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.     

Tribute to Tinbergen: Putting Niko Tinbergen's ‘Four Questions’ in Historical Context

Niko Tinbergen's (Zeit. Tier. 20, 1963, 410) paper ‘On aims and methods of ethology’ is appropriately remembered as the paper in which Tinbergen characterized ethology as ‘the biological study of behavior’ and went on to explain that to study behavior biologically is to ask four distinct questions about it: (1) How is it caused physiologically? (2) What is its survival value? (3) How has it evolved? and (4) How does it develop in the individual? Here, we consider Tinbergen's paper in its historical context by looking at it from three different perspectives: (1) a comparison of Tinbergen's formulation of ‘ethology's four questions’ with similar, but different formulations of biology's basic problems offered by Julian Huxley, Konrad Lorenz, and Ernst Mayr; (2) a survey of the roles that the four questions played in Tinbergen's own work over the course of his career; and (3) a consideration of the two explicit goals of Tinbergen's (Zeit. Tier., 20, 1963, 410) paper, namely (a.) to honor Tinbergen's friend and colleague Konrad Lorenz (as part of a Festschrift for Lorenz on the occasion of his sixtieth birthday) and (b.) to provide a sketch of ethology's scope and an evaluation of the ways the field needed to develop in the future. We suggest that just as the work of Tinbergen's Oxford research team revealed how the behavior of gulls reflected compromises worked out in the face of the diverse selective pressures of particular environments, we can identify certain conflicts that arose for Tinbergen in trying to write something that his friend Lorenz would like while also assessing ethology's current state and future prospects. That said, however, Tinbergen's enduring concern was to do all he could to ensure that ethology thrive as a field and develop a scientific understanding of animal (and human) behavior. For this to happen, he insisted, the four questions of ethology needed to be pursued in a balanced, comprehensive, and integrated fashion.     

Tribute to Tinbergen: Questions and How to Answer Them

Despite the major advances that have occurred in the study of animal behaviour in the 50 years since the publication of Tinbergen's (ZeitschriftfürTierpsychologie, 20, 1963, 410) ‘Aims and Methods’ paper, the framework he outlined still remains the best way we have of guiding and organizing behavioural research. His distinction between four different types of question – adaptation, phylogeny, immediate causal mechanism and development – and his insistence on being clear on what would count as answers to each of them are still as good an introduction to the subject today as they ever were.     

Behavioural effects of temperature on ectothermic animals: unifying thermal physiology and behavioural plasticity

Temperature imposes significant constraints on ectothermic animals, and these organisms have evolved numerous adaptations to respond to these constraints. While the impacts of temperature on the physiology of ectotherms have been extensively studied, there are currently no frameworks available that outline the multiple and often simultaneous pathways by which temperature can affect behaviour. Drawing from the literature on insects, we propose a unified framework that should apply to all ectothermic animals, generalizing temperature's behavioural effects into: (1) kinetic effects, resulting from temperature's bottom‐up constraining influence on metabolism and neurophysiology over a range of timescales (from short to long term), and (2) integrated effects, where the top‐down integration of thermal information intentionally initiates or modifies a behaviour (behavioural thermoregulation, thermal orientation, thermosensory behavioural adjustments). We discuss the difficulty in distinguishing adaptive behavioural changes from constraints when observing animals' behavioural responses to temperature. We then propose two complementary approaches to distinguish adaptations from constraints, and categorize behaviours according to our framework: (i) ‘kinetic null modelling’ of temperature's effects on behaviour; and (ii) behavioural ecology experiments using temperature‐insensitive mutants. Our framework should help to guide future research on the complex relationship between temperature and behaviour in ectothermic animals.     

Four errors and a fallacy: pitfalls for the unwary in comparative brain analyses

Comparative analyses are the backbone of evolutionary analysis. However, their record in producing a consensus has not always been good. This is especially true of attempts to understand the factors responsible for the evolution of large brains, which have been embroiled in an increasingly polarised debate over the past three decades. We argue that most of these disputes arise from a number of conceptual errors and associated logical fallacies that are the result of a failure to adopt a biological systems-based approach to hypothesis-testing. We identify four principal classes of error: a failure to heed Tinbergen's Four Questions when testing biological hypotheses, misapplying Dobzhansky's Dictum when testing hypotheses of evolutionary adaptation, poorly chosen behavioural proxies for underlying hypotheses, and the use of inappropriate statistical methods. In the interests of progress, we urge a more careful and considered approach to comparative analyses, and the adoption of a broader, rather than a narrower, taxonomic perspective.     

An experimental test of the Jennings hypothesis of behavioural organization

An experimental test of H. S. Jennings’ principle of “selection of overproduced movements” was conducted using a jellyfish (Sarsia tubulosa M. Sars) as the experimental animal. The hypothesis was that behavioural repertoire and diversity (measured as Brillouin's H) would be higher under unfavourable environmental conditions. The results showed no difference in behavioural repertoire and reduced behavioural diversity under unfavourable environmental conditions. The reduction in behavioural diversity was due to lower behavioural evenness under experimental conditions.     

Alternative risk-taking styles: The case of time-budgeting strategies of terrestrial gastropods

The terrestrial slugs Arion ater, Limax maximus and Ariolimax columbianus have similar morphological designs but differ remarkably in their life history tactics and behavioural time budgets. The adaptive value of particular risk-taking styles was investigated using a comprehensive computer simulation model. The model allowed each species' success (growth rates, food acquisition) and costs (distance travelled, hydration deficits, injury from aggressive encounters) to be evaluated in various types of weather (benign, harsh and surprise). This was interpreted in terms of the species' life history design. In addition, each species was simulated with the behavioural strategy of the other two species substituted for its natural programming. The simulation experiments demonstrated how variations in a few simple rules could lead to divergent cost-benefit consequences. The model also illustrated that coarsely-tuned sensitivity to the environment may be better than finely-tuned responses, depending on the animal's ability to respond quickly and the degree of risk. The simulations suggested that competition has shaped the time-budgeting tactics of A. ater and L. maximus. Each species actually performed better in harsh weather, using the behavioural program of the other. L. maximus is an aggressive species with a narrow, nocturnal activity period. The concentrated activity of L. maximus may allow it to displace competitors more effectively, whereas the broader time span of A. ater's activity may be necessary to avoid L. maximus.     

Tinbergen on mirror neurons

Fifty years ago, Niko Tinbergen defined the scope of behavioural biology with his four problems: causation, ontogeny, survival value and evolution. About 20 years ago, there was another highly significant development in behavioural biology—the discovery of mirror neurons (MNs). Here, I use Tinbergen''s original four problems (rather than the list that appears in textbooks) to highlight the differences between two prominent accounts of MNs, the genetic and associative accounts; to suggest that the latter provides the defeasible ‘best explanation’ for current data on the causation and ontogeny of MNs; and to argue that functional analysis, of the kind that Tinbergen identified somewhat misleadingly with studies of ‘survival value’, should be a high priority for future research. In this kind of functional analysis, system-level theories would assign MNs a small, but potentially important, role in the achievement of action understanding—or another social cognitive function—by a production line of interacting component processes. These theories would be tested by experimental intervention in human and non-human animal samples with carefully documented and controlled developmental histories.     

Plasticity of the phonotactic selectiveness of four species of chirping crickets (Gryllidae): Implications for call recognition

Earlier studies of phonotaxis by female crickets describe this selective behavioural response as being important in the females' choices of conspecific males, leading to reproduction. In the present study, moderate (30+) to very large data sets of phonotactic behaviour by female Acheta domesticus L., Gryllus bimaculatus DeGeer, Gryllus pennsylvanicus Burmeister and Gryllus veletis Alexander demonstrate substantially greater plasticity in the behavioural choices, as made by females of each species, for the syllable periods (SP) of model calling songs (CS) than has been previously described. Phonotactic choices by each species range from the very selective (i.e. responding to only one or two SPs) to very unselective (i.e. responding to all SPs presented). Some females that do not respond to all SPs prefer a range that includes either the longest or shortest SP tested, which fall outside the range of SPs produced by conspecific males. Old female A. domesticus and G. pennsylvanicus are more likely to be unselective for SPs than are young females. Each species includes females that do not respond to a particular SP when responding to CSs with longer and shorter SPs. The results suggest that the plasticity of phonotactic behaviour collectively exhibited by the females of each species does not ensure that choices of a male's CS effectively focus the female's phonotactic responses on CSs that represent the conspecific male. The phonotactic behaviour collectively exhibited by females of each species does not readily fit any of the models for selective processing by central auditory neurones that have been proposed to underlie phonotactic choice.     

Aggressiveness,Boldness and Parental Food Provisioning in Male House Wrens (Troglodytes aedon)

Behavioural syndromes have been identified in a large number of species, yet our understanding of them in an ecological context remains poor. Specifically, there are few data that relate behavioural syndromes to other biologically important behaviours and, ultimately, to reproductive success. In this field study, we examined the aggressiveness and boldness of free‐living male house wrens (Troglodytes aedon) and found a statistically significant positive relationship between these two behaviours (i.e. a behavioural syndrome). When we examined the two axes of this behavioural syndrome in relation to the male's share of provisioning, we found a negative relation between a male's aggressiveness and his provisioning rate, but no relationship between male boldness and provisioning behaviour. These differences in provisioning behaviour among males with different levels of aggression may reflect differences in reproductive strategies or different life‐history trade‐offs among males. Moreover, these results indicate that while some behavioural traits may be correlated, this does not mean that traits that compose the behavioural syndrome cannot evolve independently of one another.     

NOTES ON THE NESTING OF THE WHITE-FRONTED SANDPLOVER,Charadrius marginatus,AT GAMTOOS RIVER MOUTH IN 1950

Young, H.G. 1999. Comparative study of the courtship displays of Meller's Duck Anus melleri, Yellowbilled Duck A. undulata and Northern Mallard A. platyrhynchos. Ostrich 70(2): 117–122

The little-known Meller's Duck Anas melleri is a monochromatic species endemic to Madagascar that has been linked to the Northern Mallard A. platyrhynchos, or the African Yellowbilled Duck A. undulata. This study compared group courtship between these species, and analysed the structure and duration of the main display components, the grunt-whistle, head-up-tail-up and down-up. Meller's Duck differed significantly from the other species, and lacked a down-up display. Meller's Duck shows some behavioural similarities to the African Black Duck A. sparsa.     

On the Utility of the Proximate-Ultimate Distinction in the Study of Animal Behavior

The importance of Tinbergen's “four problems” approach lies in assuring that the answers provided are truly appropriate to the questions that are asked. No problem is any more important than any other. I suggest that the spirit of this formulation can be best realized if we revise the ways in which recent authors have grouped the various problems in the study of behavior. One consequence of this regrouping is an elimination of the proximate-ultimate dichotomy.     

Signs of a vector's adaptive choice: on the evasion of infectious hosts and parasite‐induced mortality

Laboratory and field experiments have demonstrated in many cases that malaria vectors do not feed randomly, but show important preferences either for infected or non‐infected hosts. These preferences are likely in part shaped by the costs imposed by the parasites on both their vertebrate and dipteran hosts. However, the effect of changes in vector behaviour on actual parasite transmission remains a debated issue. We used the natural associations between a malaria‐like parasite Polychromophilus murinus, the bat fly Nycteribia kolenatii and a vertebrate host the Daubenton's bat Myotis daubentonii to test the vector's feeding preference based on the host's infection status using two different approaches: 1) controlled behavioural assays in the laboratory where bat flies could choose between a pair of hosts; 2) natural bat fly abundance data from wild‐caught bats, serving as an approximation of realised feeding preference of the bat flies. Hosts with the fewest infectious stages of the parasite were most attractive to the bat flies that did switch in the behavioural assay. In line with the hypothesis of costs imposed by parasites on their vectors, bat flies carrying parasites had higher mortality. However, in wild populations, bat flies were found feeding more based on the bat's body condition, rather than its infection level. Though the absolute frequency of host switches performed by the bat flies during the assays was low, in the context of potential parasite transmission they were extremely high. The decreased survival of infected bat flies suggests that the preference for less infected hosts is an adaptive trait. Nonetheless, other ecological processes ultimately determine the vector's biting rate and thus transmission. Inherent vector preferences therefore play only a marginal role in parasite transmission in the field. The ecological processes rather than preferences per se need to be identified for successful epidemiological predictions.     

“New Canadians are new conservatives”: race,incorporation and achieving electoral success in multicultural Canada

Despite declarations of race's irrelevance, the Conservative Party of Canada's (CPC) stance on race-related policies under former Prime Minister Stephen Harper's leadership was key to every electoral campaign it fought. Moreover, it is not despite but because of their race that racialized political elites have been incorporated into the CPC and its antecedents. Indeed, beginning in the 1990s, the inclusion of Asian Members of Parliament (MP) became for the Reform Party of Canada, a weapon in the struggle for electoral success; that is, part of an era of Conservative racial realignment. By tracing the role of Asian Conservative MP in the rise of the Reform Party since its 1987 inception and the electoral success of the CPC (2006–2015), this article explores how racialized political elites become crucial to the legitimization of the racial state when it is through a discourse of inclusion that exclusion is crafted.     

Barlow's Lark: a new species in the Karoo Lark Certhilauda albescens complex of southwest Africa

The Karoo Lark Certhilauda albescens complex, endemic to southwest Africa, is characterized by regional phenotypic variation. Recent consensus has been to recognize two species, Dune Lark Certhilauda erythrochlamys and Karoo Lark Certhilauda albescens, but intermediate forms around the mouth of the Orange River have resulted in some authors treating it as a single polytypic species complex. We reexamined the status of taxa in this group by sequencing a segment of the mitochondrial DNA cytochrome b gene. Most samples were from the area around the mouth of the Orange River, where there is considerable local phenotypic variation. Our results indicate that the complex comprises three species, Karoo Lark, Dune Lark and Barlow's Lark Certhilauda barlowi, separated by 1.9-5.5% sequence divergence. There were no sequence differences among described subspecies, but there was limited variation among Dune Lark individuals (sequence divergence values 0.2-0.4%). The Red Lark Certhilauda burra is closely related to the Karoo Lark complex; indeed, it may be that Karoo Lark is the ancestral form. There was morphological (biometrics and plumage) and behavioural (male display song structure) support for the recognition of Barlow's Lark as a separate species. Species ranges within the complex are allopatric or narrowly parapatric, and they occur in different habitats and climatic conditions. Discriminant function analysis correctly identified 99% of skins assigned to taxa based on range, but a few individuals collected in the contact zone between Karoo and Barlow's Larks exhibited intermediate phenotypes, and further investigations are warranted to search for evidence of hybridization. The newly recognized Barlow's Lark has a maximum range of 18,000 km². It appears to have disappeared from heavily grazed farms around Aus, southern Namibia, and occurs almost exclusively in diamond mining areas, where domestic livestock are excluded. Changes to land use practices which reduce vegetation cover could seriously impact this species.     

Interaction between sexes and between different circadian phenotypes affects lifespan in the fruit fly Drosophila melanogaster

Circadian clocks regulate the daily temporal structure of physiological and behavioural functions. In the fruit fly Drosophila melanogaster Meigen, disruption of daily rhythms is suggested to reduce the fly's lifespan. In the present study, because pairs of mixed‐sex flies are known to show an activity pattern different from that of individual flies, this hypothesis is tested by measuring the lifespan of flies housed same‐sexually or mixed‐sexually under an LD 12 : 12 h photocycle at a constant temperature of 25 °C. The effect of housing wild‐type (Canton‐S) flies with period (per) circadian clock mutant flies is also examined because the mutant flies have different daily activity patterns. When males and females of wild‐type flies are housed together, their lifespan is substantially lengthened (males) or shortened (females) compared with same‐sex housed flies. The shortening of the lifespan in females is significantly enhanced when mated with per mutant males. The shortening effects are significantly reduced when the mixed‐sex interaction is limited for the first 5 days after emergence. A slight elongation in lifespan, rather than a reduction, occurs when wild‐type females are housed same‐sexually with per⁰ or per^L mutant flies. In male flies, the elongation of lifespan occurs not only when wild‐type males are housed with wild‐type, per⁰ or per^L females, but also when housed with per⁰ or per^S mutant males. Mixed‐sex couples always show altered daily locomotor rhythms with an enhanced night‐time activity, whereas same‐sex couples show daily behavioural profiles slightly altered but essentially similar to a sum of the respective two flies. No significant correlation is found between the lifespan and reproductive capacity. These results suggest that the alteration of daily activity rhythms and sexual interaction may have significant impact on the fly's lifespan.     

Predator naïve minnows respond to their conspecific alarm substance but not the odour from a non-native predator

When exposed to predator cues, ostariophysan fishes exhibit short-term anti-predator behavioural responses in order to minimise predation risk. Non-native predator cues are, however, likely to elicit poor behavioural responses in native prey fishes. This study investigated whether chubbyhead barb Enteromius anoplus, a native freshwater minnow in South Africa, had the innate ability to recognise and respond to largemouth bass Micropterus salmoides, a non-native piscivore. This was experimentally evaluated by investigating behavioural responses to both the non-native predator's odour and damage-released conspecific alarm substance (CAS). Chubbyhead barbs did not exhibit any behavioural response to largemouth bass odour both before and after exposure to CAS. This suggests that the chubbyhead barbs likely lacked the innate ability to recognise the non-native largemouth bass predator kairomones. By comparison, exposure to CAS was associated with significant behavioural responses, with chubbyhead barbs shifting from free-swimming to hovering, and frequent use of refugia. This suggests that despite ineffective response to non-native largemouth bass odour, chubbyhead barbs responded to general predator attack. Overall, this study suggests the potential for non-native largemouth bass to induce negative consumptive effects on chubbyhead barbs due to their inability to identify non-native predator's odour. In addition, nonconsumptive effects are likely due to altered activities in response to predator attack.     

Masterpiece of epigenetic engineering – how Toxoplasma gondii reprogrammes host brains to change fear to sexual attraction

The protozoan parasite Toxoplasma gondii is known to induce specific behavioural changes in its intermediate hosts, including humans, that are believed to increase the chance of its successful transmission to the definitive host, the cat. The most conspicuous change is the so‐called fatal attraction phenomenon, the switch from the mice's and rats’ natural fear of the smell of cats toward an attraction to this smell. The mechanism of this manipulation activity is unknown; however, many indices suggest that changes in the concentrations of dopamine and testosterone are involved. In this issue of Molecular Ecology, Hari Dass & Vyas ( 2014 ) present results of a study showing that, by hypomethylation of certain regulatory elements of key gene, Toxoplasma is able to reprogramme the brain's genetic machinery in such a way that cat odour activates and changes the wiring of the medial amygdala circuits responsible for sexual behaviour. This study delivers the first clear evidence of a parasite's ability to use sophisticated epigenetic engineering techniques for the manipulation of the phenotype of its infected host.     

Searching by Adalia bipunctata (L.) (Coleoptera: Coccinellidae) and escape behaviour of its aphid and cicadellid prey on lime (Tilia×vulgaris Hayne)

• 1 The paper describes the behavioural interactions between searching larvae of Adalia bipunctata and its aphid and cicadellid prey on lime (Tilia×vulgaris Hayne).
• 2 The frequency with which the predator achieves contact with cicadellid nymphs of differing ages is related to direction of predator approach and predator perception by the cicadellid.
• 3 The success of a coccinellid in contacting and capturing its aphid prey is related to the predator's size and direction of approach, the perception of the predator by an aphid and the latter's ability to escape, the effectiveness of which is discussed.