Evolution of behavioural control from chordates to primates

This article outlines a hypothetical sequence of evolutionary innovations, along the lineage that produced humans, which extended behavioural control from simple feedback loops to sophisticated control of diverse species-typical actions. I begin with basic feedback mechanisms of ancient mobile animals and follow the major niche transitions from aquatic to terrestrial life, the retreat into nocturnality in early mammals, the transition to arboreal life and the return to diurnality. Along the way, I propose a sequence of elaboration and diversification of the behavioural repertoire and associated neuroanatomical substrates. This includes midbrain control of approach versus escape actions, telencephalic control of local versus long-range foraging, detection of affordances by the dorsal pallium, diversified control of nocturnal foraging in the mammalian neocortex and expansion of primate frontal, temporal and parietal cortex to support a wide variety of primate-specific behavioural strategies. The result is a proposed functional architecture consisting of parallel control systems, each dedicated to specifying the affordances for guiding particular species-typical actions, which compete against each other through a hierarchy of selection mechanisms. This article is part of the theme issue ‘Systems neuroscience through the lens of evolutionary theory’.

Habitat selection by vulnerable golden bandicoots in the arid zone

In 2010, vulnerable golden bandicoots (Isoodon auratus) were translocated from Barrow Island, Western Australia, to a predator-free enclosure on the Matuwa Indigenous Protected Area. Golden bandicoots were once widespread throughout a variety of arid and semi-arid habitats of central and northern Australia. Like many small to medium-sized marsupials, the species has severely declined since colonisation and has been reduced to only four remnant natural populations. Between 2010 and 2020 the reintroduced population of golden bandicoots on Matuwa was monitored via capture-mark-recapture data collection which was used in spatially explicit capture-recapture analysis to monitor their abundance over time. In 2014, we used VHF transmitters to examine the home range and habitat selection of 20 golden bandicoots in the enclosure over a six-week period. We used compositional analysis to compare the use of four habitat types. Golden bandicoot abundance in the enclosure slowly increased between 2010 and 2014 and has since plateaued at approximately one quarter of the density observed in the founding population on Barrow Island. The population may have plateaued because some bandicoots escape through the fence. Golden bandicoots used habitats dominated by scattered shrubland over spinifex grass more than expected given the habitat’s availability. Nocturnal foraging range was influenced by sex and trapping location, whereas diurnal refuge habitat was consistent across sex and trapping location. Our work suggests that diurnal refuge habitat may be an important factor for the success of proposed translocations of golden bandicoots.

Lightscapes of fear: How mesopredators balance starvation and predation in the open ocean

Like landscapes of fear, animals are hypothesized to strategically use lightscapes based on intrinsic motivations. However, longitudinal evidence of state-dependent risk aversion has been difficult to obtain in wild animals. Using high-resolution biologgers, we continuously measured body condition, time partitioning, three-dimensional movement, and risk exposure of 71 elephant seals throughout their 7-month foraging migrations (N = 16,000 seal days). As body condition improved from 21 to 32% fat and daylength declined from 16 to 10 hours, seals rested progressively earlier with respect to sunrise, sacrificing valuable nocturnal foraging hours to rest in the safety of darkness. Seals in superior body condition prioritized safety over energy conservation by resting >100 meters deeper where it was 300× darker. Together, these results provide empirical evidence that marine mammals actively use the three-dimensional lightscape to optimize risk-reward trade-offs based on ecological and physiological factors.

Spatio-temporal patterns of foraging behaviour in a wide-ranging seabird reveal the role of primary productivity in locating prey

Predicting the distribution and behaviour of animals is a fundamental objective in ecology and a cornerstone of conservation biology. Modelling the distribution of ocean-faring species like seabirds remains a significant challenge due to ocean dynamics, colony-specific effects and the vast ranges seabirds can cover. We used a spatial and behavioural approach to model the distribution of the Manx shearwater Puffinus puffinus, a pelagic, central-place forager that can cover great distances while foraging. GPS data from birds tagged in 2 colonies over 3 yr were modelled with a range of environmental predictors of marine productivity. For both colonies, transitions to foraging behaviour correlated with chlorophyll a, and the distribution of foraging behaviour was also associated with areas of high chlorophyll a concentration in coastal but not offshore areas for one colony. Furthermore, there was evidence for colony differences in habitat use, prevalence of nocturnal foraging, and for some competitive exclusion on foraging grounds, even though the colonies were 170 km apart. Despite the extensive dataset, our models had modest predictive power, which we suggest can probably only be improved by including biotic interactions, including more direct measures of food resource distribution. Our results highlight the importance of including spatial complexity and data from multiple sites when predicting the distribution of wide-ranging predators, because patterns of distribution and habitat use likely differ across the range of a population.

Daily and seasonal movements of Cape Cod gray seals vary with predation risk

White sharks Carcharodon carcharias and gray seals Halichoerus grypus are re-establishing their ecological roles within the Northwestern Atlantic Ocean, presenting an opportunity to understand gray seal movement and at-sea behavior under predation risk. As with other shark-seal hotspots, movements to and from terrestrial haul outs can be risky for gray seals, thereby eliciting antipredator strategies. We investigated the movement and coastal behavior of gray seals on Cape Cod (USA) in relation to seasonal and diel changes in white shark activity. Analyzing 412 trips to sea by 8 seals and more than 25000 acoustic detections from 23 individual white sharks, we observed seasonally homogeneous movements in seal behavior during months with greater shark presence. During riskier months, seal behavior manifested in near-exclusive nocturnal foraging, reduced offshore ranging, and limited at-sea activity. On these nocturnal trips to sea, seals returning to haul outs tended to avoid daybreak and traversed during diel minima in shark activity. However, seals tended to depart haul outs at dusk when shark presence was maximal. As conservation efforts succeed in rebuilding depleted populations of coastal predators, studying re-emerging predator-prey interactions can enhance our understanding about the drivers of movement and behavior.

Artificial Light at Night (ALAN) Is the Main Driver of Nocturnal Feral Pigeon (Columba livia f. domestica) Foraging in Urban Areas

Artificial light at night (ALAN) is one of the most extreme environmental alterations in urban areas, which drives nocturnal activity in diurnal species. Feral Pigeon (Columba livia f. domestica), a common species in urban centers worldwide, has been observed foraging at night in urban areas. However, the role of ALAN in the nocturnal activity of this species is unknown. Moreover, studies addressing the relationship between ALAN and nocturnal activity of diurnal birds are scarce in the Southern Hemisphere. The objective of this study is to assess the environmental factors associated with nocturnal activity of the Feral Pigeon in Argentinian cities. Environmental conditions were compared between sites where pigeons were seen foraging and randomly selected sites where pigeons were not recorded foraging. Nocturnal foraging by the Feral Pigeon was recorded in three of four surveyed cities. ALAN was positively related to nocturnal foraging activity in Salta and Buenos Aires. The results obtained suggest that urbanization would promote nocturnal activity in Feral Pigeons. Moreover, nocturnal activity was mainly driven by ALAN, which probably alters the circadian rhythm of pigeons.