Adjustment of the foraging effort in response to predation risk
In order to allocate more time and energy to predator avoidance behaviours when exposed to predation risk, individuals should postpone foraging task (Higginson et al., 2012). This decrease of the foraging effort should not straightforwardly be interpreted as a reduction of the number of items consumed. Indeed, our results show that considering the number of items consumed as the sole metric of the intensity of an individual’s response to a risk of predation could be misleading. Individuals of the granivore, H. affinis, when exposed to chemicals cues of a potential predator were found to significantly increase the total number of food items consumed in comparison to the control or the competition treatments. This increase in the number of food items consumed suggest that individuals H. affinis reduced their level of choosiness toward feeding items. H. affinis showed a marked reduction of the latency to first acceptance of a seed in comparison to the control or competitions treatments, suggesting that the effort that an individual is willing to invest in the acquisition of a resource (i.e. choosiness) is reduced under predation. Such foraging patterns cannot be interpreted as a lack of behavioural adjustment to the risk of predation or be explained by differences in handling time or trajectometry, as there were no differences in the handling time or the trajectometry metrics between the treatments.
Reductions in individual levels of choosiness could lead to the consumption of prey items that would be rejected under control conditions, but it might also provide important benefits. It could allow a greater focus on predator avoidance, for example, by reducing the cognitive load attributable to food item selection (Block et al., 2010). Metcalfe et al. (Metcalfe et al., 1987a, 1987b) found that salmon exposed to a fake predator reduced their level of choosiness for passing food pellets. Given that salmon use vision to acquire information both for predator vigilance and for assessing the quality of their prey they might accept a potential reduction in food quality in order to focus on vigilance. Bees were observed to lower their threshold of acceptance of flower quality when exposed to potential ambush predation by cryptic crab spiders in flowers. In doing so, the bees were able to minimize conflict between foraging and predator vigilance and the high energetic costs of foraging flights (Wang et al., 2013).
The performance of any two tasks that use similar sensory machinery, such as vision or chemoreception, can result in “dual task interference” (Lawrence, 1985; Pashler, 1994). Due to limitations of cognitive load either one of the tasks could be detrimental to the other, thus producing an “outcome conflict” (Lawrence, 1985; Navon and Miller, 1987). Even where these two tasks could be performed simultaneously, this will be both energy and time consuming (Wang et al., 2013) and many taxa do not succeed in solving the conflicts of dual task interference. Birds (Dukas, 2000) and humans (Joseph et al., 1997) have been observed failing to divide their attention between two complex visual tasks (Wang et al., 2013), for example. Hence, one solution to managing the limited available cognitive load, and the potential associated extra costs, might be to apply a weighting to each task (Pashler, 1994). In the vigilance-foraging trade-off this would be expressed by a reduction in the weight assigned to the foraging task, as was observed for salmon and bees (Metcalfe et al., 1987a, 1987b; Wang et al., 2013). Such difficulties in making acute choices, while performing a high-load cognitive task, were reviewed by Block et al. (Block et al., 2010), who noted that individuals typically respond by reducing their period of judgment and making more rapid choices. Rodents living in patches without refugia have been shown to reduce their time exposed to predators by reducing the time spent choosing seed food items (Perea et al., 2011), lowering both the risk of starvation and the risk of predation (Lawrence, 1985; Lima and Bednekoff, 1999).
Reductions in levels of choosiness for food items, as found for H. affinis, might therefore serve as a sensible strategy to reduce both the total duration of a foraging task and the cognitive load of the food quality assessment (Leaver and Daly, 2003). Our results therefore serve to extend the predation risk allocation hypothesis (Lima and Bednekoff, 1999), by suggesting that individuals could adopt one of several alternative strategies, with both reductions and increases in their level of choosiness for food items being possible in risky situations. Future experimental assessments of the risk allocation hypothesis should, therefore, try to define “foraging effort” and take into account the process of decision making itself.
Response to competition risk
A core expectation of our study was that the individuals should also decrease their level of choosiness in response to the risk of competition, due to opportunity costs (Dechaume-Moncharmont et al., 2016). We found that the effects of competition on the level of choosiness (i.e. latency to first acceptance and mean number of seeds eaten) were similar across the two competition treatments. Latency to first acceptance of a seed and mean number of seed eaten per individuals were also not significantly different between the competition treatments and to the control. However, the values of the effect size for the latencies to first acceptance would suggest at a reduction in individual levels of choosiness and that it would be misleading to interpret these results as evidence for absence of a competition effect (Nakagawa and Cuthill, 2007). Rather, it suggests that we may not have taken into account all possible co-variates of competition that affect foraging, such as individual personality (David et al., 2011; Royauté and Pruitt, 2015), and future studies should seek to evaluate the importance of these co-variates.
In order to avoid agonistic behaviours or competitive interference between individuals, our protocol was based on indirect competition or predation risks in the form of olfactory cues impregnating the arena paper. It may be that the use of odour as a competition cue, in place of test competitor individuals and the associated reduction in food items that would have ensued, might have lowered the perceived risk of competition enough that the H. affinis individuals did not modify their foraging effort, irrespective of the potential linked costs (Mohamad et al., 2014). Moreover, given that individuals were maintained in groups of up to 20 individuals prior to experiment, which matched the amount of individuals used to impregnate the tests papers, the focal individuals might have become habituated to situations of competition similar to the one under test potentially reducing our power to test for competition risk perception (Milinski, 1982; Mohamad et al., 2014).
While changes in level of choosiness were not observed under both competition treatments, our results did demonstrate a difference in latency to first movement and in space use between the two competition treatments. H. affinis individuals were found to move later and visit fewer squares of the arena in the intraspecific competition treatment. Similar patterns in the use of space were observed for P. melanarius in avoiding papers impregnated with chemical cues from conspecifics (Guy et al., 2008). We hypothesise that this lower space use and increased latency to first movement may be due to an effect of sex, with male and female arresting in the presence of odours from the opposite sex. An alternative hypothesis is that the perceived risk of competition itself affects space use. For example, individuals of the Bullethead Parrotfish, Chlorurus spilurus, do not change their feeding rate under competition, but modify the way that they use space during foraging (Davis et al., 2017).
Carabid beetles in agroecosystem
Our study group of choice is the carabid beetles that naturally inhabit arable farmland. Many thousands of individuals exist in farm fields in communities of granivore, omnivore and predatory species that can be cannibalistic and inter-specific predators (McKemey et al., 2003; Charalabidis pers.obs.). Reductions in the level of choosiness, in an environment filled with predation cues, might lead to an increase in the number of weed seeds accepted by the granivorous carabids. Counterintuitively, therefore, predation risk might be a mechanism for a biodiversity-ecosystem function (Hines et al., 2015; Reiss et al., 2009) relationship amongst the carabids. Rather than the commonly held expectation that communities formed of granivores alone should have the highest weed seed predation (Petit and Bohan, 2017), our results predict that the ecological function of weed seed predation would increase with the diversity of the carabid community.
The authors would like to thank the staff of the INRA Epoisses experimental farm. We also wish to thank the staff at INRA Dijon for their technical support, and Benjamin Carbonne for his help with trapping and handling the carabids. This work was supported by the Joint Programming Initiative on Agriculture, Food Security and Climate Change, European Research Area Network in the Coordinated-Integrated Pest Management in Europe Strategic Research Agenda (FACCE ERA-NET C-IPM) project BioAWARE (AFB Projet 00000877, https://www.faccejpi.com) and the PEERLESS (ANR-12-Agro-0006) and AGROBIOSE (ANR-13-Agro-0001) grants from the French Agence Nationale de la Recherche (http://www.agence-nationale-recherche.fr/en/) to DB and SP. The PhD of Alice Charalabidis was co-funded by the Institute Nationale de la Recherche Agronomique (INRA) and the Region of Burgundy Franche-Comté. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Table of contents :
First Chapter: General introduction
1. The implicit costs of choosing
2. Feeding preferences and individual levels of choosiness
3. Variation of choosiness
4. A growing interest for the use of biocontrol agents in agricultural fields
4.1. Agronomy general context
4.2. Alternatives to the use of pesticides products
5. Carabids beetles as biological control agents of weeds in arable fields
5.1. Seed of weeds predation by carabids
5.2. Possible source of variation in granivory rates.
5.3. Feeding guilds co-occurring in the wild
6. The brief aims and summary of this PhD
7. Building an experimental methodology to assess change in levels of choosiness in foraging carabids
7.1. A laboratory controlled experiment that uses olfactory cues to simulate interference risk in the place of live carabids
7.2. Choice of the carabid species used in tests
7.3. Choice of a valid metric to evaluate the variation in level of choosiness
Second Chapter: Is individual level of choosiness modified by predatory and competitive interference in carabid beetles: a case study using the granivorous carabid beetle Harpalus affinis
1) Introduction to chapter II
2) Article 1
F. Supplementary materials
3) Chapter conclusion
Third Chapter: Effect of the diet of a carabid species on its level of choosiness for seeds when foraging under intraguild interferences
1) Introduction to chapter III
2) Article 2
G. Supplementary materials
3) Chapter conclusion
Fourth Chapter: Effect of individual personality traits and immune defences on the level of choosiness.
1) Introduction to chapter IV
2) Article 3
F. Supplementary materials
3) Chapter conclusion
Fifth Chapter: Consistency of the behavioural adjustment to predation risk in more complex, and potentially realistic, spatiotemporal conditions – the effect of the intensity of the risk and seed preference on individual level of choosiness
1) Introduction to chapter V
2) Article 4
F. Supplementary material
3) Chapter conclusion
Sixth Chapter: General discussion
1. H. affinis changes its level of choosiness for seeds of T. officinale under intraguild interference from other carabid species
2. Factors affecting change in level of choosiness in carabids
2.1. Adjustment of level of choosiness with carabid species
2.2. Adjustment of level of choosiness according to the seed species
2.3. Adjustment of level of choosiness according to risk intensity
2.4. Variation in level of choosiness under predation risk might be dependent on individual characteristics, such as sex, immunity and personality traits.
3. Potential issues encountered through our results
3.1. Encountered difficulties raising from using wild caught individuals
3.2. Effect of the season on the data
4. Conclusion – the impact of changes in H. affinis choosiness and foraging behaviour, and its implications for the biocontrol of weeds