Mr. Mom: Nocomis Embryo‐Burying Effectively Increases Embryo Survival Amidst Predation by All Mutualism Participants

Partner swapping and cheating: why do different minnow species spawn together?

Many North American minnows (Cyprinidae) exhibit nest association, a spawning mode in which one species (associate) uses nests constructed by another species (host). Although this relationship may be obligate for some species, many nest associates can use alternative reproductive modes, indicating that the strength of the relationship between associate and host may vary. Quantifying the strength of the nest association relationship represents a necessary first step for understanding the importance of this interaction to stream fish communities. To address this question, we conducted a literature review of ecological and ethological reproductive traits for 11 nest associates of Nocomis occurring in the New River basin, Virginia. We used phylogenetic eigenvector regression (PVR) to remove the effects of phylogenetic relatedness among species and used nonmetric multidimensional scaling (NMS) to ordinate a phylogenetically independent trait similarity matrix of the 11 species. Based on the ordination results, we delineated a group of strong and weak nest associates. Strong nest associates showed significant geographic range overlap with Nocomis, while weak ones did not. No difference in spawning temperature range overlap occurred between the two groups. We then tested for effects of nest association strength on species' rarity and found that most (6 of 7) strong nest associates held rare classifications based on one or more of geographic extent, habitat breadth, or local abundance. Conversely, all weak nest associates reflected common classifications. These results indicate that nest association strength is related to rarity; this potentially crucial aspect of conservation has been previously overlooked. Clearly, conservation of rare and imperiled nest associates should be pursued through protection of their host and, consequently, the mutualism they have evolved to exploit.

Several nest-building North American minnows (Cyprinidae) function as reproductive hosts to nest associates–species that require nests of other species for spawning. Understanding the microhabitat preferences of hosts can yield insight into the reproductive ecology of many species, especially of nest associates that can utilize nests of two or more hosts. We observed nests of Central stoneroller Campostoma anomalum in which several associate species were actively spawning. Bluehead chubs Nocomis leptocephalus began constructing nests two days later in the same stream, at which time associates abandoned stoneroller nests and continued on to spawn on chub nests. This presented a unique opportunity for accomplishing two objectives: (1) quantifying stoneroller nesting microhabitat preference and (2) comparing stoneroller and chub habitat preference to gain insight into the mechanisms that may drive host switching by nest associates. We measured substrate size, current velocity, water depth, and egg depth on seven paired stoneroller and chub nests, and compared these measurements to paired microhabitat measurements at a randomly selected point near each nest. Repeated measures analysis of variance with post hoc Tukey tests revealed that stonerollers exhibited distinct nesting microhabitat preferences from chubs. Gravel on stoneroller nests was considerably smaller than on chub nests and stonerollers nested in shallower depths than chubs. However, both species nested at similar current velocities. If nest associates switch partners based on the physical characteristics of nests, then substrate size is likely the most important factor. The larger gravel sizes on chub nests likely provide better egg aeration than stoneroller nests. Chub nests may also be safer for associate broods because male Bluehead chubs cover eggs with gravel after spawning; stonerollers do not. Future work should take an experimental approach to elucidate these mechanisms.

Although nest association among Nocomis chubs and other minnows (Cyprinidae) is common throughout North America, the overall outcome of this relationship and its mechanisms of costs and benefits remain unclear. Because imperilment of stream fishes is affected by reproductive traits, the implications of this widespread interaction must be understood. Nest association mechanisms were explored using a multiple working hypotheses framework on fish assemblage data from 25 reaches in three tributaries of the New River, Virginia, USA. Multiple linear regression models predicting reproductive success (age‐0 abundance) of chubs and associates were compared based on model weights (wi) calculated from Akaike's Information Criterion, adjusted for small sample size (AICc), and relative change in AICc among models. For age‐0 chubs, models represented hypotheses emphasizing the additive effects of adult abundance, nest abundance, and egg dilution by juvenile associates (causing decreased egg predation). For age‐0 associates, models represented hypotheses emphasizing adult associate abundance, gravel substrate availability, nest abundance, parental care (as nest defence) from chubs, and egg dilution by chubs. Model evidence suggests that chubs can sustain themselves (w = 0.61), but their reproductive success is enhanced by a dilution effect from juvenile strong associates (w = 0.37). Strong associate reproductive success was best described by variables emphasizing nest association interactions (w = 0.46) and natural sources of habitat variability (w = 0.45), whereas that of weak associates was more closely related to availability of unmodified habitat (w = 0.50). Chubs and associates appear to receive a net benefit from the association, suggesting a mutualistic relationship. Community‐wide conservation strategies may be useful for protecting symbiotic spawning fishes. In addition to competition and predation, conservation practitioners should consider positive interactions in conservation plans of imperiled mutualists. Copyright © 2013 John Wiley & Sons, Ltd.

Nest association, or the habit of spawning in the nest of another species, is a widespread reproductive strategy among North American fishes, especially minnows. The hosts of nest associates include sunfishes and nest-building minnows. Previous experiments demonstrated that nest associates benefited from the parental care of hosts. The purpose of this study was to determine the effect of nest associates on hosts, and thereby characterize the relationship as parasitic, mutualistic or commensal. Since hosts with associates had higher reproductive success than those without associates in this experiment, I characterize nest association as a mutualistic relationship, at least in some systems. The dilution effect is the proposed mechanism responsible for the higher reproductive success of hosts with associates.

Nest association in fishes affects the reproductive success of the host to varying degrees, from complete failure of the host’s reproduction to fitness advantages. Such varying impacts of nest association are considered to result from both the associate’s behavior and the characteristics of the host’s reproduction. To investigate the relationship between the impact of nest associate and host/associate ecology as well as evolutionary strategies involving nest association, we compared reproductive strategies and success between an associate East Asian minnow, Pungtungia herzi, and two host fishes (a goby, Odontobutis obscura, and a catfish, Pseudobagrus nudiceps) that have different reproductive ecologies. The associate frequently spawned around the days on which both hosts spawned, and gained a fitness advantage through continuous egg protection. Spawning by the associate had a negative effect on the survival of O. obscura eggs. Male O. obscura tended to abandon their nest when it was parasitized during the pre-spawning period. This is likely a tactic to alleviate the costs of brood parasitism. In contrast, survival of P. nudiceps eggs was consistently high in all nests, regardless of the intensity of associate’s spawning, and P. nudiceps young fed on cyprinid offspring (most probably the associate’s eggs/young) in the nest. Both P. nudiceps and P. herzi populations likely gain fitness benefits from their relationship. When comparing these two hosts with another known host, the freshwater perch Coreoperca kawamebari, the observed differences in the impact of nest association to the associate species likely correspond to differences in the spatial reproductive resources used by the respective hosts.

Nest construction by males is a common reproductive strategy in fishes, but little is known about intra-specific variation in nesting behavior and reproductive interactions with other species. In the southeastern USA, reproductive interactions between bluehead chub (Nocomis leptocephalus) and their nest associate, such as yellowfin shiner (Notropis lutipinnis), are mutualistic because the shiner requires chub nests to spawn but the chub also benefits from additional shiner eggs by reducing predation risk on their own eggs (i.e., dilution effect). As proxies for reproductive success of bluehead chub, we studied factors affecting their nest size variation and utilization by yellowfin shiner in three streams in the upper Piedmont region of South Carolina, USA. A total of 92 nests (71 spawned and 21 abandoned) were located, and we recorded spawning activity, nest size, number and size of male bluehead chub, number of yellowfin shiner, and environmental variables for 89 consecutive days in 2016. Path analysis showed that larger males spawned earlier in the season than smaller males, and instances of pebble re-use for nest construction increased through the spawning season, which extended from April to June. Larger males more likely shared the same nest with each other than smaller males, and larger or more males constructed larger nests and attracted more yellowfin shiner. Nest size also increased when males re-used substrate materials from old nests, and nests built in this manner (36 nests) were equally prevalent as newly constructed nests (35 nests). This study suggests that complex mechanisms mediate host nest size and interactions with nest associates, and individual variation likely shapes dynamics of the mutualistic reproductive interaction.

Yellowfin shiners spawn in nests constructed by male bluehead chubs. To determine whether yellowfin shiners are obligatory symbionts of bluehead chubs, different densities of shiners were isolated from chubs and presented with artificial nests in stream enclosures. Yellowfin shiners failed to reproduce in the absence of bluehead chubs, indicating that the symbiosis is obligatory for the shiners. Bluehead chubs tended nests by moving stones, which kept the nests free of silt. Nest tending lasted for the same amount of time that embryos and larvae of both species were found in the nests. Yellowfin shiners benefit from a protective nest and parental care given by the chub. Eggs, embryos and larvae of both species may benefit from reduced predation due to a dilution effect. These observations suggest that this nest association is an obligatory, mutualistic symbiosis.

Premating barriers such as variation in reproductive behaviour can evolve quickly, but because gametic and postzygotic incompatibilities often evolve more slowly, circumstances that bring gametes into contact can breach the boundaries of premating isolation. In aquatic environments, the gametes of organisms with external fertilization are released into a constantly moving environment and may come into contact with heterospecific gametes. In fishes, nest association (spawning in another species' nest) is a behaviour that brings gametes from different species into close spatiotemporal proximity. These interactions might increase chances of hybridization, especially when multiple species associate with a single nest builder. This study addresses these interactions in the largest clade of North American freshwater fishes, the minnows (Cyprinidae). We compiled a list of over 17,000 hybrid specimens in conjunction with species distribution data, breeding behaviours, and an inferred phylogeny to test if breeding behaviour, in addition to evolutionary history, is an important predictor of hybridization. We find that breeding behaviour is a significant predictor of hybridization, even when phylogenetic relatedness and divergence time are accounted for. Specifically, nest associates are more likely to hybridize with other nest associates whereas non-nesting species had relatively low rates of hybridization.

Mechanisms of Convergent Egg Provisioning in Poison Frogs.

Mutualisms are complex, interspecific relationships, which sometimes create "selfish-herds" as individuals of each species compete to maximize their own fitness. Nest association, where individuals of different species spawn on a nest created by a host species, is a reproductive interaction characteristic of some minnows (Leuciscidae) and is considered mutualistic despite mimicking the behavior labeled "brood parasitism." We studied the spawning behaviors of bluehead chub (Nocomis leptocephalus) and its nest associates, testing the hypothesis that bluehead chub exploits the selfish-herd dynamic in a novel manner by arranging embryos within its nest to maximize the survival of its own offspring at the expense of the nest associates' offspring. Our results show that embryos were not uniformly distributed within a nest, as one section representing one-sixth of the nest's total volume contained a disproportionate percentage of embryos (x¯ = 40.0% ± 6.1% SE). We found three-quarters of host embryos within deeper nest sections safer from embryo predators, whereas only a third of all associate embryos were found in the same sections. These results support our hypothesis that male Nocomis leptocephalus create "embryonic selfish-herds" within their nests. This is the first study to document the existence of embryonic selfish-herds, a phenomenon that warrants the reexamination of some vertebrate reproductive interactions labeled as brood parasitism.

Variation in nest predation rates among bird species are assumed to reflect differences in risk that are specific to particular nest sites. Theoretical and empirical studies suggest that parental care behaviors can evolve in response to nest predation risk and thereby differ among ecological conditions that vary in inherent risk. However, parental care also can influence predation risk. Separating the effects of nest predation risk inherent to a nest site from the risk imposed by parental strategies is needed to understand the evolution of parental care. Here we identify correlations between risks inherent to nest sites, and risk associated with parental care behaviors, and use an artificial nest experiment to assess site‐specific differences in nest predation risk across nesting guilds and between habitats that differed in nest predator abundance. We found a strong correlation between parental care behaviors and inherent differences in nest predation risk, but despite the absence of parental care at artificial nests, patterns of nest predation risk were similar for real and artificial nests both across nesting guilds and between predator treatments. Thus, we show for the first time that inherent risk of nest predation varies with nesting guild and predator abundance independent of parental care.

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.

Theories of parental care evolution predict that genetic relatedness will be an important variable in the amount of care a parent provides. However, current inferences of relatedness-based parental investment from studies in humans and birds remain challenged. No study has yet demonstrated parental care adjustment in a manner uncomplicated by life-history correlates or experimental design. We now present a unique test that controls for individual life histories and demonstrates paternity-related dynamic adjustments in parental care. Brood-rearing male bluegill sunfish (Lepomis macrochirus) that are cuckolded to a varying degree will either increase or decrease their parental investment in response to changing information on paternity during brood development. Specifically, as parental males detect paternity lost to cuckolders and, hence, a reduction in the value of their brood, they adaptively lower their level of parental care. Conversely, if they detect that their paternity is higher than previously assessed, they adaptively raise their level of parental care. This dynamic adjustment during brood rearing indicates the importance of genetic relatedness in parental investment decisions and provides needed empirical support for theoretical predictions.

Predation risk on birds is often an important source of natural selection that shapes parental care and may promote behavioral changes. Parents can often estimate certain risks and adjust their behavior to reduce the likelihood of nest predation. The fragmentation of habitats is one of the main consequences of loss of habitats, and in general, for birds breeding in smaller patches, their daily nest-survival rate is lower due to increased nest predation. Since nest survival is an estimate of predation risk in the environment, we evaluated the daily survival rate (DSR) for nests of spectacled tyrants (Hymenops perspicillatus) and parental care behavior on fragmented and unfragmented grasslands. We conducted nest searching and monitoring during the 2012–2013 breeding season in small patches and in a continuous patch of grassland. In addition, parental activity was recorded using video monitoring. We found a lower DSR for the spectacled tyrant in fragmented grasslands, associated with increased nest predation risk; females showed a variation in parental care. This variation was evidenced by larger incubation bouts and lower visitation rate during the incubation period, and by a lower food delivery rate to nestlings, compensated by larger prey sizes. The results show that fragmentation not only reduces the fitness of individuals and impacts adversely on population, but individuals are also subjected to a strong selection pressure, and their reproductive success may depend to some extent on the ability of parents to estimate at least certain predation risk and adjust their behavior in this regard.