Behavioural Ecology: Ethology and Sensory Ecology, Foraging, Mating Systems and Sexual Selection, and Social Behaviour

Tinbergen (1963) set out four questions to ask of any behaviour. Two are proximate, about how the behaviour works in the individual: its mechanism (the stimuli, nerves and hormones that cause it) and its development or ontogeny (how it arises through genes, experience and learning). Two are ultimate, about why it evolved: its function or adaptive value (how it increases fitness) and its phylogeny (its evolutionary history across related species). A bird sings in spring because lengthening days raise testosterone (mechanism), because it learnt its song as a nestling (development), because song holds a territory and attracts a mate (function), and because its ancestors sang (phylogeny) — four answers that do not compete.

Lorenz, Tinbergen and von Frisch shared the 1973 Nobel Prize for founding ethology. A fixed action pattern is a stereotyped, species-typical sequence that, once triggered by a sign stimulus (releaser), runs to completion: a greylag goose rolls an egg back into its nest and completes the movement even if the egg is removed mid-way. Male sticklebacks attack crude models with a red belly but ignore accurate models without one. Herring-gull chicks peck at the red spot on the parent’s bill, and peck even more at an exaggerated model — a supernormal stimulus. Lorenz showed filial imprinting: goslings follow the first moving object they see during a brief sensitive (critical) period after hatching.

Neuroethology studies the neural basis of natural behaviour. Echolocating bats emit ultrasonic calls and locate prey from the echoes; many noctuid moths have ears with just two sensory cells, tuned to bat calls, and respond to a distant bat by turning away and to a close one by erratic diving (Roeder’s work). The toad’s prey-catching response is released by a small elongated object moving along its long axis — a "worm" — and not by the same object moving across it. Behavioural endocrinology links hormones to behaviour: testosterone rises in many male birds during territorial establishment (the challenge hypothesis), and in ring doves courtship by the male triggers hormonal changes in the female that bring her into breeding condition.

Von Frisch decoded the honeybee waggle dance: on the vertical comb, the angle of the waggle run from vertical equals the angle of the food source from the sun’s azimuth, and the duration of the run increases with distance; a round dance signals food close to the hive. Signals are expected to be honest when they are costly or cannot be faked (an index such as the depth of a toad’s croak, limited by body size). Navigation ranges from piloting by landmarks, through compass orientation — a sun compass compensated by the internal clock, a star compass learnt from the rotation of the night sky around the pole star (Emlen’s indigo buntings in a planetarium), and a magnetic compass — to true navigation, which needs a map sense as well as a compass, as in homing pigeons displaced to unfamiliar sites.

Optimal foraging theory assumes that selection favours foragers that maximise their net rate of energy intake, and builds models with a currency, a decision and constraints. In the prey (diet) model, each prey type i has energy Eᵢ, handling time hᵢ and encounter rate λᵢ; its profitability is Eᵢ/hᵢ. Rank prey by profitability; a forager eating only the best prey gains at a long-term rate R₁ = λ₁E₁/(1 + λ₁h₁). The next prey should be added to the diet only if its profitability exceeds the rate obtainable without it. With E₁ = 10 J, h₁ = 2 s and λ₁ = 0.1 per s, R₁ = 1/1.2 = 0.83 J/s; a second prey with E₂ = 1 J and h₂ = 2 s has profitability 0.5 J/s < 0.83 and should be ignored however often it is met. Two predictions follow: whether a poor prey is eaten depends on the abundance of better prey, not on its own abundance; and inclusion is all-or-none.

Charnov’s marginal value theorem (1976) treats food in patches with diminishing returns: the longer a forager stays, the slower it gains. It predicts that a forager should leave a patch when its instantaneous rate of gain falls to the average rate for the habitat as a whole, travel included. Graphically, the optimal residence time is where a line from the start of travel time on the time axis touches the gain curve. The predictions: longer travel times between patches mean longer stays, and in a richer habitat (a higher average rate) patches are left sooner. Starlings carrying more leatherjackets per trip the farther they flew from the nest fit this. Risk-sensitive foraging adds variance: an animal that will starve without a high intake may prefer a variable option.

Space use: a home range is the area an animal normally uses; a territory is an area it defends. Brown’s principle of economic defendability says territoriality pays only when the benefit of exclusive access exceeds the cost of defence — so it is favoured at intermediate resource density, when resources are neither so scarce that they are not worth defending nor so abundant that intruders are overwhelming. Golden-winged sunbirds defend flower territories only when the nectar gained saves more foraging time than defence costs. When individuals move freely among patches of different quality, the ideal free distribution predicts that they distribute so that every individual gets the same intake: numbers are proportional to resource input, and 20 foragers at two patches supplied at 30 and 10 prey per minute should split 15 and 5.

Anisogamy — large, costly eggs and small, cheap sperm — underlies sexual differences. Bateman’s principle: male reproductive success usually varies more than female success and rises more steeply with the number of mates, because a female’s output is limited by egg production. Trivers’ parental investment theory generalises this: the sex that invests more in each offspring becomes the limiting resource and is choosy, while the other sex competes for access. The operational sex ratio, the ratio of sexually receptive males to females, predicts the intensity of competition; where males invest more, as in pipefish and seahorses or in jacanas, the roles reverse and females compete.

Darwin distinguished intrasexual selection — competition within one sex for mates, which favours weapons such as antlers and large body size — from intersexual selection, choice of mates by the other sex, which favours ornaments. Why choose ornaments? Fisher’s runaway process: a genetic correlation between the preference and the trait makes each reinforce the other until natural selection halts it. Good genes (indicator) models: ornaments reveal heritable quality — Hamilton and Zuk proposed that bright plumage shows resistance to parasites. Zahavi’s handicap principle (1975): an ornament is reliable because it is costly, so only high-quality males can afford it. Sensory bias: a preference that existed before the trait, as in water mites and swordtails, is exploited by males. Sexual conflict arises when the sexes’ optima differ: seminal fluid proteins of male Drosophila raise the female’s egg-laying and reduce her remating at a cost to her lifespan, and bedbug males pierce the female’s body wall (traumatic insemination). Sperm competition favours large testes, mate guarding and copulatory plugs.

Parental care evolves when its benefit to offspring survival outweighs the cost to the parent’s future reproduction. Uniparental female care is the rule in mammals (lactation), biparental care in birds, and male-only care is common in fish with external fertilisation. Explanations include certainty of paternity (higher with external fertilisation) and the order of gamete release: with internal fertilisation the male can leave first, whereas with external fertilisation the female often releases eggs first and the male, left with the fertilised eggs, guards them. Trivers also predicted parent–offspring conflict: an offspring is related to itself by 1 but to a full sibling by 0.5, so it is selected to demand more care than the parent is selected to give, as seen in weaning conflict.

• Benefits of groups: dilution (in a group of n, each individual’s chance of being the one taken in an attack is 1/n); the many-eyes effect (with n members each scanning independently with probability v, the chance that at least one is vigilant is 1 − (1 − v)^n, so each can scan less); Hamilton’s selfish herd (each individual reduces its own domain of danger by moving towards others); group hunting and information about food.
• Costs of groups: competition for food and mates, faster spread of parasites and disease, greater conspicuousness to predators, and interference. Because joining pays as long as the joiner does better than alone, groups tend to grow beyond the size that is optimal for their members.
• Intraspecific competition is scramble when resources are shared out so that every individual gets less as density rises (larval blowflies in a carcass) and contest when some individuals win whole shares and others get nothing (territories, dominance hierarchies); contest competition regulates populations more stably.

When the best action depends on what others do, behaviour is analysed with game theory. Maynard Smith and Price defined an evolutionarily stable strategy (ESS): a strategy that, once adopted by most of a population, cannot be invaded by any rare alternative. In the hawk–dove game individuals contest a resource of value V; hawks escalate and risk an injury costing C, doves display and retreat if attacked.

If V ≥ C, pure hawk is the ESS: winning is worth the risk of injury. If V < C, neither pure strategy is stable — a population of doves is invaded by hawks (who win V against doves), and a population of hawks by doves (who get 0 rather than the negative (V − C)/2). The ESS is a mix in which hawks and doves do equally well: with a proportion p of hawks, p(V − C)/2 + (1 − p)V = (1 − p)V/2, which gives p* = V/C. With V = 4 and C = 10, p* = 0.4; at that mix the payoff to either strategy is 0.4 × (−3) + 0.6 × 4 = 1.2 for hawks and 0.6 × 2 = 1.2 for doves. The mean payoff, 1.2, is below the 2 that an all-dove population would enjoy — the ESS is stable, not optimal for the group. The bourgeois strategy ("hawk if owner, dove if intruder") is an ESS that settles contests by an arbitrary asymmetry.

An altruistic act lowers the actor’s own reproduction and raises another’s. Hamilton (1964) showed how it can evolve: a gene for altruism spreads if rB > C, where C is the cost to the actor, B the benefit to the recipient (both in offspring) and r the coefficient of relatedness, the probability that a gene in the actor is present in the recipient by common descent. Inclusive fitness counts an individual’s own reproduction plus its effects on relatives weighted by r. Worked example: an act costing the actor 2 offspring is favoured towards a half-sibling (r = 0.25) only if B > C/r = 8 offspring, but towards a full sibling (r = 0.5) whenever B > 4. Kin selection is the selection that results; Belding’s ground squirrels give alarm calls more when close female kin are nearby, and helpers at the nest in many birds are often the breeders’ earlier offspring.

In the Hymenoptera males are haploid, so full sisters share all their father’s genes and half their mother’s: r = 0.5 × 1 + 0.5 × 0.5 = 0.75, higher than the 0.5 to their own offspring. Hamilton suggested this favours workers raising sisters — the haplodiploidy hypothesis for eusociality — though multiple mating by queens lowers r, eusociality also occurs in diploid termites and naked mole-rats, and ecological factors are now thought equally important. Altruism between non-relatives needs another route: reciprocal altruism (Trivers, 1971), in which help is returned later, requires repeated interactions and the ability to recognise and punish cheats, as in vampire bats that regurgitate blood to roost-mates that fed them before. In the iterated prisoner’s dilemma, tit-for-tat — cooperate first, then copy the partner’s last move — is a robust cooperative strategy.