The confusion effect from neural networks to reduced predation risk

The confusion effect is often cited as an antipredatory benefitof group living and has been demonstrated by numerous studiesacross a range of taxa. However, there have been relativelyfew studies examining the mechanisms behind the effect and noexperimental test of its supposed theoretical basis (informationdegradation in neural networks) using a natural predator–preypairing. In agreement with other studies, we demonstrate thatattack success of the three-spined stickleback (Gasterosteusaculeatus L.) is reduced by an increase in Daphnia magna groupsize. Neural network models attempt to explain this trend withmultiple prey inducing poor neural mapping of target prey, thusleading to an increase in the spatial error of each attack.We explicitly tested this prediction and demonstrate that thedecrease in attack success by sticklebacks does correspond toan increase in spatial targeting error with larger prey groupsize. Finally, we show that the number of targets, rather thanthe density or area occupied by the group, has the greatesteffect on reducing the rate of attack. These results are discussedin the context of the information processing constraints ofpredators, the ultimate cause of the confusion effect.     

Three‐spined sticklebacks Gasterosteus aculeatus as a model for exploring behavioural biology

Niko Tinbergen chose the three‐spined stickleback Gasterosteus aculeatus for his classic behavioural studies because they are small, robust, common and easy to house in the laboratory under reasonably natural conditions and also because their behaviour, while sufficiently simple to be tractable, is still sufficiently complex to be interesting. An analysis of citation records shows that this was an inspired choice. Research on these small fish has addressed all four of Tinbergen's famous questions (causation, development, functions and evolution) and has contributed to the understanding of many different behavioural systems. The G. aculeatus literature is used here to explore several themes in fundamental behavioural biology (diet choice, shoaling, behavioural syndromes and sexual signalling) and the extent to which research using G. aculeatus has informed both fundamental and applied behavioural biology, the latter in the context of aquaculture research.     

Brain development and predation: plastic responses depend on evolutionary history

Although the brain is known to be a very plastic organ, the effects of common ecological interactions like predation or competition on brain development have remained largely unexplored. We reared nine-spined sticklebacks (Pungitius pungitius) from two coastal marine (predation-adapted) and two isolated pond (competition-adapted) populations in a factorial experiment, manipulating perceived predatory risk and food supply to see (i) if the treatments affected brain development and (ii) if there was population differentiation in the response to treatments. We detected differences in plasticity of the bulbus olfactorius (chemosensory centre) between habitats: marine fish were not plastic, whereas pond fish had larger bulbi olfactorii in the presence of perceived predation. Marine fish had larger bulbus olfactorius overall. Irrespective of population origin, the hypothalamus was smaller in the presence of perceived predatory risk. Our results demonstrate that perceived predation risk can influence brain development, and that the effect of an environmental factor on brain development may depend on the evolutionary history of a given population in respect to this environmental factor.     

Female mate preferences for male body size and shape promote sexual isolation in threespine sticklebacks

Female mate preferences for ecologically relevant traits may enhance natural selection, leading to rapid divergence. They may also forge a link between mate choice within species and sexual isolation between species. Here, we examine female mate preference for two ecologically important traits: body size and body shape. We measured female preferences within and between species of benthic, limnetic, and anadromous threespine sticklebacks (Gasterosteus aculeatus species complex). We found that mate preferences differed between species and between contexts (i.e., within vs. between species). Within species, anadromous females preferred males that were deep bodied for their size, benthic females preferred larger males (as measured by centroid size), and limnetic females preferred males that were more limnetic shaped. In heterospecific mating trials between benthics and limnetics, limnetic females continued to prefer males that were more limnetic like in shape when presented with benthic males. Benthic females showed no preferences for size when presented with limnetic males. These results show that females use ecologically relevant traits to select mates in all three species and that female preference has diverged between species. These results suggest that sexual selection may act in concert with natural selection on stickleback size and shape. Further, our results suggest that female preferences may track adaptation to local environments and contribute to sexual isolation between benthic and limnetic sticklebacks.     

Climate change alters the reproductive phenology and investment of a lacustrine fish,the three‐spine stickleback

High‐latitude lakes are particularly sensitive to the effects of global climate change, demonstrating earlier ice breakup, longer ice‐free seasons, and increased water temperatures. Such physical changes have implications for diverse life‐history traits in taxa across entire lake food webs. Here, we use a five‐decade time series from an Alaskan lake to explore effects of climate change on growth and reproduction of a widely distributed lacustrine fish, the three‐spine stickleback (Gasterosteus aculeatus). We used multivariate autoregressive state‐space (MARSS) models to describe trends in the mean length for multiple size classes and to explore the influence of physical (date of ice breakup, surface water temperature) and biological (density of con‐ and heterospecifics) factors. As predicted, mean size of age 1 and older fish at the end of the growing season increased across years with earlier ice breakup and warmer temperatures. In contrast, mean size of age 0 fish decreased over time. Overall, lower fish density and warmer water temperatures were associated with larger size for all cohorts. Earlier ice breakup was associated with larger size for age 1 and older fish but, paradoxically, with smaller size of age 0 fish. To explore this latter result, we used mixing models on age 0 size distributions, which revealed an additional cohort in years with early ice breakup, lowering the mean size of age 0 fish. Moreover, early ice breakup was associated with earlier breeding, evidenced by earlier capture of age 0 fish. Our results suggest that early ice breakup altered both timing and frequency of breeding; three‐spine stickleback spawned earlier and more often in response to earlier ice breakup date. While previous studies have shown the influence of changing conditions in northern lakes on breeding timing and growth, this is the first to document increased breeding frequency, highlighting another pathway by which climate change can alter the ecology of northern lakes.     

Deviation from the line of least resistance does not exclude genetic constraints: a comment on Berner et al. (2010)

Berner et al. (2010) found that freshwater adaptation of three-spined sticklebacks had not followed the direction of maximal evolvability. Based on this, they suggested that ancestral variance structure has not appreciably biased adaptive diversification. We reanalyze their data to show that evolution has happened in directions of much larger than average evolvability, and we conclude that their data are consistent with an influence of ancestral variational constraints.     

Schistocephalus infestation improves prey-size selection by three-spined sticklebacks, Gasterosteus aculeatus

Schistocephalus -infected sticklebacks ate slightly less but fed more selectively on larger prey than non-infested fish. It follows that, in the short-term, the net energy gain in foraging is larger for infested fish. This matches the expectation that infested sticklebacks compensate energy losses due to Schistocephalus.     

The Darwinian stickleback Gasterosteus aculeatus: a history of evolutionary studies*

The history of studies on the taxonomy and evolutionary biology of the three‐spined stickleback Gasterosteus aculeatus from the 18th century to the present is reviewed. After the publication of Darwin's Origin of the Species, four important dates, 1925, 1947, 1967 and 2001, are identified as marking major gains in the understanding of the evolution of the diversity in morphological, life‐history, physiological and behavioural traits that characterizes G. aculeatus. The period 1925–1970 led to the identification of the main themes of research: status and adaptive significance of lateral‐plate morphs; inter and intrapopulation trait variation in freshwater resident G. aculeatus and the adaptive significance of the variation. Between 1970 and 2001, these themes were investigated using variation observed particularly along the Pacific coast of the U.S.A. and Canada, notably in the Cook Inlet region of Alaska and the Haida Gwaii Archipelago. Studies on adaptive radiation and reproductive isolation in lacustrine, ecomorph pairs (limnetics and benthics) discovered in the Strait of Georgia region have been particularly productive. From 2001, the application of genomic studies to these problems began to open up the study of the relationships between genotype, phenotype and selective advantage to causal analysis.     

Rapid bioconcentration of steroids in the plasma of three-spined stickleback Gasterosteus aculeatus exposed to waterborne testosterone and 17β-oestradiol

The relationship over time between the concentrations of two steroids, singly and in combination, in a static exposure system and in the blood of three-spined stickleback Gasterosteus aculeatus , held within the exposure system was investigated. Groups of three-spined stickleback were exposed (nominally) to either 1000 ng l⁻¹ 17β-oestradiol (E2), testosterone (T) or E2 and T in combination at the same concentrations for 6 days. Both water and fish were sampled at intervals and steroid concentrations in both compartments were determined. The plasma steroid time profile revealed a rapid bioconcentration within the first 6 h of exposure. The plasma steroid levels attained at this time point (20–90 ng ml⁻¹) were up to 50-fold (E2) and 200-fold (T) greater than the actual levels of steroid measured in the exposure water, while levels in the blood of control fish did not exceed 4 ng ml⁻¹. The substantial elevation of plasma steroid levels relative to the concentrations of steroid to which the fish were exposed in the ambient water gives scope for delivery of the steroids to target endocrine tissues at levels far in excess of what might be predicted on the basis of passive branchial uptake alone. These results are discussed in relation to endocrine disruption, and in particular the occurrence of effects in fish exposed to levels of endocrine active substances that are seemingly physiologically irrelevant.