Cognitive Ecology in Hummingbirds: The Role of Sexual Dimorphism and Its Anatomical Correlates on Memory

et al. (2014) Cognitive Ecology in Hummingbirds: The Role of Sexual Dimorphism and Its Anatomical Correlates on Memory. PLoS ONE 9(3): e90165. doi:10.1371/journal.pone.0090165 Cognitive Ecology in Hummingbirds: The Role of Sexual Dimorphism and Its Anatomical Correlates on Memory Paulina L. Gonza lez-Go mez 0 Natalia Madrid-Lopez 0 Juan E. Salazar 0 Rodrigo Sua rez 0 Pablo Razeto- Barry 0 Jorge Mpodozis 0 Francisco Bozinovic 0 Rodrigo A. Va squez 0 Paul Graham, University of Sussex, United Kingdom 0 1 Instituto de Ecolog a y Biodiversidad, Facultad de Ciencias, Universidad de Chile , Santiago , Chile , 2 Instituto de Filosof a y Ciencias de la Complejidad , Santiago , Chile , 3 Departamento de Biolog a, Facultad de Ciencias, Universidad de Chile , Santiago , Chile , 4 Departamento de Ecolog a, MIII & LINCGlobal, Centro de Estudios Avanzados en Ecolog a & Biodiversidad, Pontificia Universidad Cato lica de Chile , Santiago , Chile In scatter-hoarding species, several behavioral and neuroanatomical adaptations allow them to store and retrieve thousands of food items per year. Nectarivorous animals face a similar scenario having to remember quality, location and replenishment schedules of several nectar sources. In the green-backed firecrown hummingbird (Sephanoides sephanoides), males are territorial and have the ability to accurately keep track of nectar characteristics of their defended food sources. In contrast, females display an opportunistic strategy, performing rapid intrusions into males territories. In response, males behave aggressively during the non-reproductive season. In addition, females have higher energetic demands due to higher thermoregulatory costs and travel times. The natural scenario of this species led us to compared cognitive abilities and hippocampal size between males and females. Males were able to remember nectar location and renewal rates significantly better than females. However, the hippocampal formation was significantly larger in females than males. We discuss these findings in terms of sexually dimorphic use of spatial resources and variable patterns of brain dimorphisms in birds. - Funding: This work received funding from CONICYT (PGG and RS), FONDECYT 1130015 (FB) and FONDECYT 1090794, 1060186; ICM-P05-002; and PFB-23CONICYT (RAV). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Cognitive abilities, such as learning and memory are pivotal to behavioral performance of animals. These include essential activities such as learning and performing mating displays [1], predator avoidance [2], and food searching [3], among other traits closely linked to fitness [4]. In particular, spatiotemporal memory, which allows individuals to recall time and location of items simultaneously, can be especially important for animals that rely in non-visual cues to retrieve food items. For example, scatterhoarding species store food in multiple locations dispersed throughout their home range. These animals, like corvids (nutcrackers, jays) and parids (tits and chickadees), can store as much as 100,000 to 500,000 individual caches per year [5,6,7]. In this context, several studies have shown that spatial memory abilities are involved in cache retrieval in food-caching species [8,9,10], and these species show better cognitive abilities in comparison with non-caching species [11,12]. The neural mechanisms involved in spatial memory required to retrieve thousands of food items include regions of the medial pallium, such as the hippocampus in mammals [13] or its avian homologue, the hippocampal formation (HF) [14]. In fact, several studies have shown that lesioning the HF in scatter-hoarding bird species severely disrupt food retrieval performance [15,16]. The adaptive specialization hypothesis (ASH) posits that natural selection may change behavior and its underlying neural mechanisms if such modifications enhance fitness [17,18,19]. In the context of spatial memory and its mechanisms at the hippocampus, there are several bodies of evidence supporting ASH. For example, food-hoarding related species have a larger HF than non-hoarding groups [17,18]. At intraspecific level several findings reveal that populations where caching behavior is observed more often tend to have larger HF than populations that depend less on hoarded food [20,21]. In addition, several studies have shown a link between sex differences in hippocampal size and differences in the use of spatial information in breeding contexts in birds [22], mammals [23] and fish [24]. Sexually dimorphic neural phenotypes have been observed to occur in species where both sexes have strategies involving different use of space or memory demands. For example, in golden-collared manakins (Manacus vitellinus), males perform complex spatial courtship displays and exhibit larger hippocampus and areas related with motor display, while females have a larger ventrolateral mesopallium, which possibly facilitates visual processing in selecting male display traits [25]. Nectarivorous vertebrates, such as hummingbirds, experience a scenario comparable to scattered-hoarding species in which the assessment of nectar quality of individual flowers widely distributed over their home range cannot occur by visual inspection alone, but only after exploitation [26]. Thus, since nectar-rich flowers vary in their concentration, renewal rate and spatial location [27,28], the ability of hummingbirds to remember where and when nectar-rich flowers will be available results in higher energy rewards than in subjects with poorer memory abilities [29,3]. Recently, we showed that free-living male hummingbirds are able to remember when (i.e., time) and where (i.e., location) the nectar would be available and are able to match their visits to nectar availability [30]. In several hummingbird species the HF size relative to telencephalic volume has been described two to five times larger than the HF other avian species, even if they are caching songbirds [31] which is consistent with hummingbirds cognitive performance. However, whether memory abilities or HF vary between sexes in hummingbirds is currently unknown. Most hummingbird species (Trochilidae) show morphological and behavioral sexual dimorphisms, mainly related to differences in foraging ecology and resource exploitation strategies [32]. In the green-backed firecrown (Sephanoides sephaniodes) males are larger than females and actively defend feeding territories. Females, in turn, are opportunistic [33] and exploit flowers scattered throughout several patches performing rapid intrusions into male territories, as they are aggressively chased away by territorial males during the non-reproductive season [34]. Moreover, females have higher energetic expenditure due to their smaller body size - which implies higher thermoregul (...truncated)