reproductive success than effort among nests. This within-nest effort consisted of larger males spending more effort than smaller nests often accompanied by agonistic interactions, and more males building larger nests together. Coexistence of these two seemingly different mechanisms, aggression and cooperation, is not a shared behavior among species in genus Nocomis, and indeed this combination of male reproductive behaviors is rare among fishes (Taborsky 1994; 2009). Our study in this unique system demonstrated that aggression and cooperation shaped male reproductive success. This study provides a novel empirical insight on the evolution of mating systems because previous studies predominantly examined only aggression or cooperation (Gross 1996; Soler et al. 1998; Hellmann et a. 2020; but see Díaz-Muñoz et al. 2014).