Size dependent antipredator responses in a fish-shrimp mutualism.

For prey, taking refuge from predators has obvious fitness benefits but may also be costly by impinging on time and effort available for feeding or attracting mates. The antipredator responses of refuge-seeking animals are therefore predicted to vary strategically depending on how threatening they perceive the risk. To test this, we studied the impacts of a simulated predatory threat on the antipredator responses of wild sandy prawn-gobies (Ctenogobiops feroculus) that co-inhabit burrows with Alpheus shrimp (family Alpheidae) in a mutualistic relationship. We exposed goby-shrimp pairs, repeatedly on three separate occasions, to an approaching threat and measured the antipredator behaviours of both partners. We found that re-emerging from the burrow took longer in large compared to small fish. Moreover, quicker re-emergence by small-but not medium or large-sized gobies-was associated with an earlier flight from the approaching threat (i.e. when the threat was still further away). Finally, the goby and shrimp sharing a burrow were matched in body size and their risk-taking behaviour was highly dependent on one another. The findings contribute to our understanding of how an individual's phenotype and perception of danger relates to its risk-taking strategy, and how mutualistic partners can have similar risk sensitivities.

The ecology and fishery of the vendace (Coregonus albula) in the Baltic Sea.

Brackish water ecosystems often have high primary production, intermediate salinities, and fluctuating physical conditions and therefore provide challenging environments for many of their inhabitants. This is especially true of the Baltic Sea, which is a large body of brackish water under strong anthropogenic influence. One freshwater species that is able to cope under these conditions in the northern Baltic Sea is the vendace (Coregonus albula), a small salmonid fish. Here, we review the current knowledge of its ecology and fishery in this brackish water environment. The literature shows that, by competing for resources with other planktivores and being an important prey for a range of larger species, C. albula plays a notable role in the northern Baltic Sea ecosystem. It also sustains significant fisheries in the coastal waters of Sweden and Finland. We identify the need to better understand these C. albula populations in terms of the predator-prey interactions, distributions of anadromous and sea spawning populations and other putative (eco)morphs, extent of gene exchange between the populations, and effects of climate change on their future. In this regard, we recommend strengthening C. albula-related research and management efforts by improved collaboration and coordination between research institutions, other governmental agencies, and fishers, as well as by harmonization of fishery policies across national borders.

Pervasive admixture and the spread of a large-lipped form in a cichlid fish radiation.

Adaptive radiations have proven important for understanding the mechanisms and processes underlying biological diversity. The convergence of form and function, as well as admixture and adaptive introgression, are common in adaptive radiations. However, distinguishing between these two scenarios remains a challenge for evolutionary research. The Midas cichlid species complex (Amphilophus spp.) is a prime example of adaptive radiation, with phenotypic diversification occurring at various stages of genetic differentiation. One species, A. labiatus, has large fleshy lips, is associated with rocky lake substrates, and occurs patchily within Lakes Nicaragua and Managua. By contrast, the similar, but thin-lipped, congener, A. citrinellus, is more common and widespread. We investigated the evolutionary history of the large-lipped form, specifically regarding whether the trait has evolved independently in both lakes from ancestral thin-lipped populations, or via dispersal and/or admixture events. We collected samples from distinct locations in both lakes, and assessed differences in morphology and ecology. Using RAD-seq, we genotyped thousands of SNPs to measure population structure and divergence, demographic history, and admixture. We found significant between-species differences in ecology and morphology, local intraspecific differences in body shape and trophic traits, but only limited intraspecific variation in lip shape. Despite clear ecological differences, our genomic approach uncovered pervasive admixture between the species and low genomic differentiation, with species within lakes being genetically more similar than species between lakes. Taken together, our results suggest a single origin of large-lips, followed by pervasive admixture and adaptive introgression, with morphology being driven by local ecological opportunities, despite ongoing gene-flow.

Las radiaciones adaptativas han demostrado ser clave para entender los mecanismos y procesos responsables de la diversidad biológica. La convergencia en forma y función, así como la mezcla genética y la introgresión adaptativa, son algo común en las radiaciones adaptativas. Sin embargo, distinguir entre estos dos escenarios sigue siendo un desafío para la biología evolutiva. El complejo de especies del cíclido de Midas (Amphilophus spp.) es un ejemplo paradigmático de radiación adaptativa, con diversidad fenotípica en varias etapas de diferenciación genética. Una de las especies, A. labiatus, que tiene labios grandes y carnosos, se asocia a zonas rocosas de los lagos, y tiene una distribución irregular en los lagos Nicaragua y Managua. En cambio, A. citrinellus, es una especie similar pero con labios finos, más común y con una distribución más amplia. Investigamos la historia evolutiva de la especie de labios grandes y, en concreto, si este rasgo ha evolucionado de forma independiente en los dos grandes lagos nicaragüenses a partir de poblaciones ancestrales de labios finos, o si por el contrario se ha dispersado mediante migración y/o mezcla genética. Colectamos muestras de distintas localidades en ambos lagos y evaluamos las diferencias en morfología y ecología. Genotipamos miles de SNPs utilizando RAD-seq para medir la estructura genética, la divergencia, la historia demográfica y la mezcla genética de las poblaciones. Encontramos diferencias significativas entre especies en ecología y morfología, diferencias intraespecíficas locales en la forma del cuerpo y rasgos tróficos, pero sólo una limitada variación intraespecífica en la forma de los labios. A pesar de las claras diferencias ecológicas, el análisis genómico desveló una intensa mezcla genética entre especies, y una limitada diferenciación genómica, encontrando mayor semejanza genética entre especies dentro de un mismo lago, que entre especies de distintos lagos. Nuestros resultados sugieren un origen único de la especie de labios gruesos seguido de mezcla genética e introgresión adaptativa, e indican que la morfología habría sido modelada por las oportunidades ecológicas locales, a pesar del flujo génico.

Long-Term Pharmaceutical Contamination and Temperature Stress Disrupt Fish Behavior.

Natural environments are subject to a range of anthropogenic stressors, with pharmaceutical pollution being among the fastest-growing agents of global change. However, despite wild animals living in complex multi-stressor environments, interactions between pharmaceutical exposure and other stressors remain poorly understood. Accordingly, we investigated effects of long-term exposure to the pervasive pharmaceutical contaminant fluoxetine (Prozac) and acute temperature stress on reproductive behaviors and activity levels in the guppy (Poecilia reticulata). Fish were exposed to environmentally realistic fluoxetine concentrations (measured average: 38 or 312 ng/L) or a solvent control for 15 months using a mesocosm system. Additionally, fish were subjected to one of three acute (24 h) temperature treatments: cold stress (18 °C), heat stress (32 °C), or a control (24 °C). We found no evidence for interactive effects of fluoxetine exposure and temperature stress on guppy behavior. However, both stressors had independent impacts. Fluoxetine exposure resulted in increased male coercive copulatory behavior, while fish activity levels were unaffected. Under cold-temperature stress, both sexes were less active and males exhibited less frequent reproductive behaviors. Our results demonstrate that long-term exposure to a common pharmaceutical pollutant and acute temperature stress alter fundamental fitness-related behaviors in fish, potentially shifting population dynamics in contaminated ecosystems.

Aggression towards shared enemies by heterospecific and conspecific cichlid fish neighbours.

Successful territory defence is a prerequisite for reproduction across many taxa, and often highly sensitive to the actions of territorial neighbours. Nevertheless, to date, assessments of the significance of the behaviour of heterospecific neighbours have been infrequent and taxonomically restricted. In this field study, I examined the importance of both heterospecific and conspecific neighbours in a biparental fish, the convict cichlid, Amatitlania siquia. This was done by assessing the colonisation rates of vacant territories, the rates of aggression by the territory holders, and the overall rates of aggression towards intruders, in treatments that controlled the proximity of both neighbour types. Convict cichlid pairs colonised vacant nesting resources (territory locations) at similar rates independent of the proximity of heterospecific (moga, Hypsophrys nicaraguensis) or conspecific neighbours. However, a model of sympatric cichlid intruder was subjected to considerably higher overall levels of aggression when mogas were nearby. In contrast, the proximity of conspecifics did not have a significant effect on the overall aggression towards the intruder. These results suggest that previously demonstrated higher survival of convict cichlid broods in close proximity of mogas may be driven by aggression towards shared enemies. No conclusive evidence was found regarding whether mogas also influence convict cichlids' investment into anti-intruder aggression: the results show a marginally non-significant trend, and a moderately large effect size, to the direction of a lower investment in mogas', but not conspecifics', proximity. More generally, heterospecific neighbours may provide protective benefits in a wider range of ecological settings than commonly considered.

The influence of recent social experience and physical environment on courtship and male aggression.

BACKGROUND: Social and environmental factors can profoundly impact an individual's investment of resources into different components of reproduction. Such allocation trade-offs are expected to be amplified under challenging environmental conditions. To test these predictions, we used a desert-dwelling fish, the desert goby, Chlamydogobius eremius, to experimentally investigate the effects of prior social experience (with either a male or a female) on male investment in courtship and aggression under physiologically benign and challenging conditions (i.e., low versus high salinity). RESULTS: We found that males maintained a higher level of aggression towards a rival after a recent encounter with a female, compared to an encounter with a male, under low (but not high) salinity. In contrast, male investment in courtship behaviour was unaffected by either salinity or social experience. CONCLUSION: Together, our results suggest that male investment in aggression and courtship displays can differ in their sensitivity to environmental conditions and that not all reproductive behaviours are similarly influenced by the same environmental context.

Allopatry, competitor recognition and heterospecific aggression in crater lake cichlids.

BACKGROUND: Aggressive behaviour can have significant evolutionary consequences-not only within species, but also in the context of heterospecific interactions. Here, we carried out an experimental field study to investigate the importance of phenotypic similarity on levels of aggression between species whilst controlling for familiarity effects using manipulated allopatric stimuli. Specifically, we investigated aggressive responses of territory holding males and females in two species of Neotropical cichlid fish, Amphilophus sagittae and Hypsophrys nicaraguensis, that differ in their phenotypic similarity to our allopatric stimulus species, Amphilophus astorquii. RESULTS: We found that, independent of phenotypic similarity (and correlated phylogenetic proximity) between the territory holders and intruder, territorial aggression was not adjusted in relation to allopatric intruder colour markings that are associated with different levels of threat and known to provoke different responses in a sympatric setting. We also found that males and females did not differ in their overall patterns of aggression adjustment towards intruder cues. Nevertheless, the two focal species, which share the same breeding grounds and external threats, exhibited different sex roles in breeding territory defence. CONCLUSION: Together with earlier studies assessing hetrospecific aggression in sympatry, our current results highlight the importance of coevolution and learning in species interactions.

Effects of salinity on nest-building behaviour in a marine fish.

BACKGROUND: Parental allocation and reproductive success are often strongly influenced by environmental factors. In this respect, salinity is a key factor influencing species distributions and community structure in aquatic animals. Nevertheless, the effects of salinity on reproductive behaviours are not well known. Here, we used the sand goby (Pomatoschistus minutus), a small fish inhabiting a range of different salinities, to experimentally assess the effects of changes in salinity on nesting behaviour, a key component of reproduction in sand gobies and many other taxa. RESULTS: We found that salinity levels influenced some aspects of male nesting behaviour (i.e. nest entrance size) but not others (i.e. latency to build a nest, choice of nest site, sand on top of nest) and that small and large individuals were differently affected. In particular, the importance of body size in adjustment of nest entrance depended on the salinity level. CONCLUSION: The results support the prediction that geographically widespread aquatic species, such as sand gobies, are able to perform well under a range of salinity levels. The phenotype by environment interaction found between male size and behavioural responses to salinity can, in turn, help to explain the notable variation observed in nest-building (and other) behaviours closely linked to reproduction.

Cichlid Fish Use Coloration as a Cue to Assess the Threat Status of Heterospecific Intruders.

The ability to assess the threat posed by competitors, and to respond appropriately, is important for reducing the costs of aggression. In this respect, aggression directed toward heterospecifics is often just as significant as aggression among conspecifics. This is especially true for cichlid fish that share breeding grounds with heterospecifics. Indeed, cichlids are known to differentiate not only between conspecifics that pose different levels of threat but also between heterospecific territorial intruders by directing more aggression toward nonbreeding individuals. To assess whether the ability to make such distinctions could be based on color cues alone, we carried out a field study in which we experimentally presented Amphilophus sagittae cichlid pairs with model intruders of a sympatric congener, Amphilophus xiloaensis, in breeding versus nonbreeding coloration. Consistent with our prediction, we found that A. sagittae exhibited more aggression toward A. xiloaensis models of the latter color type. The results are, to our knowledge, the first to show that territory holders can, based on coloration alone, assess variation among individuals of a species other than their own in the threat posed to offspring survival.

Heterospecific aggression bias towards a rarer colour morph.

Colour polymorphisms are a striking example of phenotypic diversity, yet the sources of selection that allow different morphs to persist within populations remain poorly understood. In particular, despite the importance of aggression in mediating social dominance, few studies have considered how heterospecific aggression might contribute to the maintenance or divergence of different colour morphs. To redress this gap, we carried out a field-based study in a Nicaraguan crater lake to investigate patterns of heterospecific aggression directed by the cichlid fish, Hypsophrys nicaraguensis, towards colour polymorphic cichlids in the genus Amphilophus. We found that H. nicaraguensis was the most frequent territorial neighbour of the colour polymorphic A. sagittae. Furthermore, when manipulating territorial intrusions using models, H. nicaraguensis were more aggressive towards the gold than dark colour morph of the sympatric Amphilophus species, including A. sagittae. Such a pattern of heterospecific aggression should be costly to the gold colour morph, potentially accounting for its lower than expected frequency and, more generally, highlighting the importance of considering heterospecific aggression in the context of morph frequencies and coexistence in the wild.

Odour cues from suitors' nests determine mating success in a fish.

Animals use a range of sensory cues for finding food, avoiding predators and choosing mates. In this regard, the aquatic environment is particularly suitable for the use of olfactory and other chemical cues. Nevertheless, mate choice research, even on aquatic organisms, has focused on visual signals, while chemical cues relevant in sexual selection have been assumed to be 'intrinsic' excretions of mate candidates. Here, using the sand goby Pomatoschistus minutus, a small fish with paternal egg care, we investigated the possibility that 'extrinsic' chemical cues in the males' nests could also have a significant contribution to mating success. We found that females strongly avoided laying eggs into nests subject to the odour of Saprolegnia water moulds (an egg infection) and that this effect was independent of the females' initial, visually based preference for males. To the best of our knowledge, this is the first study to show that chemical cues related to parental failure can play a large role in sexual selection.

Infections may select for filial cannibalism by impacting egg survival in interactions with water salinity and egg density.

In aquatic environments, externally developing eggs are in constant contact with the surrounding water, highlighting the significance of water parameters and pathogens for egg survival. In this study we tested the impact of water salinity, egg density and infection potential of the environment on egg viability in the sand goby (Pomatoschistus minutus), a small fish that exhibits paternal egg care and has a marine origin, but which in the Baltic Sea lives in brackish water. To manipulate the infection potential of the environment, we added either a Saprolegnia infection vector into UV-filtered water or a fungicide into natural Baltic Sea water. Saprolegnia are widely spread water moulds that are a key cause of egg mortality in aquatic organisms in fresh- and brackish water. We found that increased water salinity indeed decreased the egg infection rate and had a positive effect on egg viability, while high egg density tended to have the opposite effect. However, the different factors influenced egg viability interactively, with a higher egg density having negative effects at low, but not in high, salinity. Thus, the challenges facing marine organisms adapting to lower salinity levels can be amplified by Saprolegnia infections that reduce egg survival in interaction with other environmental factors. Our results support the hypothesis that suppressing egg infections is an important aspect of parental care that can select for filial cannibalism, a common but poorly understood behaviour, especially in fish with parental care.

Body size mediates social and environmental effects on nest building behaviour in a fish with paternal care.

Body size, social setting, and the physical environment can all influence reproductive behaviours, but their interactions are not well understood. Here, we investigated how male body size, male-male competition, and water turbidity influence nest-building behaviour in the sand goby (Pomatoschistus minutus), a marine fish with exclusive paternal care. We found that environmental and social factors affected the nest characteristics of small and large males differently. In particular, association between male size and the level of nest elaboration (i.e. the amount of sand piled on top of the nest) was positive only under clear water conditions. Similarly, male size and nest entrance size were positively associated only in the absence of competition. Such interactions may, in turn, help to explain the persistence of variation in reproductive behaviours, which-due to their importance in offspring survival-are otherwise expected to be under strong balancing selection.

Colour biases in territorial aggression in a Neotropical cichlid fish.

Discrete colour morphs have provided important insights into the evolution of phenotypic diversity. One of the mechanisms that can help to explain coexistence of ecologically similar colour morphs and incipient species is (colour) biased aggression, which has the potential to promote continued existence of the morphs in a frequency-dependent manner. I addressed colour biases in territorial aggression in a field-based study on a Neotropical cichlid fish species, Amphilophus sagittae, which has two ecologically indistinguishable colour morphs that mate assortatively. I found that A. sagittae, in particular females, were more aggressive towards models of their own colour than those mimicking colours of the other morph. Such a behavioural pattern should result in a selection regime that benefits the rarer morph, and hence could help explain how novel, rare phenotypes may avoid competitive exclusion.

Mate sampling and choosiness in the sand goby.

To date, mate choice studies have mostly focused on establishing which mates are chosen or how the choices are performed. Here, we combined these two approaches by empirically testing how latency to mate is affected by various search costs, variation in mate quality and female quality in the sand goby (Pomatoschistus minutus). Our results show that females adjust their mating behaviour according to the costs and benefits of the choice situation. Specifically, they mated sooner when access to males was delayed and when the presence of other females presented a mate sampling cost. We also found a positive link between size variation among potential mating partners and spawning delay in some (but not all) experimental conditions. By contrast, we did not find the number of available males or the females' own body size ('quality') to affect mating latency. Finally, female mating behaviour varied significantly between years. These findings are notable for demonstrating that (i) mate sampling time is particularly sensitive to costs and, to a lesser degree, to variation among mate candidates, (ii) females' mating behaviour is sensitive to qualitative rather than to quantitative variation in their environment, and (iii) a snapshot view may describe mate sampling behaviour unreliably.

The color of artificial light affects mate attraction in the common glow-worm.

Artificial light at night, often referred to as 'light pollution', is a global environmental problem that threatens many nocturnal organisms. One such species is the European common glow-worm (Lampyris noctiluca), in which reproduction relies on the ability of sedentary bioluminescent females to attract flying males to mate. Previous studies show that broad-spectrum white artificial light interferes with mate attraction in this beetle. However, much less is known about wavelength-specific effects. In this study, we experimentally investigate how the peak wavelength (color) of artificial light affects glow-worm mate attraction success in the field by using dummy females that trap males landing to mate. Each dummy was illuminated from above by either a blue (peak wavelength: 452 nm), white (449 nm), yellow (575 nm), or red (625 nm) LED lighting, or light switched off in the control. We estimated mate attraction success as both the probability of attracting at least one male and the number of males attracted. In both cases, mate attraction success depended on the peak wavelength of the artificial light, with short wavelengths (blue and white) decreasing it more than long wavelengths (yellow and red). Hence, adjusting the spectrum of artificial light can be an effective measure for mitigating the negative effects of light pollution on glow-worm reproduction.

The role of cognition in nesting.

For many animals, nests are essential for reproductive success. Nesting individuals need to carry out a range of potentially challenging tasks, from selecting an appropriate site and choosing suitable materials to constructing the nest and defending it against competitors, parasites and predators. Given the high fitness stakes involved, and the diverse impacts both the abiotic and social environment can have on nesting success, we might expect cognition to facilitate nesting efforts. This should be especially true under variable environmental conditions, including those changing due to anthropogenic impacts. Here, we review, across a wide range of taxa, evidence linking cognition to nesting behaviours, including selection of nesting sites and materials, nest construction, and nest defence. We also discuss how different cognitive abilities may increase an individual's nesting success. Finally, we highlight how combining experimental and comparative research can uncover the links between cognitive abilities, nesting behaviours and the evolutionary pathways that may have led to the associations between them. In so doing, the review highlights current knowledge gaps and provides suggestions for future research. This article is part of the theme issue 'The evolutionary ecology of nests: a cross-taxon approach'.

Field-realistic acute exposure to glyphosate-based herbicide impairs fine-color discrimination in bumblebees.

Pollinator decline is a grave challenge worldwide. One of the main culprits for this decline is the widespread use of, and pollinators' chronic exposure to, agrochemicals. Here, we examined the effect of a field-realistic dose of the world's most commonly used pesticide, glyphosate-based herbicide (GBH), on bumblebee cognition. We experimentally tested bumblebee (Bombus terrestris) color and scent discrimination using acute GBH exposure, approximating a field-realistic dose from a day's foraging in a patch recently sprayed with GBH. In a 10-color discrimination experiment with five learning bouts, GBH treated bumblebees' learning rate fell to zero by third learning bout, whereas the control bees increased their performance in the last two bouts. In the memory test, the GBH treated bumblebees performed to near chance level, indicating that they had lost everything they had learned during the learning bouts, while the control bees were performing close to the level in their last learning bout. However, GBH did not affect bees' learning in a 2-color or 10-odor discrimination experiment, which suggests that the impact is limited to fine color learning and does not necessarily generalize to less specific tasks or other modalities. These results indicate that the widely used pesticide damages bumblebees' fine-color discrimination, which is essential to the pollinator's individual success and to colony fitness in complex foraging environments. Hence, our study suggests that acute sublethal exposure to GBH poses a greater threat to pollination-based ecosystem services than previously thought, and that tests for learning and memory should be integrated into pesticide risk assessment.

Prior associations affect bumblebees' generalization performance in a tool-selection task.

A small brain and short life allegedly limit cognitive abilities. Our view of invertebrate cognition may also be biased by the choice of experimental stimuli. Here, the stimuli (color) pairs used in the match-to-sample tasks affected the performance of buff-tailed bumblebees (Bombus terrestris). We trained the bees to roll a tool, a ball, to a goal that matched its color. Bees trained with a yellow-and-orange/red stimuli pair took more training bouts to reach our color-matching criterion than those trained with a blue-and-yellow stimuli pair. When assessing the bees' concept learning ability in a transfer test with a novel color, the bees trained with blue and yellow (novel color: orange/red) were highly successful, the bees trained with blue and orange/red (novel color: yellow) did not differ from random, and those trained with yellow and orange/red (novel color: blue) failed the test. These results highlight that stimulus salience can affect our conclusions on test subjects' cognitive ability. Therefore, we encourage paying attention to stimulus salience (among other factors) when assessing the cognition of invertebrates.

Both male and female identity influence variation in male signalling effort.

BACKGROUND: Male sexual displays play an important role in sexual selection by affecting reproductive success. However, for such displays to be useful for female mate choice, courtship should vary more among than within individual males. In this regard, a potentially important source of within male variation is adjustment of male courtship effort in response to female traits. Accordingly, we set out to dissect sources of variation in male courtship effort in a fish, the desert goby (Chlamydogobius eremius). We did so by designing an experiment that allowed simultaneous estimation of within and between male variation in courtship, while also assessing the importance of the males and females as sources of courtship variation. RESULTS: Although males adjusted their courtship depending on the identity of the female (a potentially important source of within-male variation), among-male differences were considerably greater. In addition, male courtship effort towards a pair of females was highly repeatable over a short time frame. CONCLUSION: Despite the plasticity in male courtship effort, courtship displays had the potential to reliably convey information about the male to mate-searching females. Our experiment therefore underscores the importance of addressing the different sources contributing to variation in the expression of sexually-selected traits.