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Predation risk can modify the foraging behaviour of frugivorous carnivores: implications of rewilding apex predators for plant-animal mutualisms

Citation

Burgos, Tamara et al. (2022), Predation risk can modify the foraging behaviour of frugivorous carnivores: implications of rewilding apex predators for plant-animal mutualisms, Dryad, Dataset, https://doi.org/10.5061/dryad.mpg4f4r0q

Abstract

Apex predators play key roles in food webs and their recovery can trigger trophic cascades in some ecosystems. Intra-guild competition can reduce the abundances of smaller predators and perceived predation risk can alter their foraging behaviour thereby limiting seed dispersal by frugivorous carnivores. However, little is known about how plant-frugivore mutualism could be disturbed in the presence of larger predators.

We evaluated the top-down effect of the regional superpredator, the Iberian lynx (Lynx pardinus), on the number of visits and fruits consumed by medium-sized frugivorous carnivores, as well as the foraging behaviour of identified individuals, by examining the consumption likelihood and the foraging time.

We carried out a field experiment in which we placed Iberian pear (Pyrus bourgaeana) fruits beneath fruiting trees and monitored pear removal by frugivorous carnivores, both inside and outside of lynx ranges. Using camera traps, we recorded the presence of the red fox (Vulpes vulpes), the Eurasian badger (Meles meles) and the stone marten (Martes foina), as well as the number of fruits they consumed and their time spent foraging.

Red fox was the most frequent fruit consumer carnivore. We found there were fewer visits and less fruit consumed by foxes inside of lynx ranges, but lynx presence did not seem to affect badgers. We did not observe any stone marten visits inside of lynx territories. The foraging behaviour of red foxes was also altered when inside of lynx ranges whereby foxes were less efficient, consuming less fruit per unit of time and having shorter visits. Local availability of fruit resources, forest coverage and individual personality also were important variables to understand visitation and foraging in a landscape of fear. 5. Our results show a potential trophic cascade from apex predators to primary producers. The presence of lynx can reduce frugivorous carnivore numbers and induce shifts in their feeding behaviour that may modify the seed dispersal patterns with likely consequences for the demography of many fleshy-fruited plant species. We conclude that knowledge of the ecological interactions making up trophic webs is anasset to design effective conservation strategies, particularly in rewilding programs.

Methods

Our experimental design compared the foraging of pear fruits in areas where the Iberian lynx was present or absent. We placed depots of 30 fruits beneath 30 Iberian pear adult trees. Fifteen fruit depots were located beneath pear trees inside the home ranges of two lynx couples, and the remaining 15 fruit depots were located at least 4.6 km away from any lynx home range and used as controls. We placed a camera trap (Scoutguard SG562-C; white led) in front of each fruit depot to record the species that visited the trees, the number of fruits consumed, and the time spent. The experiment lasted 15 consecutive days. We visited each camera trap site every 5-days to refill the fruit depots. We reached an overall effort of 437 days in which cameras were working and offered 2700 fruits of Iberian pear during the experiment. 

We processed all images taken by camera-traps in the fruit depots (n = 130269) and recorded the species, the date, and each event's hour. The number of fruits consumed in each visit was estimated by comparing each image with the previous one to count the number of fruits left. The time spent per visit was calculated as the difference between the time of the first image and the last one of each independent event, considering records separated by longer than 30 min as independent events (Linkie & Ridout, 2011). We considered one event per individual of the red fox when more than one was recorded in the same image because we could identify them individually. Foxes have particular fur marks that make them easily recognizable, mainly in legs, face and tail. Two experts identified the fox individuals independently and individualized more than 75% of images recorded by consensus. 

We counted the number of individual fruiting trees in the patches and visually estimated the individual crop size. We transformed our data on crop size into a logarithmic fruit abundance index (FAI): 0 = no fruits; 1 = 1–10 fruits; 2 = 11–100; 3 = 101–1,000; 4 = 1001–10,000; 5 > 10,000. (see Saracco, Collazo, & Groom, 2004). The overall crop size was calculated by adding the number of fruits on the canopy to the number of ripe fruits fallen on the ground every time we replenish the fruits in the depots (three times in total). We also recorded the forest cover inside a 100 m circular buffer around each isolated tree and around each MCP including all pear trees within the patch. We digitized the surface covered by forest from a high-resolution (0.5 m) orthophotography and calculated the percentage of forest cover within buffers (IGN, 2016).

References

IGN. (2016). Historical digital aerial orthophotographs of the Spanish National Orthophoto Program (PNOA). Available from: http://centrodedescargas.cnig.es/CentroDescargas/linkUnMD. [Accessed 15 Sept 2020]. Spanish.

Linkie, M., & Ridout, M. S. (2011). Assessing tiger-prey interactions in Sumatran rainforests. Journal of Zoology, 284(3), 224–229. doi: 10.1111/j.1469-7998.2011.00801.x

Saracco, J. F., Collazo, J. A., & Groom, M. J. (2004). How do frugivores track resources? Insights from spatial analyses of bird foraging in a tropical forest. Oecologia, 139(2), 235–245. doi: 10.1007/s00442-004-1493-7

Funding

Ministerio de Ciencia, Innovación y Universidades, Award: CGL2017-84633-P

Ministerio de Ciencia, Innovación y Universidades, Award: FPU17/04375