Susan E. Marsh-Rollo

Demography and substrate affinity of the round goby (Neogobius melanostomus) in Hamilton Harbour

ABSTRACT The invasive round goby, Neogobius melanostomus, consumes eggs and fry of other fishes, competes for resources with native fish species, and hence poses a threat to Great Lakes aquatic communities. We provide the first description of round goby demographic patterns in Hamilton Harbour, in the western tip of Lake Ontario, and the connected Cootes Paradise Marsh, a recently restored wetland. By monitoring round goby populations on a variety of distinct habitats for 7 years (2002–2008), we found that populations have declined at all sample locations and that average fish body size also has decreased. We also related abundance, body size, and reproductive patterns to seasonality, to substrate types (mud, sand, cobble and boulder) and to water quality in all locations. Round gobies were found on all substrates sampled including mud, although they were less abundant on mud than on other substrates, and to date have not extensively colonized Cootes Paradise Marsh. Our work confirms previous studies, which have suggested that habitats lacking hard structures will have fewer round gobies because they lack substrates on which round gobies can breed. However, our results also indicate that muddy and sandy substrates are not resistant to round goby invasion and will not prevent round goby colonization, a potential concern for Cootes Paradise Marsh an important spawning, nursery, and refuge habitat for warmwater native fishes and for other similar wetlands.

Liver size reveals social status in the African cichlid Neolamprologus pulcher

Wild groups (n = 167) of the cooperatively breeding Lake Tanganyika cichlid, Neolamprologus pulcher, were used to investigate how social status and sex influence liver investment. In contrast to expectations, males and females (controlling for body size) had similar liver investment and subordinates (both sexes) had relatively larger livers compared with dominants. Three hypotheses were considered for why social status results in liver size disparity: liver mass might reflect status-dependent differences in (1) energy expenditure, (2) energy storage and (3) energy acquisition. First, dominants performed more energetically costly behaviours (e.g. social policing and care) compared with subordinates, supporting the notion that energy expenditure drives liver investment. Moreover, dominants in large groups (with many subordinates to monitor) and those holding multiple territories (with large areas to patrol), tended to have smaller livers. Second, subordinates did not appear to use the liver as a strategic energy storage organ. In laboratory and field experiments, subordinates ascending in rank had similar or larger livers during periods of rapid growth compared with non-ascending controls. Third, although subordinates fed more frequently than dominants, a negative relationship was found between feeding rates and liver size. Hence, these results contrast with previous liver studies and suggest that liver investment patterns were linked to status-driven differences in energy expenditure but not to energy intake or storage in N. pulcher.

Is there a role for aggression in round goby invasion fronts

The role of aggression as a factor promoting invasiveness remains hotly debated. Increased aggression or a lack of tolerance for conspecifics may promote population spread. Some previous research suggests that more aggressive or bold individuals are increasingly likely to disperse and as such these individuals may be overrepresented at the invasion front. In contrast, it has also been argued that individuals at the invasion front represent the least aggressive or least competitive individuals in the population, as these animals are excluded from established areas. Accordingly, the invasion front should be made up of shy, submissive individuals that exhibit reduced aggression. In this study we explore these alternative predictions by quantifying the levels of intra-specific aggression in the round goby (Neogobius melanostomus), an invasive fish that continues to spread rapidly through the Laurentian Great Lakes region in North America. We collected size matched male round goby from an invasion front as well as from an area with an established population, and we staged resource contests between them. Invasion front fish won 65% of the contests and tended to perform more aggressive acts overall. Invasion front fish were not more active or bold prior to the contest, and used the same types of aggressive displays as fish from established areas. Our results also showed that body size asymmetry was an overriding determinant of competitive outcomes, and that body size rather than individual variation in aggressiveness might be the most important contributing factor determining the composition of round goby invasion fronts throughout the Laurentian Great Lakes and its tributaries.

Ovarian fluid allows directional cryptic female choice despite external fertilization

In species with internal fertilization, females can favour certain males over others, not only before mating but also within the females reproductive tract after mating. Here, we ask whether such directional post-mating (that is, cryptic) female mate choice can also occur in species with external fertilization. Using an in vitro sperm competition experiment, we demonstrate that female ovarian fluid (ovarian fluid) changes the outcome of sperm competition by decreasing the importance of sperm number thereby increasing the relative importance of sperm velocity. We further show that ovarian fluid does not differentially affect sperm from alternative male phenotypes, but generally enhances sperm velocity, motility, straightness and chemoattraction. Under natural conditions, female ovarian fluid likely increases the paternity of the preferred parental male phenotype, as these males release fewer but faster sperm. These results imply females have greater control over fertilization and potential to exert selection on males in species with external fertilization than previously thought possible.

The Stress Response of the Highly Social African Cichlid Neolamprologus pulcher

In group‐living species, dominant individuals are frequently aggressive toward subordinates, and such dominant aggression can lead to chronic stress, higher glucocorticoid levels, and decreased fitness for subordinates. However, in many cooperatively breeding species, it is surprisingly the dominants rather than the subordinates that exhibit higher levels of glucocorticoids, a possible consequence of the demands of maintaining high social rank and socially suppressing the reproduction of other group members. This study investigates the relationship between social status and circulating plasma cortisol in groups of the cooperatively breeding African cichlid Neolamprologus pulcher. Baseline (resting) levels of cortisol were quantified, as was the cortisol response following an acute stressor. Dominants had the higher cortisol concentrations, and these were not related to their social behavior. Cortisol concentrations correlated (positively) with social behaviors and general activity levels only in subordinate males, arguably the individuals with the least stability in the social group. No status‐dependent differential responses to acute stress were detected, suggesting that the status‐induced chronic stress has little effect on the capacity to mount a full stress response to large‐scale, life‐threatening risk.

Brain nonapeptide levels are related to social status and affiliative behaviour in a cooperatively breeding cichlid fish.

The mammalian nonapeptide hormones, vasopressin and oxytocin, are known to be potent regulators of social behaviour. Teleost fishes possess vasopressin and oxytocin homologues known as arginine vasotocin (AVT) and isotocin (IT), respectively. The role of these homologous nonapeptides in mediating social behaviour in fishes has received far less attention. The extraordinarily large number of teleost fish species and the impressive diversity of their social systems provide us with a rich test bed for investigating the role of nonapeptides in regulating social behaviour. Existing studies, mostly focused on AVT, have revealed relationships between the nonapeptides, and both social behaviour and dominance status in fishes. To date, much of the work on endogenous nonapeptides in fish brains has measured genomic or neuroanatomical proxies of nonapeptide production rather than the levels of these molecules in the brain. In this study, we measure biologically available AVT and IT levels in the brains of Neolamprologus pulcher, a cooperatively breeding cichlid fish, using high performance liquid chromatography with fluorescence detection. We found that brain AVT levels were higher in the subordinate than in dominant animals, and levels of IT correlated negatively with the expression of affiliative behaviour. We contrast these results with previous studies, and we discuss the role the nonapeptide hormones may play in the regulation of social behaviour in this highly social animal.

Is there convergence in the molecular pathways underlying the repeated evolution of sociality in African cichlids

Despite wide variation in the complexity of social interactions across taxa, the basic behavioral components of sociality appear to be modulated by conserved hormone pathways. Specifically, the nonapeptide hormones oxytocin and vasopressin and their receptors have been implicated in regulating diverse social behaviors across vertebrates. Here, we took advantage of the repeated evolution of cooperative breeding in African cichlids to investigate whether there are consistent brain gene expression patterns of isotocin and arginine vasotocin (teleost homologues of oxytocin and vasopressin), as well as their receptors, between four closely related pairs of social (cooperative) and non-social (non-cooperative) species. We first found that the coding sequences for the five genes studied were highly conserved across the eight species. This is the first study to examine the expression of both isotocin receptors, and so we performed a phylogenetic analysis that suggests that these two isotocin receptors are paralogues that arose during the teleost genome duplication. When we then examined brain gene expression patterns relative to social system, we found that there were whole-brain gene expression differences between the social and non-social species in many of the species pairs. However, these relationships varied in both the direction and magnitude among the four species pairs. In conclusion, our results suggest high sequence conservation and species-specific gene expression patterns relative to social behavior for these candidate hormone pathways in the cichlid fishes.

Does proximity to aquatic pollution affect reproductive traits in a wild-caught intertidal fish?

How chronic exposure to aquatic pollution affects reproductive traits was assessed in nesting wild-caught plainfin midshipman Porichthys notatus in areas with low and high contaminant exposure on Vancouver Island, British Columbia. Males in high-exposure areas had a greater degree of testicular asymmetry, sperm with shorter heads and fewer live eggs in their nests. The results of this study provide important insights into the potential consequences of contaminant exposure on the reproductive physiology of wild-caught fishes.

Reproductive sharing in relation to group and colony-level attributes in a cooperative breeding fish

The degree to which group members share reproduction is dictated by both within-group (e.g. group size and composition) and between-group (e.g. density and position of neighbours) characteristics. While many studies have investigated reproductive patterns within social groups, few have simultaneously explored how within-group and between-group social structure influence these patterns. Here, we investigated how group size and composition, along with territory density and location within the colony, influenced parentage in 36 wild groups of a colonial, cooperatively breeding fish Neolamprologus pulcher. Dominant males sired 76% of offspring in their group, whereas dominant females mothered 82% of offspring in their group. Subordinate reproduction was frequent, occurring in 47% of sampled groups. Subordinate males gained more paternity in groups located in high-density areas and in groups with many subordinate males. Dominant males and females in large groups and in groups with many reproductively mature subordinates had higher rates of parentage loss, but only at the colony edge. Our study provides, to our knowledge, the first comprehensive quantification of reproductive sharing among groups of wild N. pulcher, a model species for the study of cooperation and social behaviour. Further, we demonstrate that the frequency of extra-pair parentage differs across small social and spatial scales.

Species-specific patterns of nonapeptide brain gene expression relative to pair-bonding behavior in grouping and non-grouping cichlids

Comparative studies have revealed that vasopressin-oxytocin pathways are associated with both pair bonding and grouping behavior. However, the relationship between pair bonding and grouping behavior remains unclear. In this study, our aim was to identify whether two species that differ in grouping behavior display a corresponding difference in their pair bonds, and in the underlying vasopressin-oxytocin hormonal pathways. Using two species of cichlid fishes, the highly social Neolamprologus pulcher and the non-social Telmatochromis temporalis, we measured proximity of pairs during pair bond formation, and then measured social behaviors (proximity, aggression, submission, affiliation) and brain gene expression of isotocin and arginine vasotocin (the teleost homologues of oxytocin and vasopressin, respectively), as well as their receptors, after a temporary separation and subsequent reunion of the bonded pairs. Pairs of the social species spent more time in close proximity relative to the non-social species. Rates of aggression increased in both species following the separation and reunion treatment, relative to controls that were not separated. Overall, whole brain expression of isotocin was higher in the social species relative to the non-social species, and correlated with proximity, submission, and affiliation, but only in the social species. Our results suggest that both a social and a non-social cichlid species have similar behavioral responses to a temporary separation from a mate, and we found no difference in the brain gene expression of measured hormones and receptors based on our separation-reunion treatment. However, our results highlight the importance of isotocin in mediating submissive and affiliative behaviors in cichlid fishes, and demonstrate that isotocin has species-specific correlations with socially relevant behaviors.