Fitness, risk taking, and spatial behavior covary with boldness in experimental vole populations

Abstract

Individuals of a population may vary along a pace-of-life syndrome from highly fecund, short-lived, bold, dispersive "fast" types at one end of the spectrum to less fecund, long-lived, shy, plastic "slow" types at the other end. Risk-taking behavior might mediate the underlying life history trade-off, but empirical evidence supporting this hypothesis is still ambiguous. Using experimentally created populations of common voles (Microtus arvalis)-a species with distinct seasonal life history trajectories-we aimed to test whether individual differences in boldness behavior covary with risk taking, space use, and fitness. We quantified risk taking, space use (via automated tracking), survival, and reproductive success (via genetic parentage analysis) in 8 to 14 experimental, mixed-sex populations of 113 common voles of known boldness type in large grassland enclosures over a significant part of their adult life span and two reproductive events. Populations were assorted to contain extreme boldness types (bold or shy) of both sexes. Bolder individuals took more risks than shyer ones, which did not affect survival. Bolder males but not females produced more offspring than shy conspecifics. Daily home range and core area sizes, based on 95% and 50% Kernel density estimates (20 ± 10 per individual, n = 54 individuals), were highly repeatable over time. Individual space use unfolded differently for sex-boldness type combinations over the course of the experiment. While day ranges decreased for shy females, they increased for bold females and all males. Space use trajectories may, hence, indicate differences in coping styles when confronted with a novel social and physical environment. Thus, interindividual differences in boldness predict risk taking under near-natural conditions and have consequences for fitness in males, which have a higher reproductive potential than females. Given extreme inter- and intra-annual fluctuations in population density in the study species and its short life span, density-dependent fluctuating selection operating differently on the sexes might maintain (co)variation in boldness, risk taking, and pace-of-life.

Keywords: Microtus arvalis; animal personality; automated radio telemetry; behavioral type; fitness; home range; parentage; reproductive success.

FIGURE 1

Schematic display of one near‐natural grassland enclosure. (a) Enclosures were equipped with Automated Radio Telemetry (ART) with (1) eight radio telemetry antennae (two in each corner) as part of an automated radio telemetry system (ART), (2) four guided passages with RFID readers (gray circles) in the vegetation free area strip (white area) along the enclosure wall, and (3) 25 live traps (black squares) in vegetation cover (light gray area). (b) Wooden guide passage (white T), wood structure with a hole surrounded by a RFID ring antenna (gray circle) close to the metal wall of the outdoor enclosure (gray surface). Gray box: RFID logger (i.e., storing unit). Note: not drawn true to scale

FIGURE 2

Visits of common voles at the potentially dangerous, vegetation free edge area of the enclosures, shown by sex and boldness type: (a) number of animals visiting per population (n = 14 populations, two animals per sex‐boldness type combination per population, jitter plot), (b) number of visits per individual, n = 44 visitors, significance levels (***p < .001, *p < .1) Shown are median (line), interquartile range (box), min‐max range (whiskers), and outliers (dots)

FIGURE 3

Behavior of common voles in large grassland enclosures over 7 weeks, gray: boldness type “bold,” white: boldness type “shy”. Experiments were divided into four phases based on female reproductive biology: Expl: exploration of novel environment including social environment and mating (3 days); Grav1: first pregnancy (15 days), Mate: parturition of litters and mating after postpartum estrus (5 days), Grav2: second pregnancy (13 days). (a) Number of visits at low vegetation (risky) areas of the enclosures. (b) Duration of visits (n = 358 visits by 44 common voles in 14 populations) at low vegetation (risky) areas of the enclosures. Long visits indicate a careful and slow movement at the passage counter, short visits a quick passage. Missing observations: no visits. Width of bar indicates relative sample size. (c) Model predictions for relative size of 1004‐day ranges (95% Kernel estimates) in relation to the respective population mean (= reference line: 100%) for 58 common voles (ID included as random effect) from nine enclosed populations (population included as random effects). Each day range was computed based on 90–120 location fixes per individual over 24 h. Asterisk refers to post‐hoc differences at p < .05 (compare Table 3)

FIGURE 4

Fitness of common voles in experimental populations (a) survival of males and females (initial numbers: 4 each per population) in 14 populations over the season, year 1 solid lines, year 2 dashed lines, (b) number of assigned offspring per individual (8 populations, 57 parental candidates, 16–44 offspring per population assigned) at a significance level of p < .05 (asteriks), (c) number of assigned offspring per male, Δ bold male, ○ shy male, gray lines = 8 populations sorted by months, year 1 white, year 2 gray symbols