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The behavior and evolution of cache protection and pilferage
Abstract
Food-storing animals hide food in times of abundance and rely on memory to recover those caches several days if not months later when supplies are scarce. This review focuses on the different models that have been proposed to explain the evolution of food caching, specifically those models that describe how food caching might have evolved in an environment of cache pilferage. We discuss the use of cache protection behaviours in cachers, and the success of these behaviours in bringing about a reduction in cache theft, before looking at the behaviours of prospective thieves that facilitate cache pilferage. Finally, we consider the insights these behaviours give us into the cognitive abilities of food-storing animals.
... Haypiles represent significant resources accessible to pikas and even other herbivorous mammals in extreme weather conditions and are subject to theft predominantly by conspecifics requiring either defense or reciprocal theft ("you steal, I steal"; Kleptoparasitism) to stabilize behavioral strategies (Andersson and Krebs 1978;McKechnie et al. 1994;Dally et al. 2006;Wang et al. 2018). For example, rodents that are phylogenetically closely related to each other store food in different ways, with some species spreading caches over large areas (scatter-hoarding) and others concentrating them in relatively small areas with active guarding (larder-hoarding; Dally et al. 2006;Wang et al. 2018). ...
... Haypiles represent significant resources accessible to pikas and even other herbivorous mammals in extreme weather conditions and are subject to theft predominantly by conspecifics requiring either defense or reciprocal theft ("you steal, I steal"; Kleptoparasitism) to stabilize behavioral strategies (Andersson and Krebs 1978;McKechnie et al. 1994;Dally et al. 2006;Wang et al. 2018). For example, rodents that are phylogenetically closely related to each other store food in different ways, with some species spreading caches over large areas (scatter-hoarding) and others concentrating them in relatively small areas with active guarding (larder-hoarding; Dally et al. 2006;Wang et al. 2018). In situations of high conspecific density, the Korean Field Mouse (Apodemus peninsulae) switches from scatter-hoarding to larder-hoarding and guards caches with aggression as scatter-hoarding is not stable (leads to high levels of pilferage that are not sustainable; Wang et al. 2011). ...
... We expected that haypiles of O. ladacensis would be uniformly distributed on the colony to reduce conflict related to theft of caches by conspecifics (Vander Wall and Jenkins 2003;Male and Smulders 2007;Robin and Jacobs 2022). Haypiles of O. ladacensis were clumped in distribution, unlike that expected from game theory models and experiments on group-living animals (Andersson and Krebs 1978;Dally et al. 2006;Wang et al. 2018). Group-living animals at high densities should distribute their caches uniformly to reduce conflict between conspecifics (related to theft). ...
Food caching and haying can help species to survive extreme environmental conditions and cope with seasonal fluctuations in resource availability. We documented the food caching/haying behavior of the Ladakh Pika (Ochotona ladacensis) and the Nubra Pika (O. nubrica) from the cold desert of the Changthang biotic province, Ladakh, India, and contrasted their haying strategies under differing conditions of sociality and niche occupation. We found that the more social and larger species, O. ladacensis—which lives in open microhabitats—built larger and more conspicuous haypiles compared to O. nubrica—which built smaller, concealed haypiles in less open microhabitats. Ochotona ladacensis collected a different set of plants with greater overall richness than O. nubrica. Both species collected distasteful, toxic plants that are known to discourage herbivory. Ochotona nubrica placed haypiles closer to burrows in comparison to O. ladacensis. Haypiles in O. ladacensis colonies were clumped rather than uniformly distributed, not meeting predictions of the theory of cache defensibility associated with theft by conspecifics. The present study provides insights into haypile characteristics and associated behavioral responses of high-elevation pikas to variation in the availability of resources.
... For this behavior to be evolutionary advantageous, caching individuals must retrieve a sufficient proportion of the food they previously stored (Krebs 1990). Thus, caching individuals must not only re-locate their caches but also protect these resources from potential thieves (pilferers) (Dally et al. 2006). Indeed, many corvid (e.g., crows, magpies, jays) and parid (e.g., chickadees) species have excellent observational spatial memory and can retain this information to relocate caches made by others, sometimes days after a cache has been made (e.g., pinyon jays Gymnorhinus cyanocephalus, Bednekoff and Balda 1996a;Dunlap et al. 2006; Mexican jays Aphelocoma wollweberi and Clark's nutcrackers Nucifraga columbiana, Bednekoff and Balda 1996b;ravens Corvus corax, Scheid and Bugnyar 2008; great tits Parus major, Brodin and Urhan 2014). ...
... The aforementioned studies examining cache pilfering by avian species have mainly investigated the interactions among conspecifics, with limited investigations of pilfering by heterospecifics (but see Pravosudov 2008). However, heterospecific pilfering has been reported in the wild on multiple occasions (e.g., Burnell and Tomback 1985;Dally et al. 2006;Chock et al. 2019) and may account for a major proportion of caches lost to pilfering (e.g., Vander Wall and Jenkins 2003;Penner and Devenport 2011;Dittel et al. 2017;Swift et al. 2022). Additionally, learning to adjust caching behavior in the presence of a heterospecific observer might showcase the behavioral plasticity of caching individuals. ...
... The propensity to cache seems to be innate in most corvid species as it is hypothesized that the common ancestor of all corvids was a moderate cacher (i.e., caching different food items through the year but not being entirely dependent upon those caches; de Kort and Clayton 2006). However, more advanced caching behaviors that improve caching efficiency, such as cache protection behaviors, may require learning (Emery and Clayton 2001;Dally et al. 2006). Yet, whether corvids can determine if a heterospecific observer is a potential pilfering threat and engage in behavioral plasticity through cache protection behaviors when observed by a heterospecific, remains unknown. ...
Behavioral plasticity can be described as the ability to adjust behavior depending on environmental information. We used a food-storing (caching) paradigm, during which individuals either ate or cached food under different conditions, to investigate whether they could adjust their caching behavior when observed by conspecifics and heterospecifics and which social cues they used to elicit these behavioral changes. We examined the location and number of caches made by two corvid species differing in sociality: highly social pinyon jays (Gymnorhinus cyanocephalus) and less social Clark’s nutcrackers (Nucifraga columbiana). Although pinyon jays cached a similar amount of food across conditions, they allocated significantly more caches to areas less accessible to the observer. Nutcrackers, however, significantly reduced the number of seeds cached when another nutcracker was present in comparison to when they cached alone. Both species relied on different social cues to elicit re-caching: pinyon jays responded to the amount of time the observer spent close to the caching locations, whereas nutcrackers responded to the amount of time the observer spent pilfering their caches. The differences in cache protection behaviors and the social cues eliciting them may be explained by the species’ social organization. Pinyon jays may only adjust their caching behavior when necessary, as they are often surrounded by other individuals. Being less social, Clark’s nutcrackers reduce their caching when observed, as they have more opportunities to cache alone and may resort to additional cache protection when experiencing pilferage. Overall, our results provide insight into understanding how pressures associated with the social environment may influence foraging behaviors.
Significance statement
To maximize resources, Corvidae will hide food for later consumption and seek out the hidden food of others. These birds also subvert this ecological game of “hide-and-seek” by re-hiding food that other birds know about. We demonstrate that two corvid species initiate “hide-and-seek” in response to different social information. Social pinyon jays re-hide their food after another bird approaches their hiding spots, a proactive response suited for species living in groups, in which attributing food theft to a specific individual may be difficult. Less-social Clark’s nutcrackers re-hide food only after seeing another bird steal from them, a reactive response suited for species that typically have more opportunities for privacy when hiding food. We demonstrate corvids adapt to the risk posed by birds “seeking” their food, though which behaviors of the seeker are deemed risky differ between species and are shown to align with ecological demands.
... The cached foods of hoarders are often pilfered by intraor inter-specific competitors, which threaten the survival and reproduction of the hoarders (Vander Wall & Jenkins 2003;Gu et al. 2017). Accordingly, food hoarders have evolved different strategies to reduce pilfering of their caches and replace lost caches by harvesting food from the source and/or pilfering caches from other hoarders (Vander Wall & Jenkins 2003;Dally et al. 2006;Niu et al. 2020a). Due to differences in hoarding behaviors (larder hoarding vs. scatter hoarding), ability to protect caches, and pilferage among sympatric animals, the results showed that the competition are usually asymmetric, in that some species (e.g. ...
... Dominant species with large body sizes (e.g. CWR) usually prefer to larder hoard food and aggressively defend these caches against subordinate species (Dally et al. 2006;Zhang et al. 2014a;Niu et al. 2020a), and also eat more food items to maintain their higher energetic needs due to different body sizes (Dally et al. 2006;Niu et al. 2020a). By contrast, the subordinate species with small body sizes (e.g. ...
... Dominant species with large body sizes (e.g. CWR) usually prefer to larder hoard food and aggressively defend these caches against subordinate species (Dally et al. 2006;Zhang et al. 2014a;Niu et al. 2020a), and also eat more food items to maintain their higher energetic needs due to different body sizes (Dally et al. 2006;Niu et al. 2020a). By contrast, the subordinate species with small body sizes (e.g. ...
Asymmetric competition occurs when some species have distinct advantages over their competitors and is common in animals with overlapping habitats and diet. However, the mechanism allowing coexistence between asymmetric competitors is not fully clear. Chinese white‐bellied rats (Niviventer confucianus, CWR) and Korean field mice (Apodemus peninsulae, KFM) are common asymmetric competitors in shrublands and forests west of Beijing city. They share similar diet (e.g. plant seeds) and activity (nocturnal), but differ in body size (CWR are bigger than KFM), food hoarding habit (CWR: mainly larder hoarding; KFM: both larder and scatter hoarding), and ability to protect cached food (CWR are more aggressive than KFM). Here, we tested seed competition in 15 CWR‐KFM pairs over a 10‐day period under semi‐natural enclosure conditions to uncover the differences in food hoarding, cache pilferage and food protection between the two rodents, and discuss the implication for coexistence. Prior to pilferage, CWR harvested and ate more seeds than KFM. CWR tended to larder hoard seeds, whereas KFM preferred to scatter hoard seeds. Following pilferage, CWR increased consumption, decreased intensity of hoarding, and pilfered more caches from KFM than they lost, while KFM increased consumption more than they hoarded, and they preferred to hoard seeds in low and medium competition areas. Accordingly, both of the two rodent species increased their total energy consumption and hoarding following pilferage. Both rodent species tended to harvest seeds from the source, rather than pilfer caches from each other to compensate for cache loss via pilferage. Compared to CWR, KFM consumed fewer seeds when considering seed number, but hoarded more seeds when considering the seeds’ relative energy (energy of hoarded seeds/rodent body mass2/3) at the end of the trials. These results suggest that asymmetric competition for food exists between CWR and KFM, but differentiation in hoarding behaviour could help the subordinate species (i.e., KFM) hoard more energy than the dominant species (i.e., CWR), and may contribute to their coexistence in the field. This article is protected by copyright. All rights reserved
... For example, rooks (Corvus frugilegus) cache food cautiously hiding the activity when conspecifics are around, such as caching in long grass where their activity is less likely to be observed [personal observation of Emery and Clayton, in: (26)]. However, they do not adopt the same prudence in the presence of other rooks who are also engaged in caching [ (27), cited in: (26)], as though they were "confident" that other rooks focused on the same activity would not be interested in pilfering. ...
... Similarly, western scrub-jays (Aphelocoma californica) who suffered pilfering of their caches in the past, unlike naïve individuals, tended to cache in new sites, out-of-view sites or shaded sites when observed by competitors [from Emery and Clayton (29), cited in (26)] or maximise the distance from an observer when this could not be left out of sight [(30), cited in: (26)]. The birds also repeatedly moved specific caches that were hidden while observers were watching, possibly to confuse them, and recached items as soon as they were given a private moment from others (26). ...
... Similarly, western scrub-jays (Aphelocoma californica) who suffered pilfering of their caches in the past, unlike naïve individuals, tended to cache in new sites, out-of-view sites or shaded sites when observed by competitors [from Emery and Clayton (29), cited in (26)] or maximise the distance from an observer when this could not be left out of sight [(30), cited in: (26)]. The birds also repeatedly moved specific caches that were hidden while observers were watching, possibly to confuse them, and recached items as soon as they were given a private moment from others (26). However, when scrub-jays do not see competitors around, they show no preference between shady and well-lit sites [(30), cited in: (26)], suggesting that experience might play a role in their performance of privacy behaviours. ...
Privacy is an essential consideration when designing interactive systems for humans. However, at a time when interactive technologies are increasingly targeted at non-human animals and deployed within multispecies contexts, the question arises as to whether we should extend privacy considerations to other animals. To address this question, we revisited early scholarly work on privacy, which examines privacy dynamics in non-human animals (henceforth “animals”). Then, we analysed animal behaviour literature describing privacy-related behaviours in different species. We found that animals use a variety of separation and information management mechanisms, whose function is to secure their own and their assets' safety, as well as negotiate social interactions. In light of our findings, we question tacit assumptions and ordinary practises that involve human technology and that affect animal privacy. Finally, we draw implications for the design of interactive systems informed by animals' privacy requirements and, more broadly, for the development of privacy-aware multispecies interaction design.
... While larder-hoarding species that make a few large caches have the opportunity to defend these caches against potential robbers (e.g. Clarke & Kramer, 1994), scatterhoarding species that cache each item in a separate location typically do not defend these specific locations (reviewed in Dally et al., 2006a). However, many scatter-hoarding species are territorial. ...
... Researchers have attempted to understand and categorize the strategies used by scatter-hoarding species to minimize cache robbery (reviewed in Dally et al., 2006a). These strategies can be generally classified as either quantity based or location based. ...
... Additionally, we found that Canada jays may use their own location to reduce cache robbery. While cache protection strategies are common among scatter hoarders (see Dally et al., 2006a), species are typically assigned or assessed for only one cache protection strategy at a time. This is one of the first demonstrated examples of individuals using, and modulating, multiple strategies simultaneously. ...
Food caching is a behaviour used by a variety of birds and mammals and can be an essential strategy for surviving food-scarce periods. Ensuring that cached food remains available for later recovery is critical to the fitness of caching individuals. Cache robbers, conspecific or heterospecific individuals that remove and consume food stored by the original cacher, present a unique threat to food-caching individuals. Accordingly, caching species have evolved a variety of cache protection strategies to limit the potential risk of cache robbery. We assessed these cache protection strategies in Canada jays, year-round residents of Canada and the western United States that rely on cached food to survive food-scarce winters. We evaluated caching behaviour and movement patterns of captive Canada jays in caching contexts that varied in potential risk of cache robbing: presence versus absence of a model cache robber and visual cover from the cache robber. We found that depending on perceived risk, Canada jays flexibly used a variety of nonmutually exclusive cache protection strategies including cache depression, out-of-sight caching and spacing. These cache protection strategies likely reduce the risk of cache robbing and increase the probability of caches remaining available for recovery and consumption.
... Food items can be hoarded in central larders (larder hoarding) or in multiple sites with a few food items in each (scatter hoarding) (Vander Wall, 1990). Larderhoarding behaviour leads to aggressive cache defence where individuals exclude most thieves but are at risk of complete food loss from a superior competitor (Dally, Clayton, & Emery, 2006;Gerhardt, 2005). In contrast, scatter hoarding helps prevent complete cache loss by spreading out the cached items across space but increases costs associated with caching and later retrieving numerous caches (MacDonald, 1997;Preston & Jacobs, 2001). ...
... Cache pilferage from conspecifics and heterospecifics is one of the selective forces on the evolution of food-hoarding behaviour (Clarke & Kramer, 1994;Dally et al., 2006;Vander Wall & Jenkins, 2003). Generally, scatter-hoarders are sensitive to competitors when caching food items and tend to reduce cache loss by increasing hoarding, spacing caches, caching repeatedly, shifting to larder hoarding, evicting competitors and/or engaging in deceptive behaviour (pilferage avoidance hypothesis; Vander Wall & Jenkins, 2003;Dally et al., 2006;Steele et al., 2008Steele et al., , 2014. ...
... Cache pilferage from conspecifics and heterospecifics is one of the selective forces on the evolution of food-hoarding behaviour (Clarke & Kramer, 1994;Dally et al., 2006;Vander Wall & Jenkins, 2003). Generally, scatter-hoarders are sensitive to competitors when caching food items and tend to reduce cache loss by increasing hoarding, spacing caches, caching repeatedly, shifting to larder hoarding, evicting competitors and/or engaging in deceptive behaviour (pilferage avoidance hypothesis; Vander Wall & Jenkins, 2003;Dally et al., 2006;Steele et al., 2008Steele et al., , 2014. Andersson and Krebs (1978) and Stapanian and Smith (1978) proposed that food hoarding would become evolutionarily stable only if the hoarder gains significantly more from retrieving its own caches than a pilferer. ...
The reciprocal pilferage hypothesis argues that, despite the occurrence of pilferage, scatter-hoarding behaviour could evolve if cache loss is compensated by gains pilfered from others. However, this model has not been strictly tested because of the difficulty associated with tracking caches, including ownership, over long periods. Using infrared radiation cameras, we tracked caching of Juglans regia seeds by groups of two Père David's rock squirrels, Sciurotamias davidianus, within a large natural enclosure. Our goal was to quantify how squirrels responded to the presence of a conspecific when seed hoarding and pilfering and test the reciprocal pilferage hypothesis. We found that the numbers of seeds harvested from the seed sources and pilfered from conspecifics was initially low, increasing as seeds were removed and then dropping off once few seeds remained at the seed sources. Additionally, the number of seeds scatter hoarded increased with a decreasing number of seeds remaining at the sources. Seeds harvested from the source and pilfered from competitors were at first cached randomly within the enclosure and then centralized to the low-competition area near the nest as seed sources declined. Overall, pilferage was not high. The proportions of seeds pilfered did not vary between conspecifics and were positively correlated with each other over trials. More seeds were harvested from the seed sources than pilfered by competitors at the early stage of hoarding. These results suggest that, under conspecific competition, squirrels appeared first to compete for food at the sources, then for caches with each other as food sources decreased, and finally cache ownership became relatively stable. Squirrels compensated for cache loss by both harvesting food from the sources and pilfering caches from its competitor. The amount of seeds gained from pilfering was sufficient to replace pilfered caches, supporting the reciprocal pilferage hypothesis.
... Food-caching, the behavior of storing food when plentiful to ensure availability of nourishment when resources are scarce, is a natural behavior often used during investigations of the sociocognitive abilities of corvids (e.g., Clary, & Kelly, 2011;Emery & Clayton, 2001). Two important components involved in food-caching are spatial memory, remembering where (and possibly when) an item was stored (reviewed by Gould, Kelly, & Kamil, 2010;Pravosudov & Smulders, 2010), and securing the food store-for instance, protecting the resource against pilferage (reviewed by Bugnyar, 2013;Dally, Emery, Clayton, 2006a;Emery & Clayton, 2009). Corvids present an excellent opportunity to examine sociocognitive abilities, as they have natural variation in their caching behavior and socioecology, both argued to influence cache protection strategies (Dally, Emery, & Clayton, 2006a). ...
... Two important components involved in food-caching are spatial memory, remembering where (and possibly when) an item was stored (reviewed by Gould, Kelly, & Kamil, 2010;Pravosudov & Smulders, 2010), and securing the food store-for instance, protecting the resource against pilferage (reviewed by Bugnyar, 2013;Dally, Emery, Clayton, 2006a;Emery & Clayton, 2009). Corvids present an excellent opportunity to examine sociocognitive abilities, as they have natural variation in their caching behavior and socioecology, both argued to influence cache protection strategies (Dally, Emery, & Clayton, 2006a). For instance, Clark's nutcrackers (Nucifraga columbiana) make thousands of caches in the autumn and rely on these food stores almost exclusively over the subsequent winter and spring, whereas jackdaws (Corvus monedula) do not cache at all (de Kort & Clayton, 2006). ...
... California scrub jays (Aphelocoma californica) are semisocial and live in small groups, whereas Eurasian jays (Garrulus glandarius) are territorial (Emery & Clayton, 2009). Joining these two facets, caching and sociality, through the investigation of cache protection strategies, has provided an insight into whether the socioecological demands of a particular species influence its cache protection strategies (Clayton, Dally, & Emery, 2007;Dally, Emery, & Clayton, 2006a). ...
Caching species store food when plentiful to ensure availability when resources are scarce. These stores may be at risk of pilferage by others present at the time of caching. Cachers may reduce the risk of loss by using information from the social environment to engage in behaviors to secure the resource-cache protection strategies. Here, we examined whether pinyon jays, a highly social corvid, use information from the social environment to modify their caching behavior. Pinyon jays were provided with pine seeds to cache in two visually distinct trays. The cacher could be observed by a non-pilfering conspecific, a pilfering conspecific, or an inanimate heterospecific located in an adjoining cage compartment, or the cacher could be alone. After caching, the pilfered tray was placed in the adjoining compartment where caches were either pilfered (pilfering conspecific and inanimate heterospecific conditions) or remained intact (non-pilfering conspecific and alone conditions). The safe tray was placed in a visible, but inaccessible, location. Overall, pinyon jays reduced the number of pine seeds cached in the pilfered tray when observed, compared with caching alone. However, their caching behavior did not differ between the pilfering conspecific and the non-pilfering conspecific conditions. These results suggest that either pinyon jays were unable to discriminate between the pilfering and non-pilfering conspecifics, or they generalized their experience of risk from the pilfering conspecific to the non-pilfering conspecific. Thus, we report evidence that pinyon jays use cache protection strategies to secure their resources when observed, but respond similarly when observed by pilfering and non-pilfering conspecifics.
... Animals of-ten store food during a food-rich period (e.g. in autumn) and rely on these foods for survival and/or reproduction in the following periods of food scarcity (e.g. in winter and early spring), thereby increasing fitness of survival and reproduction (Vander Wall 1990). The food-hoarding spectrum varies from larder-hoarding (concentrating food items in a few locations) to scatter-hoarding (with multiple small caches) under different conditions (Vander Wall 1990;Dally et al. 2006). ...
... As an important consequence of food loss, food pilferage by intraspecific and interspecific competitors threatens the survival and the reproductive capacity of hoarders when food is scarce (Wauters et al. 1995;Vander Wall & Jenkins 2003;Gerhardt 2005). Evidently, food hoarders are sensitive to competitors and have evolved an array of strategies to reduce or prevent the risk of pilferage posed by competitors (reviewed by Vander Wall & Jenkins 2003;Dally et al. 2006;Grodzinski & Clayton 2010). ...
... Food hoarders can adopt one or more of the following strategies to compete for food and/or minimize and compensate for food loss. First, food hoarders can limit or invalidate the information that a potential pilferer has gathered (MacDonald 1976;Dally et al. 2006;Grodzinski & Clayton 2010). Some hoarders hoard foods in secret locations far away from the sources (Galvez et al. 2009;Zhang et al. 2014a;Steele et al. 2014Steele et al. , 2015, recache items to invalidate pilferers' sensory information (Dally et al. 2005(Dally et al. , 2006, use misinformation (e.g. ...
Superior species may have distinct advantages over subordinates within asymmetrical interactions among sympatric animals. However, exactly how the subordinate species coexists with superior species is unknown. In the forests western Beijing city, intense asymmetrical interactions of food competition exist among granivorous rodents (e.g. Apodemus peninsulae, Niviventer confucianus, Sciurotamias davidianus, Tscherskia triton) that have broadly overlapping habitats and diets, but have varied body‐size (range 15 – 300 g), hoarding habit (scatter vs. larder) and/or daily rhythm (diurnal vs. nocturnal). The smallest rodent, A. peninsulae, which usually faces high competitive pressure by larger rodents, is an ideal model to explore how subordinate species coexist with superior species. Under semi‐natural enclosure conditions, we tested responses of seed‐hoarding behaviour in A. peninsulae to intra‐ and inter‐specific competitors at the situations of pre‐competition (without competitor), competition (with competitor) and post‐competition (competitor removed). The results showed that A. peninsulae increased intensity of larder‐hoarding, reduced intensity of scatter‐hoarding in the presence of intraspecifics and S. davidianus, whereas, they ceased foraging and hoarding in the presence of N. confucianus and T. triton. A. peninsulae reduced intensity of hoarding outside the nest, and moved more seeds into the nest for larder‐hoarding under competition from intraspecific individuals and S. davidianus. In most cases, the experimental animals could recover to its original state of pre‐competition when competitors were removed. These results suggest that subordinate species contextually regulate their food‐hoarding strategies according to different competitors, promoting species coexistence among sympatric animals that have asymmetrical food competition. This article is protected by copyright. All rights reserved.
... Because scatter hoards are not specifically protected and defended by hoarders (Vander Wall, 1990), they are more likely to be pilfered than larder hoards Daly, Jacobs, Wilson, & Behrends, 1992;Dittel & Vander Wall, 2018;Wang et al., 2018). Therefore, scatter-hoarders adopt strategies to repeatedly recover and move caches (Dally, Clayton, & Emery, 2006), increase or reduce caching in response to pilfering risk (Huang, Wang, Zhang, Wu, & Zhang, 2011) or directly establish caches in areas with low seed density or high risk of predation to avoid cache pilferage (Geng, Wang, & Cao, 2017;Hirsch, Kays, Pereira, & Jansen, 2012;Steele et al., 2015Steele et al., , 2014Yang, Zhang, & Yi, 2016). Larder-hoarding animals are thought to be typical central-place foragers (Larimer et al., 2011), ranging from their nests to collect food items. ...
... Larder-hoarding animals are thought to be typical central-place foragers (Larimer et al., 2011), ranging from their nests to collect food items. Although larder-hoarding animals are able to defend their larder hoards aggressively to effectively reduce cache pilferage by competitors (Clarke & Kramer, 1994;Dally et al., 2006), the benefit that larder-hoarders gain from larder-hoarded food decreases with increasing distance between nests and foraging patches (Charnov, 1976;Schmidt-Nielsen, 1972). Therefore, the hoarding strategy can be expected to change as a function of distance between a food patch and the home burrow or nest (Jenkins & Rothstein, 1995;Tsurim & Abramsky, 2004). ...
... Optimal cache spacing theory or optimal density models predict that larder-hoarders, which are central-place foragers, should trade the distance from the food source to the nest against the risk of cache pilferage (Donald & Boutin, 2011;Gerhardt, 2005). Scatterhoarding animals must optimally trade the benefits of reducing cache loss risk against the costs of carrying food items to caches (Clarkson et al., 1986;Dally et al., 2006;G alvez et al., 2009;Stapanian & Smith, 1984). Therefore, optimizing the distance between caches and the food source or nests during hoarding may guarantee consistent returns from caches (Daly et al., 1992;Smith & Reichman, 1984;Tsurim & Abramsky, 2004). ...
The rapid sequestering hypothesis predicts that scatter-hoarding animals quickly sequester food items by rapidly storing seeds in caches nearby seed sources to reduce competition. However, tests of this hypothesis usually use food hoarding animals with a single load or a small load size. How multi-load animals place their caches between food sources and nests remains largely unknown. Here, we hypothesized that multi-load animals, compared to single-load animals, may not necessarily sequester food items but adopt alternative hoarding strategies due to their multi-load ability. In this study, we presented seeds at different distances away from the nests of the multi-load chipmunk Tamias sibiricus and mapped the spatial distribution of their caches in multi-compartment enclosures to test our hypothesis that a multiple prey loader will consistently establish caches near nests rather than rapidly sequester nearby the seed source. By using multiple-compartment enclosures with different distances between the seed source and nests, and given potential intra- and inter-specific competition, we found T. sibiricus consistently placed their caches near nests but away from the seed source. Cache placement near nests may serve as an alternative strategy that not only guarantees a maximum harvest rate at the seed source but also ensures effective cache defense near nests. Moreover, scatter-hoarding seeds near nests may alternatively guarantee food supply in case of complete loss of larder-hoarded seeds. Unlike other scatter-hoarding animals that rapidly sequester seeds near food sources, establishing caches near nests by T. sibiricus implied long dispersal distances for seeds in our study. Therefore, scatter-hoarding by multiple prey loaders is expected to be ecologically important for the structure and function of tree communities, especially in ecosystems in which seeds depend on food hoarding animals for dispersal and germination.
... Inconsistent with the "optimal cache spacing model" predicting that dispersal distance increases with seed abundance, however, A. peninsulae and T. sibiricus cached seeds further away under low acorn abundance. This suggests that caching effort represents a trade-off between the costs of transporting caches away from the seed source and the costs of distance-dependent cache loss (Clarkson, Eden, Sutherland, & Houston, 1986;Dally, Clayton, & Emery, 2006;Stapanian & Smith, 1978). Our results may also echo other studies that document that scatter-hoarding animals rapidly sequester the food near the food sources to cache when confronted with an ephemeral food supply (Jansen et al., 2004;Jenkins et al., 1995;Moore et al., 2007;Zhang, Steele, Zhang, Wei, & Yu, 2014). ...
... Many scatter-hoarding birds and mammals often modify their behavior in response to the presence of competitors or pilfering risks (Dally et al., 2006;Emery, Dally, & Clayton, 2004;Pravosudov & Lucas, 2000). Cache spacing is proposed to be one of the means by which scatter-hoarding animals protect cached food from pilferers or competitors (Bugnyar & Kotrschal, 2002;Clarkson et al., 1986;Dally, Emery, & Clayton, 2005;Stapanian & Smith, 1978. ...
... In addition, some acorns pilfered by T. sibiricus were excavated and re-cached by A. peninsulae, implying that A. peninsulae applied behavioral tactics to minimize cache pilferage, for example, reciprocal pilferage (Vander Wall & Jenkins, 2003). Scatter-hoarders may vary their consumption or caching strategy in response to the presence of food competitors (Dally et al., 2006;Hopewell et al., 2008). Therefore, cache pilferage by T. sibiricus seems not as damaging to them as it might because of reciprocal pilfering by A. peninsulae. ...
Seed caching and reciprocal cache pilferage play an important role in the coexistence of food‐hoarding animals. Understanding what affects seed caching and how cache pilferage occurs is an important question in seed dispersal ecology. However, tracking seed fate and cache pilferage presents substantial practical difficulties. Siberian chipmunks Tamias sibiricus always remove the entire pericarp when scatter‐hoarding acorns of Mongolian oak Quercus mongolica, whereas wood mice Apodemus peninsulae often store whole acorns in their caches. These differences in behavior provide an opportunity to investigate unilateral cache pilferage of T. sibiricus from A. peninsulae in response to seed abundance. In this study, tagged acorns were released at the peak and end periods of seed rain from Q. mongolica. This allowed us to investigate seed caching and unilateral cache pilferage at different seed abundances. We found that a higher proportion of acorns were cached at lower level of seed abundance (toward the end of seed rain), mainly because T. sibiricus rather than A. peninsulae scatter‐hoarded significantly more acorns at this time. Cache distances decreased with increasing seed abundance, indicating that acorns were cached further away and into smaller caches at lower seed abundance. Unexpectedly, unilateral cache pilferage by T. sibiricus was not significantly influenced by seed abundance—remaining at around 28% during both periods of high and low seed abundance.
... Cache loss due to pilferage by both inter-specifics and intra-specifics is an important evolutionary factor of food-hoarding behavior (Andersson & Krebs 1978;Dittel et al. 2017). In the cacher-pilferer arms race, both cachers and pilferers are sensitive to this antagonistic interaction and take precautions against opponents (Vander & Jenkins 2003;Dally et al. 2006;Grodzinski & Clayton 2010). ...
... Cache protection strategies in mammals and birds have been extensively studied (reviewed by Dally et al. 2006;Grodzinski & Clayton 2010). Food hoarders have shown one or more strategies that are not mutually exclusive to reduce cache loss when faced with the likelihood of pilferage. ...
... Cache protection strategies adopted by food hoarders often comprise ways to limit or invalidate the information that a potential pilferer has gathered (e.g. visual information and spatial memory; Grodzinski & Clayton 2010): for example (i) increasing scatter-hoarding, ceasing or delaying caching, and/or increasing cache vigilance to decrease probability of food loss (reviewed by Dally et al. 2006); (ii) caching food far away from the source to reduce competition and spacing caches to reduce density-dependent loss (Galvez et al. 2009;Zhang et al. 2014); (iii) making "false" caches to confuse potential pilferers at the time of caching (Steele et al. 2008); (iv) storing food in unfavorable places (e.g. out of tree canopy cover, open grassland or shrub edge) to avoid high rates of pilferage (Muñoz & Bonal 2011;Zhang et al. 2013;Steele et al. , 2015; (v) hiding food in secret places and repeatedly caching items to invalidate pilferers' sensory information while they are observed (Dally et al. 2004(Dally et al. , 2005; and/or (vi) concealing auditory information from potential pilferers (Stulp et al. 2009). ...
In the struggle for survival, scatter‐hoarding rodents are known to cache food and pilfer the caches of others. The extent to which rodents utilize auditory/visual cues from conspecifics to improve cache‐pilfering is unknown. Here, Siberian chipmunks (Tamias sibiricus) were allowed to search for caches of Corylus heterophylla seeds (man‐made caches and animal‐made caches) after experiencing cues from a conspecific’s cache‐searching events. For each type of cache, three experimental scenarios were presented: 1) alone (control), 2) auditory/visual (hearing and seeing conspecific’s cache‐searcing events) and 3) auditory only (hearing conspecific’s cache‐searcing events only) with random orders. The subjects located man‐made caches faster, harvested more caches, and hoarded more seeds both in the auditory/visual and the auditory only treatments compared to the control, while scatter‐hoarded more seeds in the auditory/visual treatment, but larder‐hoarded more seeds in the auditory only treatment. Compared to the control, the animals spent less time locating animal‐made caches, harvested more caches, ate less seeds, larder‐hoarded more seeds and hoarded more seeds in total both in the auditory/visual and the auditory only treatments, while ate more seeds and hoarded less seeds in total in the auditory only treatment than in the auditory/visual treatment. The results also show that females spent less time locating the animal‐made caches, but they scatter‐hoarded fewer seeds than males in the auditory/visual treatment. To our best knowledge, this is the first report that visual and/or auditory cues of conspecifics improve cache‐pilfering and hoarding in rodents.
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... Rooks (Corvus frugilegus) are a highly social and colonial corvid species Seed et al., 2007), often mating for life and returning to nesting sites yearly . In the wild they cache extensively, and recover caches accurately after months (Dally, Clayton, et al., 2006a;Källander, 2007). They exhibit complex social behaviors: social foraging (Dally et al., 2008;Jolles et al., 2013), third-party postconflict affiliation Seed et al., 2007), possibly recognizing their partners in video (Bird & Emery, 2008), and cooperate with conspecifics to solve string-pulling problems (but without evidence of understanding underlying causalities; Seed et al., 2008). ...
... The importance of considering social factors and individual repeatable patterns of behavior when conducting cognitive tests was underlined (Jolles et al., 2013; unfortunately the individual names of birds involved and the full hierarchy resulting from that study are not published). Likewise, the relative dominance of focal birds to their observers has been demonstrated to be a factor in caching: California scrub-jays protect their caches when observed by both dominant and subordinate conspecifics, but engage in higher levels of recaching when observed by dominant birds (Dally et al., 2005a, 2005b, Dally, Clayton et al., 2006a, Dally, Emery et al. 2006b; and Eurasian jays have been shown to cache more frequently in ground locations and to recache more often when observed by subordinate birds, but suppressed caching, cached more away from the ground, and further away from observer birds when these were dominant (Shaw & Clayton, 2012). ...
Piagetian object permanence (OP) refers to the ability to know that an object continues to exist when out of sight: In humans, it develops in six stages. Species of great apes, other mammals, and birds (parrots, corvids, and pigeons) have been shown to possess partial or full OP, which is a prerequisite for more complex physical cognition abilities they may possess. In birds, the greatest variation is in Stage 6 (invisible displacements) and in “A-not-B” errors—incorrectly persevering in searching an empty location rewarded previously. Caching abilities have been invoked as holding explanatory power over results in corvids, for which this error is sometimes completely absent. The rook ( Corvus frugilegus ), a cognitively advanced, social, caching corvid, has not yet been studied for OP. This study applies tasks of one OP scale commonly adapted for nonhuman animals, Uzgiris and Hunt’s Scale 1, as well as later-conceived tasks 16 and S, to a sample of adult, captive rooks. One rook demonstrated full OP (Stage 6b, multiple invisible displacements), whereas other individuals varied, attaining between Stages 5a (single visible displacements) and 6a (single invisible displacements). Like some corvids, a few made transient “A-not-B” errors. Behavioral considerations potentially underlying observed individual variation in results in rooks, including dominance, neophobia, past experiences, and individual idiosyncrasies, are examined. Rooks, like other corvids, possess well-developed OP abilities, and these results support the idea that exertion of executive control is required to avoid “A-not-B” errors, rather than caching abilities or developmental age, as previously suggested.
... When cached seeds are not retrieved, because the rodent dies or forgets the caching location, these dispersed seeds have an opportunity to germinate, marking a mutualistic benefit to the plant (Sawaya et al., 2018). Pilferage is a key step in this process in which animals locate and steal seeds from other individuals' caches (Dally et al., 2006;Vander Wall, 2000). Pilferers often recache the stolen seeds, which may then be pilfered by new individuals and can be moved to over 30 different caches by pilferers or recaching owners (Jansen et al., 2012;Vander Wall & Joyner, 1998), potentially resulting in compounded increased seed dispersal distance, or alternatively, increased likelihood of seed predation Cao et al., 2018;Jansen et al., 2012). ...
... When deer mouse abundance was higher, deer mice were more likely to locate caches, and when total small mammal abundance was higher, pilferage rates were higher across grids and sessions, in line with past research indicating density-dependent competition as a main determinant in pilferage rates (Dittel & Vander Wall, 2018), which may lead to increased immediate consumption of seeds and decreased benefit to the plant (Zwolak et al., 2023). Thus, a variety of pilferage avoidance strategies have evolved, including spatial memory techniques (Ribeiro & Vieira, 2016), active cache surveillance (Hirsch et al., 2013) and recaching seeds to safer locations (Vander Wall & Jenkins, 2003), which can significantly reduce pilferage while bolstering seed recovery by cache owners (Dally et al., 2006). ...
Small mammals such as mice and voles play a fundamental role in the ecosystem service of seed dispersal by caching seeds in small hoards that germinate under beneficial conditions. Pilferage is a critical step in this process in which animals steal seeds from other individuals' caches. Pilferers often recache stolen seeds, which are often pilfered by new individuals, who may recache again, and so on, potentially leading to compounded increased dispersal distance. However, little research has investigated intraspecific differences in pilfering frequency, despite its importance in better understanding the role of behavioural diversity in the valuable ecosystem service of seed dispersal.
We conducted a field experiment in Maine (USA) investigating how intraspecific variation, including personality, influences pilferage effectiveness.
Within the context of a long‐term capture‐mark‐recapture study, we measured the unique personality of 3311 individual small mammals of 10 species over a 7‐year period. For this experiment, we created artificial caches using eastern white pine ( Pinus strobus ) seeds monitored with trail cameras and buried antennas for individual identification.
Of the 436 caches created, 83.5% were pilfered by 10 species, including deer mice (( Peromyscus maniculatus ) and southern red‐backed voles ( Myodes gapperi ). We show how individuals differ in their ability to pilfer seeds and that these differences are driven by personality, body condition and sex. More exploratory deer mice and those with lower body condition were more likely to locate a cache, and female southern red‐backed voles were more likely than males to locate caches. Also, caches were more likely to be pilfered in areas of higher small mammal abundance.
Because the risk of pilferage drives decisions concerning where an animal chooses to store seeds, pilferage pressure is thought to drive the evolution of food‐hoarding behaviour. Our study shows that pilferage ability varies between individuals, meaning that some individuals have a disproportionately strong influence on others' caching decisions and disproportionately contribute to compounded longer‐distance seed dispersal facilitated by pilferage. Our results add to a growing body of knowledge showing that the unique personalities of individual small mammals play a critical role in forest regeneration by impacting seed dispersal.
... However, navigation is a rich behavior that includes both mnemonic and non-mnemonic spatial strategies. For example, an animal using memory to obtain a reward may also engage in opportunistic foraging, use memoryindependent search strategies, and exhibit spatial biases (Dally et al., 2006;Kamil and Roitblat, eLife digest Humans form new memories about what is happening in their lives every day. These autobiographical memories depend on a part of the brain called the hippocampus. ...
... Previous work has shown spatial biases in the wild. For example, individual birds can cache in different zones within a shared territory or on different parts of a tree (Cowie et al., 1981;Dally et al., 2006;Lahti et al., 1998). This strategy has a clear ethological advantage: biases reduce the memory load of cache locations, whereas choosing biases idiosyncratically minimizes unwanted overlap between individuals. ...
Animals use memory-guided and memory-independent strategies to make navigational decisions. Disentangling the contribution of these strategies to navigation is critical for understanding how memory influences behavioral output. To address this issue, we studied spatial behaviors of the chickadee, a food-caching bird. Chickadees hide food in concealed, scattered locations and retrieve their caches later in time. We designed an apparatus that allows birds to cache and retrieve food at many sites while navigating in a laboratory arena. This apparatus enabled automated tracking of behavioral variables - including caches, retrievals, and investigations of different sites. We built probabilistic models to fit these behavioral data using a combination of mnemonic and non-mnemonic factors. We found that chickadees use some navigational strategies that are independent of cache memories, including opportunistic foraging and spatial biases. They combine these strategies with spatially precise memories of which sites contain caches and which sites they have previously checked. A single memory of site contents is used in a context-dependent manner: during caching chickadees avoid sites that contain food, while during retrieval they instead preferentially access occupied sites. Our approach is a powerful way to investigate navigational decisions in a natural behavior, including flexible contributions of memory to these decisions.
... The advantages of banking food for future consumption are paired with the costs of pilfering by other animals (Andersson & Krebs, 1978;Lucas & Zielinski, 1998). Many corvids have evolved behaviors that minimize the ability of a competitor to pilfer their caches (see Dally et al., 2006 for a review). Several corvids either decrease, terminate, or delay the onset of caching when observed by a conspecific (e.g., ravens [Corvus corax], Bugnyar & Kotrschal, 2004;Heinrich & Pepper, 1998; Stellar's jays [Cyanocitta stelleri] Kalinowski et al., 2015). ...
... Social factors appear to be important in the evolution of the cognitive abilities of some corvids (Clayton et al., 2007) and may have contributed to the development of cache protection (Bugnyar & Kotrschal, 2002). Although it is clear that many social corvids such as the scrub jay engage in multiple cache protection strategies (Dally et al., 2006), researchers have recently explored to what extent less social corvids might also engage in cache protection. Clary and Kelly (2011) found that Clark's nutcrackers (Nucifraga columbiana) decreased the amount they cached when they had been observed by a conspecific and recovered more from more risky cache locations. ...
Previous work with corvids such as scrub jays (Aphelocoma californica) and ravens (Corvus corax) suggests that many social corvids alter their caching behavior when observed by conspecifics to protect their caches. We examined whether the Clark’s nutcracker (Nucifraga columbiana), an asocial corvid, can utilize a barrier to conceal its caching activities from a conspecific observer. Nutcrackers were allowed to cache nuts in a visible or concealed location in either the presence or absence of an observer. Nutcrackers were also given experience of having their caches pilfered. The nutcrackers cached significantly more nuts in the concealed compared to a visible location when observed. Importantly, nutcrackers also recovered a larger percentage of their nuts 24 hr later from a visible cache location but when the observer was no longer present. The results extend recent work suggesting that relatively nonsocial corvids, similar to their more social relatives, also engage in multiple forms of cache protection.
... The dispersal distance indirectly reflects the value of food resources to animals (Dally et al. 2006). In the present study, the dispersal distances were much longer for Quercus acorns in pine forests than those for Pinus seeds in oak forests, and the dispersal distance was mostly short in the dispersal prophase. ...
... In the present study, the dispersal distances were much longer for Quercus acorns in pine forests than those for Pinus seeds in oak forests, and the dispersal distance was mostly short in the dispersal prophase. These results conform with models that explain the evolution of rodent caching behavior based on the influence of the value of food resources, thereby predicting how rodents should distribute their caches to avoid cache pilferage (Vander Wall and Jenkins 2003;Dally et al. 2006). In simple terms, food with low nutritional value should be stored near the resource site, whereas food with high nutritional value is more likely to be cached away from the resource site to prevent it from being stolen by competitors. ...
Background
Seed dispersal by scatter-hoarding animals can affect the developmental dynamics of plant communities. However, how animals might participate in plant inter-community competition has rarely been investigated. Forest community junction is an area where the competition between plant communities is most prominent and animal activity is more frequent. At present, little is known about how scatter-hoarding animals might assist competitions by adjacent plant communities. Thus, for 3 years (2015–2017), we tracked the fate of 2880 tagged seeds ( Quercus aliena var. acuteserrata , Pinus tabuliformis , and P. armandii seed) placed near an edge where the forest composition changes from a pine forest to an oak forest in northwestern China.
Results
We found that the seed fates differed when Quercus and Pinus seeds entered adjacent stands. In contrast to Pinus seeds, acorns that entered pine forests were characterized by higher caching rates and longer dispersal distances. Pinus seeds had the highest probability of being predated (85%) by rodents, and eleven Q. aliena var. acuteserrata seedlings were established in pine forests, although none survived in the later stages. In addition, rodents exhibited obvious selectivity in terms of the microhabitats for the seed caching sites.
Conclusions
Seed fates differed when Quercus and Pinus seeds entered adjacent stands. The predation pressure by rodents on the seeds of Pinus species limited the germination of seeds and seedling establishment in oak forests. The different seed fates after their bidirectional dispersal could affect the differences in natural regeneration between pine and oak forests, and they might increase the recruitment rates for oak at the edge of an adjacent community. Rodent-mediated seed dispersal could potential unintentionally affect the competition between plant communities.
... Covering the carcass parts delayed the rate of consumption by invertebrates by more than five days, although this result should be taken with caution due to the limited sample size for the insect experiment. This implies that covering a carcass constitutes a very effective cache protection measure [13,31] for a large felid preying on ungulates in forested habitats. Our results are consistent with a similar study on mountain lion caching behavior in Arizona, which showed that simulated caching reduced wastage during dry and hot periods [21]. ...
... The lynxes in our study area, by comparison, were usually able to completely consume most of the meat on their kills over several days. This allows them to continue being roe deer specialists even when roe deer occur at low density [31], because even though there may be considerable search time expended in finding a prey, once killed it can provide food for many days. In turn, this can help explain why lynx presence has such a clear impact on low-density roe deer populations [32,33]. ...
Large solitary felids often kill large prey items that can provide multiple meals. However, being able to utilize these multiple meals requires that they can cache the meat in a manner that delays its discovery by vertebrate and invertebrate scavengers. Covering the kill with vegetation and snow is a commonly observed strategy among felids. This study investigates the utility of this strategy using observational data from Eurasian lynx (Lynx lynx)-killed roe deer (Capreolus capreolus) carcasses, and a set of two experiments focused on vertebrate and invertebrate scavengers, respectively. Lynx-killed roe deer that were covered by snow or vegetation were less likely to have been visited by scavengers. Experimentally-deployed video-monitored roe deer carcasses had significantly longer time prior to discovery by avian scavengers when covered with vegetation. Carcass parts placed in cages that excluded vertebrate scavengers had delayed invertebrate activity when covered with vegetation. All three datasets indicated that covering a kill was a successful caching/anti-scavenger strategy. These results can help explain why lynx functional responses reach plateaus at relatively low kill rates. The success of this anti-scavenging behavior therefore has clear effects on the dynamics of a predator-prey system.
... Scatter hoarding allows the hoarder to manage its own caches and to reduce excessive losses from pilfering (the removal of food items by an individual other than the storer; Vander Wall & Jenkins, 2003), but requires mechanisms to relocate the large number of widely spread food items (Dally, Clayton, & Emery, 2006). Many rodents are scatter-hoarders, and olfaction plays a pivotal role in their detection of food (Vander Wall, 2003, 2005, Thayer & Vander Wall, 2005Dally et al., 2006;Zhang & Zhang, 2007;Hollander, Vander Wall, & Longland, 2012;Yi, Wang, Zhang, & Zhang, 2016;Niu, Chu, Yi, & Zhang, 2018). ...
... Scatter hoarding allows the hoarder to manage its own caches and to reduce excessive losses from pilfering (the removal of food items by an individual other than the storer; Vander Wall & Jenkins, 2003), but requires mechanisms to relocate the large number of widely spread food items (Dally, Clayton, & Emery, 2006). Many rodents are scatter-hoarders, and olfaction plays a pivotal role in their detection of food (Vander Wall, 2003, 2005, Thayer & Vander Wall, 2005Dally et al., 2006;Zhang & Zhang, 2007;Hollander, Vander Wall, & Longland, 2012;Yi, Wang, Zhang, & Zhang, 2016;Niu, Chu, Yi, & Zhang, 2018). Birds from the family Corvidae are another important group of scatter-hoarders (G omez et al., 2018;Pessendorfer et al., 2016). ...
The sense of olfaction has been traditionally considered of low relevance in bird biology. In particular, the location of cached seeds by scatter-hoarder corvids is assumed to depend on spatial memory, whereas no study has demonstrated the use of olfaction to detect these seeds. In this study we tested whether olfaction might play a role in the precise location of cached nuts by magpies, Pica pica, a scatter-hoarder corvid species. We conducted an experiment under natural conditions where nuts belonging to four treatments were buried, simulating natural caches, and we monitored the rate of nut detection by magpies. Three of the treatments included nuts with natural odour or odour of a strong-smelling substance (untreated nuts, nutshells filled with soil and nuts soaked in diesel), whereas the fourth treatment consisted of 3D-printed fake nuts made of polypropylene. The experiment was replicated in two sites and in several breeding territories, using a total of 624 nuts. Motion-activated cameras were installed to identify the animals foraging in the plots. The results show that magpies detected untreated nuts, nutshells or nuts soaked in diesel ca. three times more than 3D-printed fake nuts. Among detected and unburied nuts, the 3D-printed nuts were largely abandoned on site, followed by nutshells without a kernel, natural nuts and nuts soaked in diesel. All this strongly supports the hypothesis that magpies use olfaction to pinpoint cached nuts, either for nut recovery or pilfering, but once a nut is detected they may use other senses such as vision or touch for selection. Given the strong changes in landscape features that may occur under natural conditions between the time of nut caching and nut retrieval, we suggest that the use of olfaction might be crucial to help spatial memory in determining the location of cached nuts in corvids.
... Some of this advantage can be a simple consequence of distribution of home ranges (as long as they do not overlap completely) but it also depends on the ability of scatterhoarders to remember cache sites (Gu, Zhao, & Zhang, 2017;Vander Wall, 2000;Wang, Zhang, Wang, & Yi, 2018). Pilferers, on the other hand, observe caching animals (documented mostly in corvids: Shaw & Clayton, 2014) or detect caches by searching at random or in response to scent cues (documented mostly in rodents: Dally, Clayton, & Emery, 2006). A recent study on Siberian chipmunks Tamias sibiricus suggested that ability to remember one's own caches versus detect caches made by other animals trades off among individuals (Yi, Wang, Zhang, & Zhang, 2016). ...
... Given the ubiquity of cache pilferage Vander Wall & Jenkins, 2003), it is not surprising that caching animals evolved strategies to reduce cache pilferage (reviewed in Dally et al., 2006). These strategies include caching in risky (usually open) habitats, where potential pilferers are less likely to venture (Muñoz & Bonal, 2011;Steele et al., 2014). ...
Consistent individual tendencies in behaviour, or behavioural types, are likely to impact the dynamics and outcomes of animal‐mediated seed dispersal. We review the extant literature on this issue and outline a conceptual overview to guide this emerging field. We provide an overview of possible ways in which behavioural types can affect animal‐mediated seed dispersal. We summarize theoretical mechanisms linking behavioural types with seed dispersal outcomes and review how behavioural types might affect each stage of seed dispersal, beginning with fruit encounter and harvest, and ending with events that take place after seed deposition.
Since behavioural types involve correlations among different behaviours (i.e. behavioural syndromes), they can generate unexpected associations between different decisions that are involved in seed dispersal, with conflicting (or reinforcing) effects on different stages of seed dispersal. Thus, we draw particular attention to trade‐offs faced by seeds dispersed by individuals with different behavioural tendencies. We also note that since seed dispersal is a multiplicative process with different stages, disperser behavioural types that provide moderately efficient dispersal at each stage will be better for plants than behavioural types that are very efficient at some steps, but inefficient on others. Finally, we provide testable predictions on the links between behavioural types and characteristics of seed dispersal, including, for example, influences on the probability of seed harvest, dispersal distance, deposition sites and condition of dispersed seeds.
We argue that investigating the links between behavioural types and animal‐mediated seed dispersal will provide a better mechanistic understanding of seed dispersal and plant regeneration.
A free plain language summary can be found within the Supporting Information of this article.
... observer). Indeed, corvids react to what others can and cannot see while caching and manipulating food or objects (Bugnyar, 2011;Bugnyar et al., 2016;Dally et al., 2006;Emery & Clayton, 2002). ...
... Moreover, there is a lot of evidence of behaviour in non-human animals that looks as though it is evidence of MTT. Scrub-jays tend to re-cache food if their caching activity is observed by a dominant bird [21], but only re-cache in these situations if the bird itself has previously stolen food from another bird's cache [22]. The scrub-jays' food-caching behaviour is evidence that they can recollect what was cached, where it was cached and when it was cached, and use this information in a flexible and variable manner (e.g. ...
While many aspects of cognition have been shown to be shared between humans and non-human animals, there remains controversy regarding whether the capacity to mentally time travel is a uniquely human one. In this paper, we argue that there are four ways of representing when some event happened: four kinds of temporal representation. Distinguishing these four kinds of temporal representation has five benefits. First, it puts us in a position to determine the particular benefits these distinct temporal representations afford an organism. Second, it provides the conceptual resources to foster a discussion about which of these representations is necessary for an organism to count as having the capacity to mentally time travel. Third, it enables us to distinguish stricter from more liberal views of mental time travel that differ regarding which kind(s) of temporal representation is taken to be necessary for mental time travel. Fourth, it allows us to determine the benefits of taking a stricter or more liberal view of mental time travel. Finally, it ensures that disagreement about whether some species can mentally time travel is not merely the product of unrecognized disagreement about which temporal representation is necessary for mental time travel. We argue for a more liberal view, on the grounds that it allows us to view mental time travel as an evolutionarily continuous phenomenon and to recognize that differences in the ways that organisms mentally time travel might reflect different temporal representations, or combinations thereof, that they employ. Our ultimate aim, however, is to create a conceptual framework for further discussion regarding what sorts of temporal representations are required for mental time travel.
This article is part of the theme issue ‘Elements of episodic memory: lessons from 40 years of research’.
... Cache location on tree trunks, cache concealment with bark, and cache duration (<14 days) were consistent with findings for other fruits from elsewhere (Strickland and Ouellet 2020;Swift et al. 2022). Caching behaviour of Canada Jays is influenced by the potential for their caches to be pilfered by other resident species during periods of food scarcity (Dally et al. 2006), thus their need to spread caches widely, place them above ground in obscure sites and sometimes conceal them, which helps reduce the total amount of cached food lost if a few caches are pirated. Our observations of three Canada Jays openly caching in close proximity to each other are consistent with those of Burnell and Tomback (1985), who suggest cache pilferage is more likely by individuals of other species rather than conspecifics. ...
... Like several other corvids, they can also mimic other sounds, including anecdotal evidence of human voice mimicry [41,43,47] (N.S.C. and V.D., personal observations). Rooks also show longterm vocal recognition of conspecifics, have excellent learning, memory and planning skills, and more generally show good socio-cognitive skills [40,48,49]. They also appear to have the same song-related neural circuits as other oscines [50]. ...
Vocal communication is widespread in animals, with vocal repertoires of varying complexity. The social complexity hypothesis predicts that species may need high vocal complexity to deal with complex social organization (e.g. have a variety of different interindividual relations). We quantified the vocal complexity of two geographically distant captive colonies of rooks, a corvid species with complex social organization and cognitive performances, but understudied vocal abilities. We quantified the diversity and gradation of their repertoire, as well as the inter-individual similarity at the vocal unit level. We found that males produced call units with lower diversity and gradation than females, while song units did not differ between sexes. Surprisingly, while females produced highly similar call repertoires, even between colonies, each individual male produced almost completely different call repertoires from any other individual. These findings question the way male rooks communicate with their social partners. We suggest that each male may actively seek to remain vocally distinct, which could be an asset in their frequently changing social environment. We conclude that inter-individual similarity, an understudied aspect of vocal repertoires, should also be considered as a measure of vocal complexity.
... Some birds and mammals change their caching behaviour with the aim to minimise the stealing risk (Dally et al. 2006). Nevertheless, the response of grey squirrels did not seem to be consistent. ...
Squirrels and some corvids have successfully adapted to urban conditions. Their populations are often more abundant in city parks than in rural areas. These species may compete, especially in terms of food resources. We studied interactions between corvids (hooded crows and rooks) and red squirrels inhabiting urban park, mostly in relation to supplementary food utilisation in Poland. The study included the following: (a) feeding trials, when squirrels were offered hazelnuts and all stealing attempts by other animals were noted; (b) direct observations of groups of animals (at least one squirrel and one corvid species) with all behaviours being recorded. During the feeding trial, and with constant corvid presence, corvids tried to steal almost every third nut cached by squirrels. Regardless of the season, the share of nuts that corvids tried to steal was similar. When the feeding trial proceeded, more squirrels joined in order to obtain food. On the contrary, the presence of corvids seemed to refrain other corvids from joining the trial. The presence of a bird/squirrel audience did not result in more deceptive caches. During direct observations, squirrels interacted mostly with corvids, and less often with people or other squirrels. The most frequent interaction of squirrels with other animals was flight and chasing away; for corvids, it was chasing and following or attempting to steal food. Overall, we showed that corvids can be food competitors and kleptoparasites for red squirrels. Red squirrels, with whom people often have affinity relationships, benefited from direct supplementary feeding. Corvids, in turn, learnt to follow red squirrels to steal human-delivered nuts.
... Environmental factors affect use (and hence the benefits) of stored food for species that rely on hoarding. For example, though most scatterhoarding species rely on memory to find their own hoarded food (Lavenex et al. 1998), they do use olfaction to locate and steal food hoarded by others (Vander Wall 1991;Dally et al. 2006), and environmental conditions can influence these senses. For example, yellow pine chipmunks (Tamias amoenus Allen, 1980) are able to find and pilfer more seeds when seeds and soils are wet, while dry conditions greatly hinder the use of olfaction to locate seeds in other scatterhoarders (Vander Wall 1991, 2000. ...
Scatterhoarder responses to factors that influence stored food (i.e., flooding) is important given the strong reliance on hoarded food for survival. We examined how eastern gray squirrels (Sciurus carolinensis, Gmelin 1778) have adapted to a seasonally flooded ecosystem in Alabama. Our study area was dry September–November and flooded the rest of the year. We predicted squirrels would respond to flooding by storing food in areas that stay dry during winter, seasonally shifting to dry habitat, or decreasing the amount of hard mast in their winter diet. We also examined previously reported survival differences between the dry and flooded seasons. During the dry season, 72% of acorns were buried in areas that later flooded. Habitat use did not change significantly during the flooded and dry seasons; however, squirrels used habitat that stayed dry during flooding to a greater degree during non-flood seasons. The amount of hard mast in the diet did not change significantly between the dry and flooded seasons. However, squirrels were more likely to die during the flooded season (P = 0.02). We did not find any behavioral adaptations to seasonal flooding. Further research is needed to fully understand the effects of fluctuating environmental conditions on scatterhoarders.
... We also showed that travelling time was longer in walnuts than in acorns, which could be caused by three possibilities. First, squirrels could exhibit deceptive behaviour when they store walnuts; some scatter-hoarding animals store inedible food or create an empty cache to deceive other individuals (Heinrich, 1999;Dally et al., 2006;Steele et al., 2008). In our study site, supplemental feeding for squirrels was common; thus, the density of squirrels is higher than that in natural conditions. ...
Scatter-hoarding animals decide their food hoarding location by assessing food quality and pilfering risk. Previous studies have proposed two non-mutually exclusive hypotheses; the optimal density model (ODM) and the habitat structure hypothesis (HSH). The ODM proposes that animals utilize low cache density to protect their valuable caches by transporting food far from food sources. The HSH proposes that animals utilize predation risk to protect their valuable caches by hoarding food in open areas. Here, we investigated the hoarding behaviours in Eurasian red squirrels Sciurus vulgaris by experimentally providing high-quality (walnuts) and low-quality (acorns) food, to examine if they follow ODM or HSH. Compared to acorns, squirrels hoarded walnuts in places further from the area where food was provisioned and in areas with low canopy cover. These results agree with both ODM and HSH, providing the first evidence that hoarding behaviour in Eurasian red squirrels is shaped by multiple factors.
... For example, seed predator identity and size affect foraging decisions in many ant, bird, and mammal seed predator guilds (Mares and Rosenzweig 1978;Kelt et al. 2004). By excluding conspeci c and heterospeci c subordinates from accessing high-quality seed patches, large territorial seed predators can create dominance hierarchies in their foraging communities (Dally et al. 2006;Tsuji et al. 2020), signi cantly in uencing variation in seed predation (Manson and Stiles 1998;Garrote et al. 2019). The spatial distribution of seeds within an area can also affect foraging decisions. ...
Multiple factors affect seed predation, including seed traits, habitat type, seed predator community composition, predation risk, and seasonality. How all these factors and their interactions simultaneously influence seed predation has rarely been tested experimentally in situ. Here, we assessed the relative contribution of the factors driving seed predation in an African savanna rodent community, comprising six ecologically similar species. We first conducted seed preference tests under semicaptive conditions to determine which seed trait (size, shell hardness, nutritional content) influenced seed predation. Then we performed in situ experiments to establish whether rodent community composition (diversity and abundance), seed type, habitat type, seasonality, predation risk, and their interactions affected seed predation. Semicaptive experiments showed that rodents preferred smaller, lighter seeds, containing relatively high water content. In situ experiments showed that predation risk was an important factor influencing seed predation, with rodents removing considerably more seeds in areas where predation risk was lower. Habitat type also affected seed predation, but its effects were strongly linked to predation risk. In areas where predation risk was higher, rodents removed more seeds in more heterogeneous habitats, whereas in areas where predation risk was lower, rodents removed more seeds in less heterogeneous habitats. Seasonality was the least influential factor shaping seed predation. Rodents removed more seeds in winter compared to other seasons, but only in areas where predation risk was low. We provide experimental evidence for a multifaceted approach to understanding the relative contribution of the different factors driving variation in seed predation in natural communities and show that these factors are likely hierarchically arranged.
... First, the cache owner can retrieve the seed for consumption, which was why it had been cached in the first place. However, rates of seed removal from a cache (henceforth referred to as 'cache removal') are usually higher than actual rates of seed predation as seeds tend to be moved around from one cache to another (Vander Wall and Jenkins 2003, Dally et al. 2006, Zamora Guttierez 2010. Therefore, cache removal can also be the result of an owner that rapidly sequestered fresh seeds in the past and then returns to the caches to relocate the seeds (Jenkins and Peters 1992). ...
... Leopard seals that hunt under the ice rely on memory to find their way back to their breathing holes. Food-storing animals such as woodpeckers, jays, hamsters, and squirrels, hide food in times of abundance and rely on memory to recover their caches, perhaps several months later when the ground is covered with snow [33]. The trace map is a heat map that covers the same area as the perception map and represents the agent's most recent positions. ...
Ecosystem models can be used for understanding general phenomena of evolution, ecology, and ethology. They can also be used for analyzing and predicting the ecological consequences of human activities on specific ecosystems, e.g., the effects of agriculture, forestry, construction, hunting, and fishing. We argue that powerful ecosystem models need to include reasonable models of the physical environment and of animal behavior. We also argue that several well-known ecosystem models are unsatisfactory in this regard. Then we present the open-source ecosystem simulator Ecotwin, which is built on top of the game engine Unity. To model a specific ecosystem in Ecotwin, we first generate a 3D Unity model of the physical environment, based on topographic or bathymetric data. Then we insert digital 3D models of the organisms of interest into the environment model. Each organism is equipped with a genome and capable of sexual or asexual reproduction. An organism dies if it runs out of some vital resource or reaches its maximum age. The animal models are equipped with behavioral models that include sensors, actions, reward signals, and mechanisms of learning and decision-making. Finally, we illustrate how Ecotwin works by building and running one terrestrial and one marine ecosystem model.
... Conifer species, specifically spruce trees, preserve cached perishable food better than other tree species (Sechley et al., 2015;Strickland et al., 2011). Additionally, as Canada jays' caches are most at risk from acute pilferage at the time of caching (Burnell & Tomback, 1985;Rutter, 1972), caching amongst an abundance of branches (and needles) may help to disguise the location of caches (broadly reviewed in Dally et al., 2006). Whilst the forest composition of territories jays inhabit has long been assumed to be related to food-caching preferences, our results provide a key empirical link showing that Canada jays do indeed prefer to cache in tree species most suitable for long-term cache preservation. ...
Food caching is a foraging strategy used by many vertebrates, involving the storage and subsequent recovery of food items for later consumption, when other food sources are scarce. Once cached, stored food, particularly highly perishable items, can degrade over time. Evidence suggests that for birds, some conifers may aid in cache preservation through protective properties in resin. However, due to the challenges involved with following birds to their caching locations, cache‐site preferences are not easily studied in the wild. We investigated eight captive Canada jays’ (Perisoreus canadensis) ability to both identify and exploit conifer tree species. Further, we examined potential cues that birds may use to identify and select these potentially beneficial sites. We found strong evidence to suggest that birds can quickly identify conifer tree species and subsequently exploit those cache locations preferentially. Furthermore, our evidence suggests that although birds do not appear to use olfactory cues when making caching decisions, they potentially to attend to structural cues. We suggest that visual information is essential to both the identification of conifer trees and to cache‐site selection decisions. These findings indicate that jays make rapid, fine scale assessments of their environments, discriminating amongst trees of different species and use this information to select cache‐sites. Canada jays quickly identify beneficial tree species for caching (A). Once identified, Canada jays disproportionally perch (B) and cache (C‐E) in these trees when compared to trees that are not considered beneficial. These findings indicate that jays make rapid, fine scale assessments of their environments, discriminating amongst trees of different species and use this information to select cache‐sites.
... Among corvids, conspecific caches may be stolen through random searches or observational recall, though in Clark's Nutcrackers, recall wanes after only 48 h (Kamil and Balda 1985;Bednekoff and Balda 1996;Bugnyar and Kotrschal 2002). Among other social hoarders such as tits and chickadees, or solitary hoarders with overlapping home ranges like many rodents, conspecific cache theft is thought to be tolerated because it is ultimately reciprocal (Vander Wall and Jenkins 2003;Dally et al. 2006;Dittel et al. 2017). We found that the majority of stolen caches (60%) were taken by heterospecifics, namely northern red-backed voles, which have been recently documented to climb trees (Nations and Olson 2015). ...
Arctic and subarctic wildlife are among the most vulnerable species to climate change. Canada Jays (Perisoreus canadensis (Linnaeus, 1776)) are generalist residents of northern boreal forests and scatter-hoard food to insulate against food scarcity during winter. Unlike most scatter-hoarders, however, Canada Jays primarily cache perishable food, rendering their caches more susceptible to climate change induced degradation and loss. Here we use a mostly noninvasive approach to document Canada Jay foraging ecology among a population in interior Alaska, USA, including the types of food acquired, foraging and caching rates, and cache longevity and loss. We also tested for associations between foraging and caching rates with reproductive metrics to assess possible relationships among food and productivity. We found that Canada Jays have a varied diet that changed seasonally, and responded to a record-setting warm spring by directing foraging efforts away from cache recovery and towards the emergence of fresh food. We did not find evidence for relationships between foraging and caching rate with reproductive output, possibly owing to small sample sizes. We found that caches were recovered quickly (<4 weeks) and frequently lost to conspecific and heterospecific competitors. Our study suggests that Canada Jays may be better poised to respond to changes in cache integrity and food availability than has been previously recognized.
... As a corollary, individuals should invest in their pilfering tactics rather than in theft-reducing strategies (but see e.g. [32][33][34][35][36][37][38] for examples of potentially costly behaviours aimed to reduce pilferage). ...
Many plant species worldwide are dispersed by scatter-hoarding granivores: animals that hide seeds in numerous, small caches for future consumption. Yet, the evolution of scatter-hoarding is difficult to explain because undefended caches are at high risk of pilferage. Previous models have attempted to solve this problem by giving cache owners large advantages in cache recovery, by kin selection, or by introducing reciprocal pilferage of ‘shared’ seed resources. However, the role of environmental variability has been so far overlooked in this context. One important form of such variability is masting, which is displayed by many plant species dispersed by scatterhoarders. We use a mathematical model to investigate the influence of masting on the evolution of scatter-hoarding. The model accounts for periodically varying annual seed fall, caching and pilfering behaviour, and the demography of scatterhoarders. The parameter values are based mostly on research on European beech ( Fagus sylvatica ) and yellow-necked mice ( Apodemus flavicollis ). Starvation of scatterhoarders between mast years decreases the population density that enters masting events, which leads to reduced seed pilferage. Satiation of scatterhoarders during mast events lowers the reproductive cost of caching (i.e. the cost of caching for the future rather than using seeds for current reproduction). These reductions promote the evolution of scatter-hoarding behaviour especially when interannual variation in seed fall and the period between masting events are large.
This article is part of the theme issue ‘The ecology and evolution of synchronized seed production in plants’.
... It has been demonstrated that obtaining food as a producer can require individuals to learn to acquire or process food in novel ways (Laland & Reader, 1999;Ramsey et al., 2007;Reader & Laland, 2001). In contrast, cognitive mechanisms of scrounging behaviour have received less attention, except perhaps in the specific context of cache pilfering (Dally et al., 2006). ...
The producer–scrounger game is a key element of foraging ecology in many systems. Producing and scrounging typically covary negatively, but partitioning this covariance into contributions of individual plasticity and consistent between individual differences is key to understanding population‐level consequences of foraging strategies. Furthermore, little is known about the role cognition plays in the producer–scrounger game.
We investigated the role of cognition in these alternative foraging tactics in wild mixed‐species flocks of great tits and blue tits, using a production learning task in which we measured individuals’ speed of learning to visit the single feeder in an array that would provide them with a food reward. We also quantified the proportion of individuals’ feeds that were scrounges (‘proportion scrounged’); scrounging was possible if individuals visited immediately after a previous rewarded visitor. Three learning experiments—initial and two reversal learning—enabled us to estimate the repeatability and covariance of each foraging behaviour.
First, we examined whether individuals learned to improve their scrounging success (i.e. whether they obtained food by scrounging when there was an opportunity to do so). Second, we quantified the repeatability of proportion scrounged, and asked whether proportion scrounged affected production learning speed among individuals. Third, we used multivariate analyses to partition within‐ and among‐individual components of covariance between proportion scrounged and production learning speed.
Individuals improved their scrounging success over time. Birds with a greater proportion scrounged took longer to learn their own rewarding feeder. Although multivariate analyses showed that covariance between proportion scrounged and learning speed was driven primarily by within‐individual variation, that is, by behavioural plasticity, among‐individual differences also played a role for blue tits.
This is the first demonstration of a cognitive trait influencing producing and scrounging in the same wild system, highlighting the importance of cognition in the use of alternative resource acquisition tactics. The results of our covariance analyses suggest the potential for genetic differences in allocation to alternative foraging tactics, which are likely species‐ and system‐dependent. They also point to the need to control for different foraging tactics when studying individual cognition in the wild.
... [18,19]). Many such species are highly social, but information about cache locations is usually guarded from group members via behavioural strategies [20,21]. Food caches are not the only food available to these species, as they can continuously forage and even continue to cache throughout the year. ...
Social learning is a primary mechanism for information acquisition in social species. Despite many benefits, social learning may be disadvantageous when independent learning is more efficient. For example, searching independently may be more advantageous when food sources are ephemeral and unpredictable. Individual differences in cognitive abilities can also be expected to influence social information use. Specifically, better spatial memory can make a given environment more predictable for an individual by allowing it to better track food sources. We investigated how resident food-caching chickadees discovered multiple novel food sources in both harsher, less predictable high elevation and milder, more predictable low elevation winter environments. Chickadees at high elevation were faster at discovering multiple novel food sources and discovered more food sources than birds at low elevation. While birds at both elevations used social information, the contribution of social learning to food discovery was significantly lower at high elevation. At both elevations, chickadees with better spatial cognitive flexibility were slower at discovering food sources, likely because birds with lower spatial cognitive flexibility are worse at tracking natural resources and therefore spend more time exploring. Overall, our study supported the prediction that harsh environments should favour less reliance on social learning.
... Corvids often hide food to consume it in the future, and this posits a risk of it being pilfered, especially in species that forage in large social groups. Indeed, cacheprotection strategies employed by some corvid species have evolved to protect their food from a potential pilferer (Dally, Clayton, & Emery, 2006a). The decision to protect the food is dependent on whether the conspecific is present or absent (Emery & Clayton, 2001). ...
Pioneering research on avian behaviour and cognitive neuroscience have highlighted that avian species, mainly corvids and parrots, have a cognitive tool kit comparable with apes and other large-brained mammals, despite conspicuous differences in their neuroarchitecture. This cognitive tool kit is driven by convergent evolution, and consists of complex processes such as casual reasoning, behavioural flexibility, imagination, and prospection. Here, we review experimental studies in corvids and parrots that tested complex cognitive processes within this tool kit. We then provide experimental examples for the potential involvement of metacognitive skills in the expression of the cognitive tool kit. We further expand the discussion of cognitive and metacognitive abilities in avian species, suggesting that an integrated assessment of these processes, together with revised and multiple tasks of mirror self-recognition, might shed light on one of the most highly debated topics in the literature—self-awareness in animals. Comparing the use of multiple assessments of self-awareness within species and across taxa will provide a more informative, richer picture of the level of consciousness in different organisms.
... In addition to their own caches, some corvid species also remember and later pilfer the caches of conspecifics [3,4]. This led to the development of sophisticated cache protection strategies that again rely on flexible spatial cognition [5]. Corvids are also known to flexibly update their spatial memory: they switch from recovering perishable to non-perishable food after longer delays between caching and recovery [6], thus integrating information about the decay progress of caches [7]. ...
Birds are renowned for their excellent spatial cognition. Corvid songbirds, in particular, rely on explicit representation of spatial cues in memory when caching food and retrieving caches for later consumption. However, the neuronal correlates of flexible spatial memory abilities are largely unknown in birds. We therefore trained carrion crows (Corvus corone) on a spatial delayed-response task in which they had to maintain the variable location of a visual item for a few seconds in working memory. After the crows performed this task with high precision, we recorded single-cell activity from the associative endbrain area Nidopallium caudolaterale (NCL) in the behaving crows. A large fraction of NCL neurons were tuned to individual preferred locations and selectively maintained the spatial location of items in working memory. A comparison of firing rates with reaction times suggested that the majority of delay-selective neurons represented stored location information rather than motor preparation. Almost 30% of all recorded neurons were tuned during both visual presentation and memory delay, and their spatial tuning was significantly correlated. The population of recorded neurons stably maintained spatial information over the course of the working memory period. Importantly, the neural responses of spatially tuned neurons were relevant for the crows' choices and allowed a statistical classifier to predict the subsequently chosen target location in free-choice trials. Our findings demonstrate the pivotal role of the avian NCL in spatial working memory that is reminiscent of the function of the convergently evolved primate prefrontal cortex in spatial working memory.
... Yet, many species of scatter-hoarding animals put considerable effort in behaviors apparently 76 aimed to reduce pilferage (Dally et al. 2006a). This phenomenon has been particularly well-studied in 77 corvids (e.g. ...
Many plant species worldwide are dispersed by scatterhoarding granivores: animals that hide seeds in numerous, small caches for future consumption. Yet, the evolution of scatterhoarding is difficult to explain because undefended caches are at high risk of pilferage. Previous models have attempted to solve this problem by giving cache owners unrealistically large advantages in cache recovery, by kin selection (but individuals that cache and those that pilfer are usually unrelated), or by introducing reciprocal pilferage of "shared" seed resources. However, the role of environmental variability has been so far overlooked in this context. One important form of such variability is masting, which is displayed by many plant species dispersed by scatterhoarders. We use a mathematical model to investigate the influence of masting on the evolution of scatter-hoarding. The model accounts for periodically varying annual seed fall, caching and pilfering behavior, and the demography of scatterhoarders. Masting, through its effects on population density, reduces cache pilferage and lowers the reproductive cost of caching (i.e. the cost of caching for the future rather than using seeds for current reproduction). These reductions promote the evolution of scatter-hoarding behavior especially when interannual variation in seed fall and the period between masting events are high.
Animals that experience a food-scarce season can supplement their diet by scatterhoarding, or burying food around their home range, and then retrieving and consuming those food items at a later date. Theft, or pilferage, is considered the greatest risk to stored food; yet little is known about the pilferage risk of different types of seeds. We investigated the long-term relative pilferage risk of 793 artificially scatterhoarded seeds (Mockernut Hickory, Carya tomentosa (Lam. Ex Poir.) Nutt.; American Beech, Fagus grandifolia Ehrh.; White Oak, Quercus alba L.; Water Oak, Quercus nigra L.) buried in Alabama from October 2020 to February 2021 and exposed to hoarding populations of eastern gray squirrels (Sciurus carolinensis Gmelin, 1788) and eastern chipmunks (Tamias striatus (L., 1758)). We found evidence that animals can selectively pilfer whole, dormant seeds and whole seeds were pilfered more rapidly than those with excised embryos. Whole Water Oak acorns were more likely to be pilfered than all other seed types. All seeds had a combined pilferage risk of 0.98 over 182 days, and the risks for individual seed types were all greater than 0.97. Our findings indicate the importance of pilferage reduction strategies documented in hoarding species and may indicate an advantage to having a diverse supply of hoarded foods that include lower-value seeds with lower pilferage risk.
The overarching goal of neurobiology is to understand how complex behaviors are generated by the nervous system. The behavior of each species, and the brain that controls it, is shaped by the historical and current state of the environment that they inhabit. This fact is juxtaposed with the reductionist approach of neuroscience that isolates animals from their natural environment. Understanding how brains evolved to orchestrate the myriads of natural behaviors an animal performs in response to its environment requires an integrative approach to neuroscience that considers ecology, ethology, and evolution. Current technological developments are leading us to an inflection point at which studying brain functions in the wild is now possible. Ecological studies on how the environment affects behavior of animals (i.e., hibernation, foraging, food hoarding, and nest building) have framed a plurality of questions to be answered mechanistically, and yet, only few studies have addressed the relationship between the environment and the brain's anatomy and physiology. Neuroscience needs new animal models that allow us to tackle such questions in the wild. Here, we propose a new animal model for wild neuroscience, the agouti ( Dasyprocta spp.), a large wild rodent playing a critical seasonal role in the maintenance of the central and south American rainforest ecosystems. We focus on how a rodent model, like the agouti, will allow for the investigation of large‐scale brain dynamics during seasonal behaviors of ecological importance: scatter‐hoarding and retrieval. We describe agouti evolution, ecology, and physiology as well as neuro‐anatomical and neurophysiological studies, which have set the foundation for future neuroscience in natura. We suggest agoutis have the potential to be a groundbreaking model for wild neuroscience.
Long-term memory affects animal fitness, especially in social species. In these species, the memory of group members facilitates the acquisition of novel foraging skills through social learning when naïve individuals observe and imitate the successful foraging behavior. Long-term memory and social learning also provide the framework for cultural behavior, a trait found in humans but very few other animal species. In birds, little is known about the duration of long-term memories for complex foraging skills, or the impact of long-term memory on group members. We tested whether wild jays remembered a complex foraging task more than 3 years after their initial experience and quantified the effect of this memory on naïve jay behavior. Experienced jays remembered how to solve the task and their behavior had significant positive effects on interactions by naïve group members at the task. This suggests that natural selection may favor long-term memory of solutions to foraging problems to facilitate the persistence of foraging skills that are specifically useful in the local environment in social birds with long lifespans and overlapping generations.
This handbook lays out the science behind how animals think, remember, create, calculate, and remember. It provides concise overviews on major areas of study such as animal communication and language, memory and recall, social cognition, social learning and teaching, numerical and quantitative abilities, as well as innovation and problem solving. The chapters also explore more nuanced topics in greater detail, showing how the research was conducted and how it can be used for further study. The authors range from academics working in renowned university departments to those from research institutions and practitioners in zoos. The volume encompasses a wide variety of species, ensuring the breadth of the field is explored.
In previous studies, authors have demonstrated the benefits of rodent participation in the colonization process carried out by oak species. We have observed that certain rodent species (Apodemus sylvaticus and Mus spretus) partially consume acorns, beginning at the basal part and preserving the embryo. Perea et al. (2011) and Yang and Yi (2012) found that during periods of abundance the remains produced after partial consumption are left on the surface without being transported to caches because they see as leftovers.
The objective of this study is to know the role played by the remains of partially consumed acorns in the caches. To verify if these remains are seen as offal and are therefore rejected. To test this, we provided rodents with intact, partially eaten acorns to ascertain their preferences for own or foreign remains or the rejection of both. The results indicate that preferences are directed towards consuming first the remains produced by other rodents, then their own, leaving intact acorns for last. The reasons are based on questions of energy balance. Removing the shells from acorns is very costly in terms of energy, so it is preferable to use the shelled remains first, even if they must pass through a layer of fungi and molds to reach the cotyledons. The first remains to be consumed are those of others, because in case of scarcity it is convenient to conserve one's own resources.
Underlying social learning and other important aspects of successful adaptation to social life is social awareness, where individuals are required to pay attention and respond flexibly to others in their environment. We tested the influence of social context (alone, affiliate, non-affiliate, heterospecific) on behavioural interactions (manipulation, caching, head & body out of sight i.e. barrier use) with food and objects during development at fledging (1-2 months), juvenile (3-8 months) and sub-adult (14-18 months old) in 10 carrion crows (Corvus corone, C. cornix) and nine common ravens (C. corax). These species are closely related, generalist corvids and subjects were all hand-reared and housed in highly comparable conditions. Both species will routinely cache, i.e. hide food and other items for later recovery, and engage in cache-pilfering (stealing) strategies. They will interact and play with objects, potentially as part of developing social bonding and/or physical skills. We found that corvid behaviour was influenced by social context, with birds showing higher frequency of head & body out of sight behaviour while others were observing than when alone, suggesting they have an awareness of other's presence and respond by using barriers when interacting with items. There were no differences based on observer identity, supporting an interpretation of item interaction and play potentially driving development of physical skills in this setting. There were developmental effects, including increased manipulation and use of barriers as juveniles as well as increased caching with age. Ravens generally cached more than crows. Objects were manipulated more frequently than food, while barriers were used more with food, indicating that food was more likely to be actively hidden while objects may promote open play. We discuss our findings in relation to other social and developmental influences on behaviour and the wider ramifications for identifying the drivers of play in animals.
La vie en groupe social apporte des avantages considérables mais augmente aussi la compétition, qui peut parfois être surmontée par la coopération. L’objectif de ma thèse a été de déterminer l’influence des liens sociaux sur l’expression de la coopération en situation de compétition chez les corbeaux freux, une espèce coloniale monogame. Deux formes de coopération ont été étudiées : l’affiliation suite à un conflit (réconciliation et affiliation avec un tiers) et la formation de coalitions. Pris dans leur ensemble, mes résultats montrent que les corbeaux freux recourent à la coopération surtout quand cela s’avère nécessaire et que, lorsqu’ils coopèrent, ils le font quasi-exclusivement avec leur apparié. Mes résultats suggèrent que les patterns de coopération des corbeaux freux sont largement conditionnés par leur organisation sociale : l’imprévisibilité de leur environnement social a pu conduire à la flexibilité dont ils font preuve dans le recourt à la coopération et, le lien de couple, fort et durable, détermine le choix du partenaire de coopération.
In this thesis I explore the extent to which researchers of animal cognition should be concerned about the reliability of its scientific results and the presence of theoretical biases across research programmes. To do so I apply and develop arguments borne in human psychology’s “replication crisis” to animal cognition research and assess a range of secondary data analysis methods to detect bias across heterogeneous research programmes. After introducing these topics in Chapter 1, Chapter 2 makes the argument that areas of animal cognition research likely contain many findings that will struggle to replicate in direct replication studies. In Chapter 3, I combine two definitions of replication to outline the relationship between replication and theory testing, generalisability, representative sampling, and between-group comparisons in animal cognition. Chapter 4 then explores deeper issue in animal cognition research, examining how the academic systems that might select for research with low replicability might also select for theoretical bias across the research process. I use this argument to suggest that much of the vociferous methodological criticism in animal cognition research will be ineffective without considering how the academic incentive structure shapes animal cognition research. Chapter 5 then beings my attempt to develop methods to detect bias and critically and quantitatively synthesise evidence in animal cognition research. In Chapter 5, I led a team examining publication bias and the robustness of statistical inference in studies of animal physical cognition. Chapter 6 was a systematic review and a quantitative risk-of-bias assessment of the entire corvid social cognition literature. And in Chapter 7, I led a team assessing how researchers in animal cognition report and interpret non-significant statistical results, as well as the p-value distributions of non-significant results across a manually extracted dataset and an automatically extracted dataset from the animal cognition literature. Chapter 8 then reflects on the difficulties of synthesising evidence and detecting bias in animal cognition research. In Chapter 9, I present survey data of over 200 animal cognition researchers who I questioned on the topics of this thesis. Finally, Chapter 10 summarises the findings of this thesis, and discusses potential next steps for research in animal cognition.
en Florida Scrub‐Jays (Aphelocoma coerulescens) are cooperative breeders endemic to Florida’s oak scrub. In autumn, Florida Scrub‐Jays cache thousands of acorns and exhibit behaviors that appear to balance cache site selection against food degradation or cache robbery. However, both experience and position within a social dominance hierarchy could affect individual cache preferences. We examined the cache site preferences of birds with differing levels of caching experience and at different strata within a complex social dominance hierarchy. Our objective was to determine how experience, social position, and social context when caching influenced microhabitat preferences, and if these change as jays age, gain experience, and their social position changes. Naïve first‐year birds preferred to cache in well‐hidden, densely vegetated sites with relatively high soil moisture content. Naïve birds also cached farther from provisioning points if observed by a socially dominant bird than when they were alone or in the presence of birds of equal social status. Experienced adults preferred to cache in open, dry sandy sites and social context at the time of caching did not influence their preferences. As naïve birds aged, they gained experience and their social position changed. Experienced second‐year birds shifted their preference to more open, drier sites, and did so more often when they remained subordinate within their group rather than becoming dominant breeders. Second‐year birds that remained subordinate did not alter their caching behavior if observed by dominant birds. These patterns suggest that after gaining experience, jays learned which sites were more appropriate for caching and shifted their preference, regardless of their changing social status. We suggest that the risk of cache loss to food degradation might be greater than the risk of pilfering for Florida Scrub‐Jays, especially for birds in any social strata except the most subordinate, but this requires additional study.
Resumen
es Ontogenia de preferencia para obtener alimento de parte de individuos jóvenes de Aphelocoma coerulescens: evidencia de aprendizaje o cambio de estatus social?
Al arrendajo (Aphelocoma coerulescens) es un criador cooperativo endémico del matorral de roble de Florida. En el otoño, estas aves almacenan miles de bellotas y exhiben una conducta que parece balancear la selección del lugar de almacenaje con la posibilidad de que esta pueda ser robada o que las bellotas no se degraden. Sin embargo, tanto la experiencia como la posición en la jerarquía social de estas aves puede afectar las preferencias individuales en donde se almacenen las bellotas. Examinamos la preferencia en los lugares de almacenaje con diferentes niveles de experiencia y la posición que ocupa un individuo dentro de un complejo sistema jerárquico de dominancia. Nuestro objetivo fue determinar como la experiencia, la posición social, y el contexto social, contribuyen en las preferencias de selección de microhábitat, y si estos cambios influyen, con cambios en la posición social, al ganar experiencia y edad de las aves. Las aves ingenuas de primer año prefirieron almacenar las bellotas en lugares bien escondidos, con densa vegetación, y con suelos relativamente altos en humedad. Este grupo también escondió la comida en lugares más lejos, de los puntos de aprovisionamiento, si eran observadas por individuos dominantes en comparación que cuando estaban solas o eran observadas por individuos de igual rango social. Los adultos experimentados, prefirieron almacenar en lugares abiertos, arenosos y secos, y el contexto social no influjo en la preferencia del lugar de almacenaje. Según la edad de los jóvenes incrementó, estos ganaron experiencia y de igual manera cambio su posición social. Las aves de segundo año cambiaron sus lugares de almacenaje a lugares más abiertos y secos y lo hicieron con mayor frecuencia aun cuando se mantuvieron como subordinados, dentro del grupo, en vez de ser individuos dominantes y reproductivos. Este patrón sugiere que, al ganar experiencia, los arrendajos aprenden que lugares son más apropiados para almacenar y cambias sus preferencias, sin importar su estatus social. Sugerimos que el riesgo de perder las bellotas, al estas degradarse, pudiera ser mayor que el riesgo de robo, particularmente para aves de cualquier nivel social, excepto para los más subordinados, aunque esta apreciación necesita mayor estudio.
Individual recognition is the ability to differentiate between conspecifics based on their individual features. It forms the basis of many complex communicative and social behaviours. Here, we review studies investigating individual recognition in the auditory and visual domain in birds. It is well established that auditory signals are used by many birds to discriminate conspecifics. In songbirds, the neuronal structures underpinning auditory recognition are associated with the song system. Individual recognition in the visual domain has mainly been explored in chickens and pigeons, and is less well understood. Currently it is unknown which visual cues birds use to identify conspecifics, and whether they have cortical areas dedicated to processing individual features. Moreover, whether birds can recognise themselves visually, as evidenced by mirror self-recognition, remains controversial. In the auditory domain, the responses of neurons in the song system suggest identification of the bird’s own song. The surveyed behavioural and neural findings can provide a framework for more controlled investigations of individual recognition in birds and other species.
Scatter-hoarding animals cannot physically protect individual caches, and instead utilize several behavioral strategies that are hypothesized to offer protection for caches. We validated the use of physically altered, cacheable food items, and determined that intraspecific pilfering among free-ranging fox squirrels (N=23) could be assessed in the field. In this study we were able to identify specific individual squirrels who pilfered or moved caches that had been stored by a conspecific. We identified a high level of pilfering (25%) among this population. In a subsequent study, we assessed the fate of squirrel-made caches. Nineteen fox squirrels cached 294 hazelnuts with passive integrated transponder tags implanted in them. Variables collected included assessment and cache investment and protection behaviors; cache location, substrate, and conspicuousness of each cache; how long each cache remained in its original location, and the location where the cache was finally consumed. We also examined whether assessment or cache protection behaviors were related to the outcomes of buried nuts. Finally, we measured the population dynamics and heterogeneity of squirrels in this study, testing the hypothesis that cache proximity and pilferage tolerance could serve as a form of kin selection. Polymer chain reaction (PCR) was used to analyze hair samples and determine relatedness among 15 squirrels, and the potential impact of relatedness on caching behavior. Results suggested that cache protection behaviors and the lifespan of a cache were dependent on the conspicuousness of a cache. Squirrels may mitigate some of the costs of pilfering by caching closer to the caches of related squirrels than to those of non-related squirrels.
1. In a population of crested tits Parus cristatus in northern Belgium, living in group territories outside the breeding season, food was mainly stored during October and November, a time when territorial flocks are split up in age-specific subflocks. 2. First-year flock members frequently stored in the upper and outermost parts of the trees, whereas adults consistently hoarded and foraged in protected sites near the trunk. The outermost, predator-exposed sites were only used by first-year foragers in mixed-age winter flocks with adults, as a result of site competition within flocks on cold days. 3. Consequently, the overlap between foraging sites (protected) and hoarding sites (exposed) of first-year birds was small during autumn, but large during winter. Adults, in contrast, consistently showed a large overlap between their hoarding and foraging niche, independently of type of foraging flock. Due to the segregation of hoarding and foraging sites in autumn, first-year birds performed almost six times as many flights within trees as adults. 4. The overall hoarding frequency (total number of stores per hour) was (i) lower for first-year birds compared to adults, and (ii) inversely correlated with the proportion of hoarding in exposed sites. We argue that high energetic costs of flying and the high predation risk in exposed sites limit the number of stores made by first-year birds. 5. However, despite their lower hoarding frequency compared to adults, first-year birds potentially encounter equal numbers of stores when foraging in mixed-age winter flocks, primarily as a result of the high encounter rate in exposed sites. It is therefore argued that the cost of subordination for first-year crested tits might be lower than was formerly stated.
The Clark's Nutcracker (Nucifraga columbiana) stores conifer seeds in the late summer and fall of each year. During winter and spring, seeds from buried caches are the major food of nutcrackers and their young. A bird must find more than a thousand seed caches each year. The alternative means by which nutcrackers may locate seed stores are (1) memory of cache site and (2) trial and error search. While searching for stored seeds, a Clark's Nutcracker makes a series of prod holes with its bill. A hole from which a cache was recovered is usually distinguished by a pile of broken seed coats. This allows an estimate of a nutcracker's success rate in locating seed caches. Theft of seed caches by rodents and removal of intact seeds from cache sites by nutcrackers may confuse this estimate. A field technique based on deductive reasoning is presented to determine how nutcrackers recover their caches. In the eastern Sierra Nevada I gathered field data on the success rate and nearest neighbor distances among prod holes in spring and summer of 1975. Data indicating the proportion of caches taken by rodents were obtained in 1978. Analyses of these data suggest that nutcrackers find most of their caches by means of memory. A search based on memory implies that seed stores are not communal and that nutcrackers must remain in the area where they stored seeds until the following summer. Theft of seed stores by rodents must be an important selective pressure on nutcracker caching behavior. By caching seeds in storage areas which become covered with deep snow, nutcrackers may reduce their losses to rodents.
We quantified the degree of scatterhoarding and larderhoarding exhibited during late summer and early autumn by 10 individuals within a population of red squirrels (Tamiasciurus hudsonicus) in the Cypress Hills, Alberta, Canada. All squirrels made extensive and obvious larderhoards in central middens. in addition, sampling quadrats and behavioral observations revealed that ca. 43% of total stores were scatterhoarded throughout territories. Across individuals, the number of cones scatterhoarded was related inversely to the number stored in the midden. Nearest-neighbor analyses indicated that cones were distributed in a spatially clumped manner throughout each territory. However, the hoards themselves, independent of size, tended to be dispersed randomly. Cones hoarded in middens did not differ from scatter hoarded cones in terms of content of seeds, nor were they treated differently by the squirrels in terms of carrying distance. At the end of our study, seasonal hoarding was not yet complete, but squirrels already had hoarded sufficient cones to meet their energetic requirements for greater than or equal to 3 months. We conclude that the characteristic pattern of storage of food by red squirrels is a deliberate mixture of distinct larderhoarding and scatterhoarding tactics.
Accumulating and maintaining sufficient energy reserves is critical for winter survival of birds. Because high fat levels are assumed to be associated with higher risk of predation, birds have been hypothesized to regulate their body mass as a trade-off between risk of starvation and risk of predation. Theoretical models of energy management in birds typically assume that predation risk is constant throughout the day. However, this important assumption has little empirical support, and there is some evidence suggesting that it might not always be correct and that predation risk may vary during the day. Because predation risk is a critical component of the predation-starvation trade-off, any change in its value through the day might have a profound effect on birds' optimal daily tactics of energy accumulation. We used a dynamic optimization model to investigate how changes in predation risk might affect birds' energy management decisions. Daily patterns of fat accumulation and feeding activity were predicted to change with predation risk in a manner consistent with previous models (lower mass gain and less feeding when predation risk is high). Our more counterintuitive results concern daily patterns of food caching and cache retrieval. When predation risk was assumed to peak at midday, birds were predicted to cache primarily in the afternoon and not in the morning even though predation risk was identical in the morning and afternoon. With other temporal patterns of predation risk, caching intensity was highest when predation risk was lowest. Surprisingly, the daily pattern of cache retrieval was predicted to be unaffected by daily patterns of predation risk: birds were always predicted to retrieve their caches primarily during the late afternoon with a small peak in the morning. Highest mortality was predicted with predation risk decreasing from morning to evening whereas lowest mortality was predicted with predation risk increasing from morning to evening. Our model helps explain large variations in observed daily patterns of energy management in birds and provides testable predictions that could help us understand the daily dynamics of predation risk and how birds should respond to it.
We investigated the effects of pilferage on caching behavior in the Merriam's kangaroo rat by manipulating two factors associated with pilferage: the presence of a conspecific, and the opportunity for pilferage. In one experiment we assessed animals in either "Stealer" or "Victim" roles and measured changes in caching, space use, and behavior after caches were pilfered. Victims shifted from a majority scatter-hoarding to a majority larder-hoarding strategy after their caches were pilfered by the Stealer. In Experiment 2, we measured changes after exposure to a conspecific when there was no pilferage, with or without prior exposure to pilferage from Experiment 1. Merriam's kangaroo rats were vigilant when a conspecific was present, but did not change cache strategy. Prior exposure did not have any major effect on caching or behavior. Food storage is an economic decision that is often made by a solitary forager. Our results suggest that social competition nonetheless influences such economic decisions, even in a nonsocial forager.
Recovery of cached sunflower seeds by Black-capped Chickadees (Parus atricapillus) was observed in four laboratory experiments. Results of the first experiment were consistent with the hypothesis that chickadees use spatial memory to recover seeds cached 24 h earlier. The second experiment demonstrated that individuals have a high recovery rate for their own caches and a low recovery rate for caches made by another. The third and fourth experiments demonstrated that one chickadee observing another caching seeds provided no recovery benefit to the observer in comparison to its performance when recovering seeds hidden in its absence. This result held for 2-h and for 6-min delays between observation and attempted recovery. We believe that spatial memory is used by chickadees, that the individual carrying out the caching has a large recovery advantage over a conspecific that searches the same patch, and that the perceptual and motor experience involved in the act of traveling to a cache location may be necessary for the establishment of spatial memory.
Birds have been studied for centuries because they are numerous, conspicuous, and aesthetically pleasing to humans. Despite their overall regard for birds, historically, many ornithologists have considered birds as instinct-driven organisms of little intellectual capacity. For example, the ornithological textbook of choice from the 1960s states the following view of avian intelligence: Flight has proven to be an enormously successful evolutionary venture, but one that has cost birds dearly in mental development. In effect, problems merely by flying away from them. … As a consequence, much [avian] behavior is, by mammalian standards, fragmentary, stereotyped, and at times amazingly stupid. (Welty, 1962, p. 159). Research over the past 30 years has shown that this view of birds is incorrect. Field studies have demonstrated that birds possess considerable behavioral adaptability, often engaging in flexible and opportunistic behaviors while foraging, communicating, selecting mates, interacting in social groups, and avoiding predators (see Krebs and Davies, 1984). Laboratory studies have demonstrated that birds perform very well in solving a variety of complex cognitive problems (e.g., Pepperberg, 1990; Vaughan, 1988; Herrnstein, 1985; Kamil et al., 1977). Interestingly, the ability to solve many of these complex problems was once thought to be the exclusive province of primates. As Marler has suggested (this volume), the intellectual abilities of birds in some areas may be broadly equivalent or superior to that of mammals. Thus, understanding cognitive abilities of birds is an important issue for ornithologists. Most previous work on cognition in animals has been carried out by experimental psychologists who have not carefully considered either the ecological setting or evolutionary history of their subject species (see Kamil, 1988a). In this paper we present an explicit evolutionary approach to the study of cognition, with an emphasis on the use of comparative studies. Although this approach is quite general, it is particularly appropriate for ornithological studies.
This chapter discusses four aspects of these animals' behavior: (1) how stored food is recovered; (2) the life history and social consequences of food storing; (3) the economics of food caching and the decision making it involves; and (4) the interrelations between food-storing animals and their food plants. The terms hourding, storing, and caching will be used as synonyms, and the material discussed is restricted to birds and mammals. Many invertebrates store food, and one well-studied instance is described in Heinrich. The chapter describes three animals: Acorn Woodpeckers (Melanerpes formicivorus), South Island Robin (Petroicu uustrulis), and Eastern Chipmunk (Tumias striutus) that illustrate the variation, which can occur in food storing. Storing food is an essential feature of the annual cycle of many animals, it is a prerequisite for successful breeding in some species, and has advanced the time of breeding in others. Finally, food-storing animals are used as agents of dispersal by a variety of plants.
Birds have been studied for centuries because they are numerous, conspicuous, and aesthetically pleasing to humans Despite their overall regard for birds, historically, many ornithologists have considered birds as instinct-driven organisms of little intellectual capacity. For example, the ornithological textbook of choice from the 1960s states the following view of avian intelligence:
Flight has proven to be an enormously successful evolutionary venture, but one that has cost birds dearly in mental development. In effect, flight has become a substitute for cleverness; birds solve many potential problems merely by flying away from them…. As a consequence, much [avian] behavior is, by mam-malian standards, fragmentary, stereotyped, and at times amazingly stupid. (Welty, 1962, p.159).
Red squirrels (Tamiasciurus hudsonicus) exhibit two modes of food hoarding across their range, larderhoarding in the west and scatterhoarding in the east. Because most studies have been conducted in the west, it is commonly thought that larderhoarding is characteristic of the species. We investigated the numbers of cones in caches, feeding locations relative to caches, daily consumption of cones, and whether cover might influence feeding location, in a jack pine (Pinus banksiana) plantation near Brockway, New Brunswick, Canada, from November 1990 to December 1991. Scatterhoarding occurred among squirrels during autumn 1990 and 1991. Squirrels cached enough cones to survive ca. 37 days in autumn 1990 and 7 days in 1991, based on an estimate of cone consumption of 47/day from four territories in autumn 1990. During winter 1990-1991, heavy feeding occurred on cones picked from, and cached in, trees. Most cones (86%) were eaten in trees according to surveys in varied coniferous stand types throughout New Brunswick during winter 1990-1991. It appears that small, scattered caches predominate in the east and probably are as extensive as larderhoards in the west.
We tested our earlier prediction that the food content of buried nuts will influence the density at which fox squirrels (Sciurus niger) scatterhoard each species of nut. We buried black walnuts (Juglans nigra), bur oak acorns (Quercus macrocarpa), and chinquapin oak acorns (Q. muehlenbergii) at varying densities in monospecific and mixed-species grids in three different years and three different seasons within a year, and analyzed their survival from predation over time. We also observed free ranging squirrels scatterhoard walnuts and bur oak acorns, which we made available in equal numbers. The survival of buried nuts was dependent on the nut species, nut density, and squirrel density. The lowest meaningful density of buried nuts for squirrels was related to the food content of the nut species. Analysis of nut survival at the same burial sites in successive seasons indicated that squirrels did not use memory to return to specific sites where they had previously found nuts. Rather, they foraged preferentially in certain microhabitats. Squirrels were observed burying black walnuts farther away from a source pile than they buried bur oak acorns. The difference is consistent with the difference in food content between the two species and also with the threshhold density below which naive squirrels have no density-dependent effect on buried nuts. Our data on nut survival suggest that squirrel foraging varies with nut density but not with nut spacing.
Foraging success of three species of granivorous rodents (deer mouse, Peromyscus mani-culatus;. Great Basin pocket mouse, Perognathus parvus; yellow pine chipmunk, Tamias amoenus) was determined for seeds of three palatable species (antelope bitterbrush, Purshia tridentata; Indian ricegrass, Oryzopsis hymenoides; lodgepole pine, Pinus contorta) buried in dry or moistened substrates. Rodents found nearly all caches (449 of 450) when seeds were buried in moist substrate, but found only 13.3% of 450 caches buried in dry substrate. This appears to be a consequence of rodents‘ diminished ability to smell seeds in dry substrate, rather than a preference to forage where seeds are easier to detect. Great Basin pocket mice found most (83%) of the caches located in dry substrate, indicating that they may have better olfactory capabilities than do the other species. The ability of desert rodents to find buried seeds in the field may vary as soil water fluctuates. If so, rodent-seed interactions and competitive relations among granivorous rodents may change significantly between wet and dry seasons.
Granivores are likely to store food in numerous, widely scattered, small caches if they are unable to defend concentrated large caches against interspecific competitors. This scatterhoarding of seeds makes it impossible for individuals to defend all their scattered caches against intraspecific competitors as well. Optimal spacing of scattered caches should result from a balance between decreasing loss of caches to naive competitors with decreasing density and increasing cost of storage with decreasing density. A mathematical model predicting optimal density is presented. One prediction of the model is that as the (@Q) of habitat suitable for seed burial surrounding a seed source is decreased, the average distance (D) a cache is taken from the source by scatterhoarders should increase. Another prediction is that increasing the number of seeds (N) at a source, either by an increase in the size of a single seed crop or by the presence of 2 or more conspecific seed producers in close proximity to one another, should increase D. One trait of trees which increases single crop sizes and average seed dispersal distance (D) is the pattern of withholding energy from reproduction some years to allow unusually large crops during mast years. Three field tests of the model and its predictions were conducted: (1) Juglans nigra seeds were buried at 3 densities and their survival in time from predation by Sciurus niger was found to increase with decreasing density; (2) average distances that J. nigra saplings occurred from 16 parent walnut trees were found to have a statistically significant correlation with the D calculated from the model and the @Q of suitable habitat surrounding each tree; (3) Sciurus niger individuals were observed to scatterhoard Juglans nigra seeds in a pattern that maintained a mean cache density that gives low rates of loss to naive competitors as indicated from field test (1). The results strongly suggest maintenance of optimum cache density by S. niger. The coevolution of trees which have mast years and the animals that scatterhoard their seeds is discussed.
Black-capped Chickadees Parus articapillus scatter hoard food. Because they live in social groups during the winter, flock members may observe caching by others and take their caches. We present two laboratory experiments that investigate the possibility of observational learning of cache location and related behaviours. In the first experiment, 15 chickadees were observed storing food in an indoor aviary, either individually or in pairs. Five percent of caches were taken within a few minutes by birds that observed the occurrence of caching. These cache thefts may have been assisted by observation. Dominant birds made more caches and subordinate birds were more likely to take another bird's caches. When cache recovery was tested several hours later, birds recovered their own caches more accurately than those of other birds but recovery of other birds' caches was not improved by the previous observation of caching. A second experiment with 6 additional chickadees examined whether birds attempt to conceal their caching activity. In this experiment 9% of caches were taken by birds that had the opportunity to observe caching. When birds carried seeds, they flew away from their companion more than they did when they were flying without a seed. Overall, these results are consistent with those of previous laboratory studies and suggest that conspecific cache theft may be relatively rare in flocks of food-storing chickadees.
By analogy with patch-use decisions made by animals foraging among patches, animals storing food items among scattered sites must make decisions such as how long to persist in exploiting a known source before leaving to search for alternative sources. If the survival of scattered caches is density-dependent, then there should be a "source-departure threshold," beyond which additional caching would reduce the long-term average rate of storage of recoverable food. The hoarder would profit maximally by leaving the source at that threshold, even though the source still contains food. We experimentally examined how two factors influence various source-use decisions of Gray Jays Perisoreus canadensis exploiting locally abundant food sources. First, we examined the behavior of jays exploiting a food source during an initial "encounter" and during another encounter 3 days later. The jays made fewer caches during subsequent encounters with a source at a given location, around which the local density of previously made caches was high. They also compensated by spacing out their caches more widely and by increasing the rate at which they retrieved and redistributed previously made caches. Second, we investigated the effect of the composition of a food source (i.e., the value of its food items) on the jays' source-use decisions. The jays cached substantially more food items (raisins) from a large-item (X̄=491) than from a small-item (328) source when sources of each type were made available on different days. The cumulative number of caches made by individual jays (over 10 h) was more nearly asymptotic in the smaller-item treatment. We propose that the jays' tendency to recache previously made caches accounts for their failure to cease hoarding from our experimental sources. This two-stage process of food storage (i.e., initial placement and subsequent recaching) may yield long-term average rates of storage throughout the territory exceeding those predicted by simple rate-maximization, patch-use models.
The ability of yellow pine chipmunks (Tamias amoenus) and deer mice (Peromyscus maniculatus) to detect buried antelope bitterbrush (Purshia tridentata) seed caches of differing water content was examined in an arena containing dry sand. Neither species could detect caches of air-dried seeds (6.8% water) using olfaction, but they found some caches after the seeds had been hydrated (exposed to ≈100% relative humidity) for only 0.25 h (7.3% water). When seeds contained >8.0% water, subjects usually found most of the treatment caches available. Search times to find treatment caches were significantly greater for caches of very low water content (<7.3-7 4% water) compared to caches of higher water content. There were no significant differences in the abilities of deer mice and yellow pine chipmunks to detect treatment caches. When seeds were moistened (41.2% water) and then were allowed to dry out (6.4% water), subjects could not find the seeds in the dry arena sand. Variation in seed water content under natural conditions in the field may have important implications for rodent-seed interactions.
(1) The problem of how food caches should be distributed confronts all animals which hoard food for use later. If all the food is hidden close to the source then it may be found easily by others, yet if hoarded further afield a lot of time will be spent travelling. (2) A model which describes the distribution of caches that results in the best compromise between these conflicting demands is presented. The model assumes animals maximize the number of items recovered, subject to a limit on the time available for hoarding. (3) Three predictions of this model were tested: (i) If density-dependent loss of caches is high then caches should be placed at lower densities. (ii) All initial caches should be made in sites near the source, subsequent ones in sites both near to and far from the source. (iii) The density of caches should decline with distance from the source. (4) Field experiments showed that magpies (Pica pica) behaved in a manner consistent with the first prediction and the majority conformed to the second and third predictions. (5) The results are compared with the contrasting predictions of Stapanian & Smith (1978).
In coniferous forests of Central Finland, Willow (Parus montanus) and Crested Tits (P. cristatus) store seeds in a scattered distribution within their territory during the autumn. Individuals cache and recover food items while moving together as members of mixed-species flocks. The purpose of this study was to test certain predictions of scatter-hoarding models (Stapanian and Smith 1978, Clarkson etal. 1986), which predict how the animal should hoard food items from a superabundant source to maximize the number of caches recovered. Our field experiments gave support to most of the predictions of the models. Individual tits stored seeds closer to the food source when food had been available for first time (new feeder with seeds not previously available) than to feeders with seed available for 1 mo. Individual birds of both species carried large food items (hulled sunflower seeds) father than small items (spruce seeds) before caching them. Crested Tits distributed their catches uniformly around the feeder while most of the Willow Tits favored certain sectors around the feeder. Subdominant individuals carried seeds the same distances as did dominant birds when the food source was ephemeral, but farther from a continuously available food source.
Although the importance of olfaction in birds is being increasingly recognized, its role in species with very small olfactory bulbs, such as corvids, is largely unknown. In field experiments designed to examine whether Black-billed Magpies (Pica pica) use olfaction to locate hidden food, we found that magpies uncovered significantly more caches of suet and raisins scented with cod liver oil than control caches. We suggest that in recovering caches, magpies use a multicue system that may involve both memory and visual or olfactory cues. Olfactory cues may be particularly important in finding and taking food hidden by other individuals.
Laboratory experiments were conducted to investigate the foraging responses of kangaroo rats (Dipodomys merriami) and pocket mice (Perognathus amplus) to aggregates of seeds which differed in size, depth, and degree of clumping. Kangaroo rats effectively used clumps of seeds, whereas the pocket mice did not differentially select clumps of seeds over a scattered distribution of seeds. In addition to distribution, clump size and depth were important criteria for both species in determining foraging efforts. These data, coupled with recent information which suggests wide arrays of seed distribution types in the desert, lead us to propose that rodents select seeds on the basis of spatial distribution of the resource. This is an attractive hypothesis because it can accommodate both of the primary mechanism previously suggested for desert rodent coexistence, seed size selection and habitat selection.
We examined jay caching patterns over 3 yr in a woodland-prairie landscape in S-central Iowa. Three aspects were examined: jay habitat preferences for caching, jay caching patterns before and after fire, and the influence of predation on nuts by small mammals on tree recruitment in jay territories. Blue jays cached nuts in a wide range of habitats, from open, grassy patches to mature forest. Jays cached preferentially in regenerating woodland and edge habitats while usually avoiding grassland habitats. Caching increased in grassland following a controlled burn. Detection by small mammals of artificial nut caches placed by the investigator was extremely high. The results support a keystone role for blue jays in oak forest ecosystems based on their habit of caching large numbers of most acorn species in the ground in habitats generally suitable for germination and establishment. Their long-distance transport and caching activities would be most significant to tree population dynamics during climate change or in contemporary fragmented landscapes.
Among Willow Tits as well as Crested Tits conspecifics united into small, coherent, and territorial social groups (mean size, 2.9 ind for Crested Tit and 4.1 ind for Willow Tit) during the non-breeding season. Members of the same group were not closely genetically related. Throughout the winter each group contained a stable set of individuals. Adults from different breeding pairs rarely participated in the same group, but groups without adults were rare. The groups were formed and their individuals composition largely set by late summer as dispersing first year birds became resident. At settlement, the first year birds spaced among groups and distributed themselves so as to form even pairs. Most likely, the food storing behaviour necessitates the stationary life, and thus may explain the stable content of the groups. Food competition probably accounts for the spacing of conspecifics among flocks. Differential costs and benefits to group members from the social behaviour probably have to be considered to explain group size and dynamics.
Gray Jays (Perisoreus canadensis) cache surplus food extensively during summer and opportunistically at other times of the year. Food items are cached as saliva-coated boli (Dow 1965). Each bolus is cached above ground and in a separate site, such as in a bark crevice, in coniferous foliage, or in a fork between twigs. These caches are used during winter (pers. observ.) and through the following breeding season in March and April, when food supplies can still be reduced and not yet replen-ishing (Strickland unpubl., cited in Sherry 1985). Un-like animals that larderhoard (e.g., pine squirrels, Ta-miasciurus douglasii, Smith 1970; Acorn Woodpeckers, Melanerpes formicivorus, MacRoberts and Mac-Roberts 1976; pocket mice, Perognathus intermedius, Reichman and Fay 1983) Gray Jays scatter their cach-es, as do other corvids (Goodwin 1976, Ligon 1978, Vander Wall and Balda 1981. Tomback 1982. James and Verbeek 1983, Clarkson' et al. 1986). Gray Jays and Siberian Jays (Perisoreus infaustus, Blomgren 1964) however, differ from other corvids in that they cache in trees rather than on the ground. The strategy of scatterhoarding renders individual caches indefensible against pilferage by competitors, such as Gray Jays from adjacent territories. A Gray Jay transporting food from a central point to surround-ing cache sites might be expected to achieve a spatial distribution of caches that represents a trade-off be-tween the benefit of reduced cache robbery (i.e., re-duced density-dependent loss of caches to competitors which are naive to the cache locations) and time and energy costs of longer flights required to achieve low densities. Because Gray Jays have some memory for the locations oftheir caches (Bunch and Tomback 1986) placing caches in widely separated sites should dis-courage competitors without making it too difficult to find their own caches. Although much of the food eaten and cached by Gray Jays typically is not clumped (Strickland, unpubl.), jays have been observed making caching trips radiating from central food sources such as animal carcasses (e.g., red fox, Vulpes fulva, Ouellet 1970; arctic ground squirrel, Citellus parryi, and red squirrel, Tamiasciurus hudsonicus, pers. observ.) and patches of blueberries (Vaccinium sp.; pers. observ.). Thus, it seems reasonable to apply to Gray Jays two models that have been developed to describe the eco- nomics of transporting food from a central place to surrounding cache sites (Stapanian and Smith 1978, Clarkson et al. 1986). Though these models generate somewhat different predictions, they share the as-sumption that survivorship of caches decreases with increasing cache densities. In this paper I present a test ofthis assumption applied to simulated Gray Jay cach-es. To the extent that this assumption holds, Gray Jays might be predicted to balance the benefit of spacing their caches widely (i.e., a high probability that the caches will survive long enough to be recovered) against the costs required to place caches at low densities.
We examined food-caching behavior of captive Black-capped Chickadees (Par-us atricapillus) to determine if conspecific density and relative social status influenced caching behavior. Individuals cached significantly fewer seeds and initiated caching later in the trial when conspecific densities were high than when alone or in the presence of a single con-specific. Social rank was not related to the observed variation in seed caching. The results suggest that conspecifics might he perceived as a source of potential cache loss by individuals but only when several are present.