Mixed strategies of griffon vultures' (Gyps fulvus) response to food deprivation lead to a hump-shaped movement pattern

Abstract

Background: The need to obtain food is a critical proximate driver of an organism's movement that shapes the foraging and survival of individual animals. Consequently, the relationship between hunger and foraging has received considerable attention, leading to the common conception that hunger primarily enhances a "food-intake maximization" (FIMax) strategy and intensive search. A complementary explanation, however, suggests a trade-off with precautions taken to reduce the risk of physiological collapse from starvation, under a strategy we denote as "energy-expenditure minimization" (EEMin). The FImax-EEmin trade-off may interact with the forager's hunger level to shape a complex (non-monotonic) response pattern to increasing hunger. Yet, this important trade-off has rarely been investigated, particularly in free-ranging wild animals. We explored how hunger affects the movements of adult griffon vultures (Gyps fulvus) in southern Israel. Transmitters combining GPS and accelerometers provided high-resolution data on vultures' movements and behavior, enabling the identification of feeding events and the estimation of food deprivation periods (FDPs, measured in days), which is used as a proxy for hunger.

Results: Data from 47 vultures, tracked for 339 ± 36 days, reveal high variability in FDPs. While flight speed, flight straightness and the proportion of active flights were invariant in relation to food deprivation, a clear hump-shaped response was found for daily flight distances, maximal displacements and flight elevation. These movement characteristics increased during the first five days of the FDP sequence and decreased during the following five days. These characteristics also differed between short FDPs of up to four days, and the first four days of longer FDP sequences. These results suggest a switch from FIMax to EEMin strategies along the FDP sequence. They also indicate that vultures' response to hunger affected the eventual duration of the FDP. During winter (the vultures' incubation period characterized by unfavorable soaring meteorological conditions), the vultures' FIMax response was less intensive and resulted in longer starvation periods, while, in summer, more intensive FIMax response to hunger resulted in shorter FDPs.

Conclusions: Our results show a flexible, non-monotonic response of free-ranging wild animals to increasing hunger levels, reflecting a trade-off between increasing motivation to find food and the risk of starvation. The proposed trade-off offers a unifying perspective to apparently contradictory or case-specific empirical findings.

Keywords: Fasting period; GPS-ACC tracking; Internal motivation; Movement ecology; Non-linear response; Optimal foraging; Starvation risks; Supplementary feeding management; Vulture conservation.

Figure 1

A map of the study area, showing the location of vultures’ roost sites (open circles), supplementary feeding stations (SFSs; black squares) and feeding events at occasional carcasses (black crosses). Each FDP sequence starts with a feeding event and ends one day before the successive feeding event.

Figure 2

Definition and occurrence of food deprivation periods (FDPs) in griffon vultures. (a) A schematic illustration of a timeline with feeding events (FE, marked in black) and FDPs to clarify terminology used throughout the paper. Each FDP sequence starts with a feeding event and ends one day before the successive feeding event. For instance, a FDP of zero represents feeding events on consecutive days. (b) A histogram of FDP for 4397 feeding events identified from the movement tracks of 47 vultures tracked with GPS/ACC tags. The inset shows the proportion of monthly events with FDP ≥ 6 days.

Figure 3

The change in various movement characteristics of vultures as a function of time since the last feeding event (the days within a FDP). The lines represent the best fitting model among a hump-shaped model (second-order polynomial, grey solid line), a linear response model (first-order polynomial; green dash-dotted line) and a lack of response model (grey dashed line on the mean value). Models were ranked according to AIC_c. Travel distance (a), maximal displacement (b) and flight elevation (d) showed similar hump-shaped trends, increasing for the first five days and decreasing afterward. FDP length had no clear effect on flight straightness (c), proportion of active days (e) and roost departure time (f). Error bars are S.E. between individual mean values.

Figure 4

The change in various movement characteristics of vultures as a function of time since the last feeding event (the days within a FDP) during short (1 ≤ FDP ≤ 4 d, white circles; shifted right for clarity) and long (FDP ≥ 6, black boxes) sequences. Long grey lines represent the best fitting model for the subset of long FDP sequences (see caption of Figure 3 for further details). Short thick lines represent linear regression for the short sequences and the corresponding period of the first four days of long sequences. Solid blue and dashed red lines are regression fits with slopes significantly or not significantly different than zero, respectively. FDP has a hump-shaped effect on daily travel distance (a), max displacement (b) and flight elevation (d); a linear effect on flight straightness (c) and no clear effect on proportion of active days (e) and roost departure time (f). Short sequences differ from the corresponding period of long sequences for all characteristics excluding flight straightness (c) and roost departure times (f).