Environ Biol Fish (2020) 103:783–794 https://doi.org/10.1007/s10641-020-00980-x Diverse reproductive patterns of Bluehead Chub (Nocomis leptocephalus) and their relationships with nest size and interactions with an associate, Yellowfin Shiner (Notropis lutipinnis) Seoghyun Kim & Brandon K. Peoples & Yoichiro Kanno Received: 17 May 2019 /Revised: 25 March 2020 /Accepted: 6 May 2020 /Published online: 5 June 2020 # Springer Nature B.V. 2020 Abstract Nest construction by males is a common males, and instances of pebble re-use for nest construc- reproductive strategy in fishes, but little is known about tion increased through the spawning season, which ex- intra-specific variation in nesting behavior and repro- tended from April to June. Larger males more likely ductive interactions with other species. In the southeast- shared the same nest with each other than smaller males, ern USA, reproductive interactions between bluehead and larger or more males constructed larger nests and chub (Nocomis leptocephalus) and their nest associate, attracted more yellowfin shiner. Nest size also increased such as yellowfin shiner (Notropis lutipinnis), are mu- when males re-used substrate materials from old nests, tualistic because the shiner requires chub nests to spawn and nests built in this manner (36 nests) were equally but the chub also benefits from additional shiner eggs by prevalent as newly constructed nests (35 nests). This reducing predation risk on their own eggs (i.e., dilution study suggests that complex mechanisms mediate host effect). As proxies for reproductive success of bluehead nest size and interactions with nest associates, and indi- chub, we studied factors affecting their nest size varia- vidual variation likely shapes dynamics of the mutual- tion and utilization by yellowfin shiner in three streams istic reproductive interaction. in the upper Piedmont region of South Carolina, USA. A total of 92 nests (71 spawned and 21 abandoned) were Keywords Reproductive behavior . Mutualism . located, and we recorded spawning activity, nest size, Leuciscidae . Individual variation . Fitness number and size of male bluehead chub, number of yellowfin shiner, and environmental variables for 89 consecutive days in 2016. Path analysis showed that Introduction larger males spawned earlier in the season than smaller Fishes exhibit an array of parental care behavior for their Electronic supplementary material The online version of this offspring (Gross 2005). Nest construction, a form of article (https://doi.org/10.1007/s10641-020-00980-x)contains parental care, is widely used among fishes (Barber supplementary material, which is available to authorized users. 2013). Nest construction can serve two main functions for male fitness. First, males construct nests to protect S. Kim : Y. Kanno Department of Fish, Wildlife, and Conservation Biology, eggs and larvae against predation and environmental Colorado State University, Fort Collins, CO 80523-1474, USA conditions (e.g., high stream flows) (Suski and : : Ridgway 2007; Rushbrook et al. 2010). Thus, nest S. Kim B. K. Peoples Y. Kanno (*) construction can maximize offspring survival by pro- Department of Forestry and Environmental Conservation, Clemson University, Clemson, SC 29634-0317, USA viding a shelter and stable environment (Chin-Baarstad e-mail: [email protected] et al. 2009). Second, nests provide information on male quality that influences mate choice by females (Blais 784 Environ Biol Fish (2020) 103:783–794 et al. 2004;Wongetal.2007). Accordingly, variation in continents among a variety of taxa (Wisenden 1999). In nest size and design is a complex component of fish North America, nest association is common among mating systems and consequently affects reproductive minnows (Leuciscidae). During nest associative success (Wong et al. 2007;Barber2013; Lehtonen et al. spawning, associates often greatly outnumber nest 2015). building individuals. Eggs of associates comprise up to Male body size is associated with the timing of 97% of eggs in a nest (Wallin 1992; Cashner and Bart spawning, social hierarchy, territoriality, nest quality, 2010). Accordingly, nest building species benefit from a and hence reproductive success (Blais et al. 2004; ‘dilution effect’ by which high proportions of associate Lindström 1992;Lehtonenetal.2015). Larger males eggs on nests greatly reduce the probability of predation tend to spawn earlier and occupy better territories on eggs of nest building species (Johnston 1994a; (Lindström 1992;Oliveiraetal.1999). They use ag- Silknetter et al. 2019). Previous studies have shown that gressive behavior to secure nesting sites because domi- associate species select nests guarded by larger males nance hierarchies are typically structured by body size for spawning (Shao 1997). However, little is known (Lehtonen et al. 2015). In addition, larger males can about how a combination of factors, including nest construct higher quality (e.g., larger) nests because nest quality (e.g., nest size) or nest sharing behavior (i.e., building is energetically costly by requiring males to number of males on the same nest), operate to attract collect building materials from surrounding areas associates that determine reproductive success of nest (Lindström 1992). Thus, larger body size affords advan- building species. tages for not only gaining access to more females (Blais Bluehead chub (Nocomis leptocephalus) (hereafter, et al. 2004), but also protecting eggs to increase off- “chub”) is a suitable species to study intraspecific varia- spring survival (Suski and Ridgway 2007; Chin- tion in nesting behavior and interspecific reproductive Baarstad et al. 2009). interactions. Chub are distributed throughout the Atlantic However, smaller males can overcome the size- slope of North America and are abundant in the Blue dependent disadvantage by selecting alternative repro- Ridge and Piedmont of South Carolina (Lanchner 1952; ductive strategies, such as temporal segregation and Marcy et al. 2005). Chub engage in nest associative parasitic behavior (Sinervo and Zamudio 2001; spawning with yellowfin shiner (Notropis lutipinnis) Taborsky 1994). Additionally, nest sharing behavior (hereafter, “shiner”), which are also common throughout (where multiple males coordinate their behavior to at- the region (Wallin 1989, 1992; Marcy et al. 2005:Fig.1). tract females to the same nest) may also offset the size- Chub prefer to spawn in particular mesohabitats (e.g. mediated influence on reproductive success (Clutton- pool tails and slow runs; Peoples et al. 2014)andmicro- Brock 2002). Several nest sharing behaviors have been habitats (optimal depths and velocities; Bolton et al. documented in fishes (Taborsky 1994; Díaz-Muñoz 2015; Peoples et al. 2016). Single or multiple males et al. 2014). Males of some fishes show mutual tolerance construct a dome-shaped nest composed of pebble- and share mates while spawning at the same nesting sized substrates for spawning (Wallin 1989; Sabaj et al. sites (Reighard 1920). Cooperative parental care among 2000). After spawning, males continue to move pebbles individuals is also known in other species (Reighard onto the nest, increasing the size of the nest (Wallin 1989; 1943;Wallin1989). Such an array of reproductive Peoples et al. 2016). Additionally, males utilize nesting strategies provides valuable insights into reproductive resources (i.e., pebbles) from existing nests to build new cooperation among male fish, but questions still remain ones later in the spawning season (Wallin 1989). Like about how nest sharing behavior affects the quality of some leuciscids, shiner are an obligate nest associate nests and subsequently reproduction. (Peoples and Frimpong 2016), and cannot spawn without Factors affecting behavior and nest quality become a host species (Wallin 1992). further complicated when reproductive interactions oc- The goal of this study was to quantify factors affect- cur with other species. Positive reproductive interactions ing two key variables related to the reproductive success (mutualism, commensalism, and facilitation) occur be- of chub: (1) nest size at the completion of reproductive tween many nest building species and ‘nest associates’, activities (including parental care), and (2) nest utiliza- or fishes that spawn in nests constructed by other species tion by shiner (shiner abundance on nests). We focused (Johnston and Page 1992). Nest associative behavior is on these two response variables because (1) nest size is diverse, having evolved independently on at least three typically an indicator of reproductive success of males Environ Biol Fish (2020) 103:783–794 785 in fishes (Lehtonen et al. 2007), particularly in polyga- mm), used by chub for nest construction, accounted for mous mating systems of chub where males can mate 47–49% of substrate across three streams (Table 1). with multiple females and larger nest size can accom- Common species found across all streams included modate more females (Wallin 1989; Sabaj et al. 2000), bluegill (Lepomis macrochirus), creek chub (Semotilus and (2) higher abundance of spawning shiner benefits atromaculatus), green sunfish (L. cyanellus), redbreast egg survival of chub via the dilution effect (Johnston sunfish (L. auritus), and striped jumprock (Moxostoma 1994b;Silknetteretal.2019). Using a path analysis, we rupiscartes). Rosyface chub (Hybopsis rubrifrons), an- developed and tested a working conceptual hypothesis other known nest associate (Marcy et al. 2005), was of causal relationships