Amodio, P., Boeckle, M., Schnell, A. K., Ostojic, L., Fiorito, G., & Clayton, N. S. (2018). Grow Smart and Die Young: Why Did Cephalopods Evolve Intelligence? Trends. Ecol. Evol., .
Abstract: Intelligence in large-brained vertebrates might have evolved through independent, yet similar processes based on comparable socioecological pressures and slow life histories. This convergent evolutionary route, however, cannot explain why cephalopods developed large brains and flexible behavioural repertoires: cephalopods have fast life histories and live in simple social environments. Here, we suggest that the loss of the external shell in cephalopods (i) caused a dramatic increase in predatory pressure, which in turn prevented the emergence of slow life histories, and (ii) allowed the exploitation of novel challenging niches, thus favouring the emergence of intelligence. By highlighting convergent and divergent aspects between cephalopods and large-brained vertebrates we illustrate how the evolution of intelligence might not be constrained to a single evolutionary route.
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Clayton, N. S. (2004). COGNITION: An Open Sandwich or an Open Question? Science, 305(5682), 344–.
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Clayton, N. S., & Dickinson, A. (1998). Episodic-like memory during cache recovery by scrub jays. Nature, 395(6699), 272–274.
Abstract: The recollection of past experiences allows us to recall what a particular event was, and where and when it occurred1,2, a form of memory that is thought to be unique to humans3. It is known, however, that food-storing birds remember the spatial location4, 5, 6 and contents6, 7, 8, 9 of their caches. Furthermore, food-storing animals adapt their caching and recovery strategies to the perishability of food stores10, 11, 12, 13, which suggests that they are sensitive to temporal factors. Here we show that scrub jays (Aphelocoma coerulescens) remember 'when' food items are stored by allowing them to recover perishable 'wax worms' (wax-moth larvae) and non-perishable peanuts which they had previously cached in visuospatially distinct sites. Jays searched preferentially for fresh wax worms, their favoured food, when allowed to recover them shortly after caching. However, they rapidly learned to avoid searching for worms after a longer interval during which the worms had decayed. The recovery preference of jays demonstrates memory of where and when particular food items were cached, thereby fulfilling the behavioural criteria for episodic-like memory in non-human animals.
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Emery, N. J., & Clayton, N. S. (2004). The Mentality of Crows: Convergent Evolution of Intelligence in Corvids and Apes. Science, 306(5703), 1903–1907.
Abstract: Discussions of the evolution of intelligence have focused on monkeys and apes because of their close evolutionary relationship to humans. Other large-brained social animals, such as corvids, also understand their physical and social worlds. Here we review recent studies of tool manufacture, mental time travel, and social cognition in corvids, and suggest that complex cognition depends on a “tool kit” consisting of causal reasoning, flexibility, imagination, and prospection. Because corvids and apes share these cognitive tools, we argue that complex cognitive abilities evolved multiple times in distantly related species with vastly different brain structures in order to solve similar socioecological problems.
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Emery, N. J., Clayton, N. S., & Frith, C. D. (2007). Introduction. Social intelligence: from brain to culture. Philos Trans R Soc B, 362.
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Emery, N. J., Dally, J. M., & Clayton, N. S. (2004). Western scrub-jays ( Aphelocoma californica) use cognitive strategies to protect their caches from thieving conspecifics. Anim. Cogn., 7(1), 37–43.
Abstract: Food caching birds hide food and recover the caches when supplies are less abundant. There is, however, a risk to this strategy because the caches are susceptible to pilfering by others. Corvids use a number of different strategies to reduce possible cache theft. Scrub-jays with previous experience of pilfering other's caches cached worms in two visuospatially distinct caching trays either in private or in the presence of a conspecific. When these storers had cached in private, they subsequently observed both trays out of reach of a conspecific. When these storers had cached in the presence of a conspecific, they subsequently watched the observer pilfering from one of the trays while the other tray was placed in full view, but out of reach. The storers were then allowed to recover the remaining caches 3 h later. Jays cached more worms when they were observed during caching. At the time of recovery, they re-cached more than if they had cached in private, selectively re-caching outside of the trays in sites unbeknown to potential thieves. In addition, after a single pilfering trial, the jays switched their recovery strategy from predominantly checking their caches (i.e. returning to a cache site to see whether the food remained there) to predominantly eating them. Re-caching remained constant across the three trials. These results suggest that scrub-jays use flexible, cognitive caching and recovery strategies to aid in reducing potential future pilfering of caches by conspecifics.
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Emery, N. J., Seed, A. M., von Bayern, A. M. P., & Clayton, N. S. (2007). Cognitive adaptations of social bonding in birds. Phil. Trans. Biol. Sci., 362(1480), 489–505.
Abstract: The “social intelligence hypothesis” was originally conceived to explain how primates may have evolved their superior intellect and large brains when compared with other animals. Although some birds such as corvids may be intellectually comparable to apes, the same relationship between sociality and brain size seen in primates has not been found for birds, possibly suggesting a role for other non-social factors. But bird sociality is different from primate sociality. Most monkeys and apes form stable groups, whereas most birds are monogamous, and only form large flocks outside of the breeding season. Some birds form lifelong pair bonds and these species tend to have the largest brains relative to body size. Some of these species are known for their intellectual abilities (e.g. corvids and parrots), while others are not (e.g. geese and albatrosses). Although socio-ecological factors may explain some of the differences in brain size and intelligence between corvids/parrots and geese/albatrosses, we predict that the type and quality of the bonded relationship is also critical. Indeed, we present empirical evidence that rook and jackdaw partnerships resemble primate and dolphin alliances. Although social interactions within a pair may seem simple on the surface, we argue that cognition may play an important role in the maintenance of long-term relationships, something we name as “relationship intelligence”.
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Griffiths, D. P., & Clayton, N. S. (2001). Testing episodic memory in animals: A new approach. Physiol. Behav., 73(5), 755–762.
Abstract: Episodic memory involves the encoding and storage of memories concerned with unique personal experiences and their subsequent recall, and it has long been the subject of intensive investigation in humans. According to Tulving's classical definition, episodic memory “receives and stores information about temporally dated episodes or events and temporal-spatial relations among these events.” Thus, episodic memory provides information about the `what' and `when' of events (`temporally dated experiences') and about `where' they happened (`temporal-spatial relations'). The storage and subsequent recall of this episodic information was thought to be beyond the memory capabilities of nonhuman animals. Although there are many laboratory procedures for investigating memory for discrete past episodes, until recently there were no previous studies that fully satisfied the criteria of Tulving's definition: they can all be explained in much simpler terms than episodic memory. However, current studies of memory for cache sites in food-storing jays provide an ethologically valid model for testing episodic-like memory in animals, thereby bridging the gap between human and animal studies memory. There is now a pressing need to adapt these experimental tests of episodic memory for other animals. Given the potential power of transgenic and knock-out procedures for investigating the genetic and molecular bases of learning and memory in laboratory rodents, not to mention the wealth of knowledge about the neuroanatomy and neurophysiology of the rodent hippocampus (a brain area heavily implicated in episodic memory), an obvious next step is to develop a rodent model of episodic-like memory based on the food-storing bird paradigm. The development of a rodent model system could make an important contribution to our understanding of the neural, molecular, and behavioral mechanisms of mammalian episodic memory.
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Krebs, J. R., Clayton, N. S., Hampton, R. R., & Shettleworth, S. J. (1995). Effects of photoperiod on food-storing and the hippocampus in birds. Neuroreport, 6(12), 1701–1704.
Abstract: Birds that store food have a relatively large hippocampus compared to non-storing species. The hippocampus shows seasonal differences in neurogenesis and volume in black-capped chikadees (Parus atricapillus) taken from the wild at different times of year. We compared hippocampal volumes in black-capped chickadees captured at the same time but differing in food-storing behaviour because of manipulations of photoperiod in the laboratory. Differences in food-storing behaviour were not accompanied by differences in the volume of the hippocampus. Hippocampal volumes also did not differ between two groups of a non-food-storing control species, house sparrows (Passer domesticus), exposed to the same conditions as the chickadees.
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Reboreda, J. C., Clayton, N. S., & Kacelnik, A. (1996). Species and sex differences in hippocampus size in parasitic and non-parasitic cowbirds. Neuroreport, 7(2), 505–508.
Abstract: To test the hypothesis that selection for spatial abilities which require birds to locate and to return accurately to host nests has produced an enlarged hippocampus in brood parasites, three species of cowbird were compared. In shiny cowbirds, females search for host nests without the assistance of the male; in screaming cowbirds, males and females inspect hosts' nests together; in bay-winged cowbirds, neither sex searches because this species is not a brood parasite. As predicted, the two parasitic species had a relatively larger hippocampus than the non-parasitic species. There were no sex differences in relative hippocampus size in screaming or bay-winged cowbirds, but female shiny cowbirds had a larger hippocampus than the male.
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