Serial visual reversal learning in captive black-handed spider monkeys, Ateles geoffroyi.

Recent research suggests that socio-ecological factors such as dietary specialization and social complexity may be drivers of advanced cognitive skills among primates. Therefore, we assessed the ability of 12 black-handed spider monkeys (Ateles geoffroyi), a highly frugivorous platyrrhine primate with strong fission-fusion dynamics, to succeed in a serial visual reversal learning task. Using a two-alternative choice paradigm we first trained the animals to reliably choose a rewarded visual stimulus over a non-rewarded one. Upon reaching a pre-set learning criterion we then switched the reward values of the two stimuli and assessed if and how quickly the animals learned to reverse their choices, again to a pre-set learning criterion. This stimulus reversal procedure was then continued for a total of 80 sessions of 10 trials each. We found that the spider monkeys quickly learned to reliably discriminate between two simultaneously presented visual stimuli, that they succeeded in a visual reversal learning task, and that they displayed an increase in learning speed across consecutive reversals, suggesting that they are capable of serial reversal learning-set formation with visual cues. The fastest-learning individual completed five reversals within the 80 sessions. The spider monkeys outperformed most other primate and nonprimate mammal species tested so far on this type of cognitive task, including chimpanzees, with regard to their learning speed in both the initial learning task and in the first reversal task, suggesting a high degree of behavioral flexibility and inhibitory control. Our findings support the notion that socio-ecological factors such as dietary specialization and social complexity foster advanced cognitive skills in primates.

Edge effects and social behavior in three platyrrhines.

Social behavior is a key adaptation for group-living primates. It is important to assess changes to social behavior in human-impacted landscape zones to better understand the impact of anthropogenic disturbance on primate species. We investigated social behavior rate and type in three species of platyrrhines across 100 m anthropogenic edge and interior zones of a fragmented forest in Costa Rica, La Suerte Biological Research Station (LSBRS). Following results from other sites, we predicted that spider monkeys (Ateles geoffroyi), capuchin monkeys (Cebus imitator) and howler monkeys (Alouatta palliata) would show lower rates and fewer types of social behavior in forest edge compared to interior. We collected 1341 h of instantaneous focal data from 2017 to 2023 across the three monkey species. We found mixed support for our predictions, with spider and capuchin monkeys modifying some but not all aspects of social behavior across forest zones at LSBRS. Spider monkeys had lower rates of social behavior and capuchin monkeys performed different types of social behaviors in forest edge compared to interior at LSBRS. In contrast, howler monkeys did not modify social behavior. Two out of three platyrrhine species altered their social behavior when in anthropogenic edges, indicating behavioral adjustment when in human-altered habitat areas at LSBRS.

Evaluating Thermal Infrared Drone Flight Parameters on Spider Monkey Detection in Tropical Forests.

Geoffroy's spider monkeys, an endangered, fast-moving arboreal primate species with a large home range and a high degree of fission-fusion dynamics, are challenging to survey in their natural habitats. Our objective was to evaluate how different flight parameters affect the detectability of spider monkeys in videos recorded by a drone equipped with a thermal infrared camera and examine the level of agreement between coders. We used generalized linear mixed models to evaluate the impact of flight speed (2, 4, 6 m/s), flight height (40, 50 m above ground level), and camera angle (-45°, -90°) on spider monkey counts in a closed-canopy forest in the Yucatan Peninsula, Mexico. Our results indicate that none of the three flight parameters affected the number of detected spider monkeys. Agreement between coders was "substantial" (Fleiss' kappa coefficient = 0.61-0.80) in most cases for high thermal-contrast zones. Our study contributes to the development of standardized flight protocols, which are essential to obtain accurate data on the presence and abundance of wild populations. Based on our results, we recommend performing drone surveys for spider monkeys and other medium-sized arboreal mammals with a small commercial drone at a 4 m/s speed, 15 m above canopy height, and with a -90° camera angle. However, these recommendations may vary depending on the size and noise level produced by the drone model.

Should I stay or should I go? How activity synchronization affects fission decisions.

Group-living animals need to deal with conflicting interests to maintain cohesion. When the costs of doing so outweigh the benefits, the group may (temporarily) split into two or more subgroups. Conflicting interests can concern what activity to pursue or the direction of travel. Temporary group separation is a common feature in species with a high degree of fission-fusion dynamics. We investigated the role activity synchronization played in fission decisions in a spider monkey group living in the Otoch Ma'ax Yetel Kooh Nature Reserve, Yucatan, Mexico. For 21 months, we recorded every fission event occurring in the followed subgroup, as well as the subgroup activity. We classified the activity as 'synchronized' when at least 75% of subgroup members performed the same activity (resting, foraging, socializing or travelling); otherwise, we classified it as 'non-synchronized'. We found that fission events occurred more often when the activity was non-synchronized. In addition, when the activity was synchronized, fission events occurred more often when spider monkeys were travelling than when they were engaged in other subgroup activities. Our findings highlight the role of conflicting interests over the activity to pursue and travel direction in fission decisions.

DIFFUSE IDIOPATHIC SKELETAL HYPEROSTOSIS WITH SECONDARY DYSPHAGIA IN A BLACK-HANDED SPIDER MONKEY (ATELES GEOFFROYI).

A 32-yr-old male black-handed spider monkey (Ateles geoffroyi) with marked kyphosis and reduced spinal range of motion developed intermittent regurgitation, which was managed with an acid reducer. Diffuse idiopathic skeletal hyperostosis (DISH) was suspected in this animal due to radiographically evident ossification of the anterior longitudinal ligament. At repeat radiographic evaluation 1.5 yr later, due to weight loss and increased frequency of regurgitation, the cervical spine was deviated ventrally and appeared to be impinging on the thoracic inlet. The spider monkey was humanely euthanized due to poor prognosis, and the presumptive diagnosis of DISH was confirmed via postmortem computed tomography and necropsy. DISH has not been reported in black-handed spider monkeys, and secondary dysphagia, an uncommon but recognized consequence in humans, has not been reported in a nonhuman primate. Earlier recognition of this possibly underreported disease process may increase treatment options and effectiveness of intervention.

Taste Responsiveness of Spider Monkeys to Dietary Ethanol.

Recent studies suggest that frugivorous primates might display a preference for the ethanol produced by microbia in overripe, fermenting fruit as an additional source of calories. We, therefore, assessed the taste responsiveness of 8 spider monkeys (Ateles geoffroyi) to the range of ethanol concentrations found in overripe, fermenting fruit (0.05-3.0%) and determined taste preference thresholds as well as relative taste preferences for ethanol presented in sucrose solutions and in fruit matrices, respectively. Using a 2-bottle preference test of short duration (1 min), we found that spider monkeys are able to detect ethanol concentrations as low as 0.5%, that they prefer ethanol concentrations up to 3% over water, and that they prefer sucrose solutions and pureed fruit spiked with ethanol over equimolar sucrose solutions and pureed fruit without ethanol. However, when presented with an ethanol-spiked sucrose solution and a higher-concentrated sucrose solution without ethanol, the animals clearly preferred the latter, even when the sucrose-ethanol mixture contained 3 times more calories. These results demonstrate that spider monkeys are more sensitive to the taste of ethanol than rats and humans and that they prefer ecologically relevant suprathreshold concentrations of ethanol over water. Tests with sucrose solutions and pureed fruits that were either spiked with ethanol or not suggest that sweetness may be more important for the preferences displayed by the spider monkeys than the calories provided by ethanol. The present results, therefore, do not support the notion that dietary ethanol might be used by frugivorous primates as a supplemental source of calories.

Clostridium difficile Enterocolitis in a Captive Geoffroy's Spider Monkey (Ateles geoffroyi) and Common Marmosets (Callithrix jacchus).

Clostridium difficile is a well-documented cause of enterocolitis in several species, including humans, with limited documentation in New World nonhuman primates. We report several cases of C. difficile-associated pseudomembranous enterocolitis, including a case in a Geoffroy's spider monkey (Ateles geoffroyi) and several cases in common marmosets (Callithrix jacchus). The histologic lesions included a spectrum of severity, with most cases characterized by the classic "volcano" lesions described in humans and several other animal species. C. difficile was isolated from the colon of the spider monkey, while the presence of toxin A or toxin B or of the genes of toxin A or B by polymerase chain reaction served as corroborative evidence in several affected marmosets. C. difficile should be considered a cause of enterocolitis in these species.

Contrasting Rates of LINE-1 Amplification among New World Primates of the Atelidae Family.

LINE-1 (L1) retrotransposons constitute the dominant category of transposons in mammalian genomes. L1 elements are active in the vast majority of mammals, and only a few cases of L1 extinction have been documented. The only possible case of extinction in primates was suggested for South American spider monkeys. However, these previous studies were based on a single species. We revisited this question with a larger phylogenetic sample, covering all 4 genera of Atelidae and 3 species of spider monkeys. We used an enrichment method to clone recently inserted L1 elements and performed an evolutionary analysis of the sequences. We were able to identify young L1 elements in all taxa, suggesting that L1 is probably still active in all Atelidae examined. However, we also detected considerable variations in the proportion of recent elements indicating that the rate of L1 amplification varies among Atelidae by a 3-fold factor. The extent of L1 amplification in Atelidae remains overall lower than in other New World monkeys. Multiple factors can affect the amplification of L1, such as the demography of the host and the control of transposition. These factors are discussed in the context of host life history.

Determination of vertebral heart score in three species of Spider monkey (Ateles fusciceps, A. hybridus and A. paniscus).

BACKGROUND: The vertebral heart score (VHS) is a method of evaluation of cardiac size well documented in domestic mammals and in other primate species, and the aim of this study was to determine the VHS in three species of Spider monkey. METHODS: In this retrospective study, right lateral radiographs of thirty clinically well animals were reviewed and VHS determined. The species included were Ateles fusciceps (n=17), Ateles hybridus (n=8) and Ateles paniscus (n=5). RESULTS: The VHS was found to vary between species and was 9.73±0.81 for A. fusciceps, 10.53±0.37 for A. hybridus and 10.45±0.27 for A. paniscus. CONCLUSIONS: The observed values appear consistent with values determined for other primate species. There was statistically significant variation noted between species, and so VHS should be considered species-specific in this genus. The values determined may be of benefit in objectively evaluating cardiac size in the species investigated.

Homosexual Behavior Between Male Spider Monkeys (Ateles geoffroyi).

Homosexual behavior is defined as genital contact or genital manipulation between same-sex individuals. In nonhuman primates, it may regulate social relationships by serving as a means of reconciliation, tension alleviation, or alliance formation. Grappling is a rare and complex behavior, which most frequently occurs between same-sex individuals of the genus Ateles and can include mutual manipulation of the genitalia. Here we report three cases of penile-anal intromission during grappling between wild male spider monkeys living in the natural protected area of Otoch Ma'ax Yetel Kooh, Mexico. In all the observed cases, the same adult male was the actor. To our knowledge, this is the first report of penile-anal intromission between males in any New World primate species.

Predation Attacks on Wild Spider Monkeys (Ateles geoffroyi).

We report 2 cases of predation on an adult and a subadult spider monkey (Ateles geoffroyi) by a puma (Puma concolor) and an unidentified terrestrial predator at the natural protected area of Otoch Ma'ax yetel Kooh, in the Yucatan Peninsula, Mexico. Although spider monkeys are believed to experience overall low predation pressure compared to other primate species, our observations show that predation occurs in the study area and therefore behavioral strategies are likely to be in place to reduce predation risk. Our observations are further evidence that terrestrial predators are a threat for both young and full-grown spider monkeys.

Ancestral resurrection of anthropoid estrogen receptor ß demonstrates functional consequences of positive selection.

Anthropoid primates arose during the Eocene approximately 55 million years ago (mya), and extant anthropoids share a most recent common ancestor ∼40mya. Paleontology has been very successful at describing the morphological phenotypes of extinct anthropoids. Less well understood is the molecular biology of these extinct species as well as the phenotypic consequences of evolutionary variation in their genomes. Here we resurrect the most recent common ancestral anthropoid estrogen receptor ß gene (ESR2) and demonstrate that the function of this ancestral estrogen receptor has been maintained during human descent but was altered during early New World monkey (NWM) evolution by becoming a more potent transcriptional activator. We tested hypotheses of adaptive evolution in the protein coding sequences of ESR2, and determined that ESR2 evolved via episodic positive selection on the NWM stem lineage. We separately co-transfected ESR2 constructs for human, NWM, and the anthropoid ancestor along with reporter gene vectors and performed hormone binding dose response experiments that measure transactivation activity. We found the transactivation potentials of the ancestral and human sequences to be significantly lower (p<0.0001 in each comparison) than that of the NWM when treated with estradiol, the most prevalent estrogen. We conclude the difference in fold activation is due to positive selection in the NWM ERß ligand binding domain. Our study validates inferential methods for detecting adaptive evolution that predict functional consequences of nucleotide substitutions and points a way toward examining the functional consequences of positive Darwinian selection.

Sustainability and comanagement of subsistence hunting in an indigenous reserve in Guyana.

Although hunting is a key component of subsistence strategies of many Amazonians, it is also one of the greatest threats to wildlife. Because indigenous reserves comprise over 20% of Amazonia, effective conservation often requires that conservation professionals work closely with indigenous groups to manage resource use. We used hunter-generated harvesting data in spatially explicit biodemographic models to assess the sustainability of subsistence hunting of indigenous Waiwai in Guyana. We collected data through a hunter self-monitoring program, systematic follows of hunters, and semistructured interviews. We used these data to predict future densities of 2 indicator species, spider monkeys (Ateles paniscus) and bearded sakis (Chiropotes sagulatus), under different scenarios of human population expansion and changing hunting technology. We used encounter rates from transect surveys and hunter catch-per-unit effort (CPUE) to validate model predictions. Paca (Cuniculus paca) (198 /year), Currosaw (Crax alector) (168), and spider monkey (117) were the most frequently harvested species. Predicted densities of spider monkeys were statistically indistinguishable from empirically derived transect data (Kolmogorov-Smirnov D = 0.67, p = 0.759) and CPUE (D = 0.32, p = 1.000), demonstrating the robustness of model predictions. Ateles paniscus and C. sagulatus were predicted to be extirpated from <13% of the Waiwai reserve in 20 years, even under the most intensive hunting scenarios. Our results suggest Waiwai hunting is currently sustainable, primarily due to their low population density and use of bow and arrow. Continual monitoring is necessary, however, particularly if human population increases are accompanied by a switch to shotgun-only hunting. We suggest that hunter self-monitoring and biodemographic modeling can be used effectively in a comanagement approach in which indigenous parabiologists continuously provide hunting data that is then used to update model parameters and validate model predictions.

How Survey Design Affects Monkey Counts: A Case Study on Individually Recognized Spider Monkeys (Ateles geoffroyi).

The fast movement and high degree of fission-fusion dynamics of spider monkeys (Ateles spp.) make them notoriously difficult to survey. We examined which aspects of survey design affect spider monkey sightings along transects in a group of individually recognized spider monkeys (Ateles geoffroyi) in Punta Laguna, Yucatan, Mexico. We calculated the number of monkeys and subgroups sighted per transect walk. Using generalized linear models, we found no effect of the number of observers, transect type (new vs. existing), walking speed, or time of day on individual monkey counts or subgroup counts. Recounting of individuals was relatively rare and occurred when transects were walked relatively slowly. We missed more young than adult monkeys. The group composition based on survey data was similar to the known group composition. Based on our findings we recommend that surveys performed on relatively flat terrain be conducted at speeds similar to or faster than the moving speed of spider monkeys to minimize recounting of individuals and that young:adult female ratios based on survey data be interpreted as conservative indicators of population health. The novel methods presented to determine sources of bias in population estimates are applicable to a wide range of primates that are difficult to survey.

Measuring stress responses in female Geoffroy's spider monkeys: Validation and the influence of reproductive state.

Fecal glucocorticoid metabolites are increasingly used to investigate physiological stress. However, it is crucial for researchers to simultaneously investigate the effects of reproductive state because estradiol and placental hormones can affect circulating glucocorticoid concentrations. Reports on the relationships between glucocorticoids and reproductive state are inconsistent among females. Unlike several primate species that have heightened glucocorticoid activity during lactation, humans experience reduced glucocorticoid activity during lactation. Rather than a taxonomic difference, we hypothesize that this is a result of different environmental stressors, particularly the threat of infanticide. Here, we expand the number of wild primate species tested by validating a glucocorticoid assay for female Geoffroy's spider monkeys. We investigate the effects of reproductive state on their glucocorticoid concentrations. Utilizing a routine veterinary exam on a captive population, we determined that fecal glucocorticoid metabolites increase in response to a stressor (anesthesia), and this rise is detected approximately 24 hr later. Additionally, we found that extracted hormone patterns in a wild population reflected basic reproductive biology-estradiol concentrations were higher in cycling than lactating females, and in lactating females with older offspring who were presumably resuming their cycle. However, we found that estradiol and glucocorticoid concentrations were significantly correlated in lactating but not cycling females. Similarly, we found that reproductive state and estradiol concentration, but not stage of lactation, predicted glucocorticoid concentrations. Unlike patterns in several other primate species that face a relatively strong threat of infanticide, lactating spider monkeys experience reduced glucocorticoid activity, possibly due to attenuating effects of oxytocin and lower male-initiated aggression than directed at cycling females. More broadly, we conclude that future studies using fecal glucocorticoid metabolites to index stress should consider that reproductive state might confound glucocorticoid measurements. Am. J. Primatol. 77:925-935, 2015. © 2015 Wiley Periodicals, Inc.

Primate extirpation from rainforest fragments does not appear to influence seedling recruitment.

Primates are important seed dispersers, especially of large-seeded tree species, but the impact that these animals have on seedling recruitment is unclear. Evidence suggests that forest regeneration might be disrupted in forest fragments in which primates were extirpated. We tested this hypothesis by assessing seedling recruitment in 3 forest fragments occupied (OF) by primates, 3 fragments unoccupied (UF) by primates, and 3 areas within a continuous forest (CF) in the Lacandona rainforest, Mexico. Species and stem densities of tree, palm and liana seedlings were recorded over 16 months. Individuals were classified according to dispersal mode: large-seeded animal-dispersed (LS), small- and medium-seeded animal-dispersed (SS), and abiotically-dispersed species (AD). We assessed the influence of primate presence, adult tree assemblage, and fragment spatial metrics (size, age, distance to nearest fragment, and distance to continuous forest) on seedling assemblages. We recorded 6879 seedlings belonging to 90 species, and 59 genera in 405 1-m(2) plots. Both seedlings and adults showed similar differences in species and stem densities of LS, SS and AD species among forest types, suggesting that seedling assemblages were strongly influenced by the adult assemblages. The recruitment of each LS species varied among study sites, but evidence supporting higher recruitment enhancement of these species in continuous forest and occupied fragments was weak. Distance to continuous forest was the unique fragment spatial metric related (negatively) to the recruitment of LS species. Thus, primate extirpation does not appear to disrupt seedling assemblages in the Lancandona rainforest. Nevertheless, we cannot reject the hypothesis that certain LS species such as Spondias radlkoferi may be affected by the extirpation of primates.

Identification of MHC I class genes in two Platyrrhini species.

The major histocompatibility complex is a diverse gene family that plays a crucial role in the adaptive immune system. In humans, the MHC class I genes consist of the classical loci of HLA-A, -B, and -C, and the nonclassical loci HLA-E, -F, and -G. In Platyrrhini species, few MHC class I genes have been described so far and were classified as MHC-E, MHC-F, and MHC-G, with MHC-G possibly representing a classical MHC class I locus while there were arguments about the existence of the MHC-B locus in Platyrrhini. In this study, MHC class I genes were identified in eight common marmosets (Callithrix jacchus) and two brown-headed spider monkeys (Ateles fusciceps). For common marmosets, 401 cDNA sequences were sequenced and 18 alleles were detected, including 14 Caja-G alleles and 4 Caja-B alleles. Five to eleven Caja-G alleles and one to three Caja-B alleles were detected in each animal. For brown-headed spider monkeys, 102 cDNA sequences were analyzed, and 9 new alleles were identified, including 5 Atfu-G and 4 Atfu-B alleles. Two or three Atfu-G and two Atfu-B alleles were obtained for each of animal. In phylogenetic analyses, the MHC-G and -B alleles from the two species and other Platyrrhini species show locus-specific clusters with bootstrap values of 86% and 50%. The results of pairwise sequence comparisons and an excess of non-synonymous nucleotide substitutions in the PBR region are consistent with the suggestion that Caja-G and Atfu-G may be classical MHC class I loci in the Platyrrhini species… But it appears that MHC-B locus of the two Platyrrhini species shares features with both classical and nonclasical MHC class I loci. Our results are an important addition to the limited MHC immunogenetic information available for the Platyrrhini species.

Seed source, seed traits, and frugivore habits: Implications for dispersal quality of two sympatric primates.

• Premise of the study: Frugivore selection of fruits and treatment of seeds together with seed deposition site are crucial for the population dynamics of vertebrate-dispersed plants. However, frugivore species may influence dispersal quality differently even when feeding on the same fruit species and, while animals disperse some seeds, others simply fall beneath the parent plant.• Methods: In southern Mexico, we investigated to see if within-species seed traits (i.e., length, width, weight, and volume) and germination success differed according to seed source. For five tropical tree species we obtained ingested seeds from two sources, howler monkey (Alouatta pigra) and spider monkey (Ateles geoffroyi) feces; and noningested seeds from two sources, the ground and tree crowns (with predispersed seeds used as control).• Key results: A principal components' analysis showed that traits of seeds ingested by howler monkeys differed from other sources while seeds ingested by spider monkeys were similar to noningested seeds. Howlers consumed on average the larger seeds in Ampelocera hottlei, Brosimum lactescens, and Dialium guianense. Both primate species consumed the smaller seeds in Spondias mombin, while no seed trait differences among seed sources were found in Spondias radlkoferi. For all five tree species, germination rate was greatest for seeds ingested by howler monkeys.• Conclusions: For the studied plant species, seed ingestion by howler monkeys confers higher dispersal quality than ingestion by spider monkeys or nondispersal. Dispersal services of both primate species, however, are not redundant and may contribute to germination heterogeneity within plant populations in tropical forests.

A comparison of computer-generated and naturally occurring foraging patterns in route-network-constrained spider monkeys.

The attribution of goal-directed behavior to observations of primate foraging and ranging requires that simpler explanations for observed behavior patterns be eliminated. Computer-generated simulations of non-goal-directed foraging behavior can be used as null models for higher complexity cognitive foraging, and can provide quantifiable data against which to compare the observed behavioral patterns in wild primates. In this paper, we compare the results of two variations of computer simulated null models with observed foraging behavior of wild spider monkeys (Ateles belzebuth). One model simulates monkeys searching using a modified random-walk model in which monkeys alternate 100-m steps with turn angles derived from observed behavior. The second model constrains travel to an observed route system derived from observations of wild spider monkeys. Simulated monkeys in each model searched among increasing densities of feeding trees ranging from 10 to 1,000. We compared travel distance, travel directness, and accuracy of starting direction for each feeding tree discovered for the two models. We then compared these results with those derived from observations of wild spider monkeys. Route-model monkeys traveled shorter distances and more directly to feeding trees than did randomly foraging monkeys, and discovered trees in the direction they started more often. Observed spider monkeys outperformed simulated monkeys from both models in all variables, allowing us to reject the null hypothesis that observed foraging and ranging behavior could be explained by non-goal-directed travel.

Ecological factors predictive of wild spider monkey (Ateles belzebuth) foraging decisions in Yasuní, Ecuador.

Because fruiting trees are uncommon in tropical forests, frugivorous primates experience selective pressure to incorporate knowledge of where to find feeding trees, what to expect when they arrive there, and when they can return after depleting a tree. I investigated these abilities in wild spider monkeys (Ateles belzebuth) in Yasuní, Ecuador, by analyzing the characteristics of feeding trees that drive foraging decisions. Foraging data were derived from four 2-week follows of focal adult females, conducted between May and December 1999, during which I measured and mapped all trees in which the focal subject fed, feeding bout duration, and the number of conspecifics feeding simultaneously with the focal. Taking into account the order in which feeding trees were visited across each follow, I analyzed each foraging decision from the second week of a follow, treating all previously visited trees as options for visits. I scored each option tree in terms of nine ecological variables, including the distance from the decision to each location tree, DBH, recent feeding time and mean feeding times for the focal and other monkeys present, and the interval in hours between the foraging decision and the most recent visit to each option tree. I then examined the predictive strength of the model using logistic regression analysis, comparing characteristics of selected trees to those not selected. The overall model successfully predicted trees selected by focal monkeys (r(2) = 0.27). Monkeys preferentially moved to nearby, large canopy trees, in which previous feeding success was high, and which were visited after an interval of 3.5 days. Interval mattered most for medium and large trees, but did not predict selection for trees <10 cm DBH. Despite the large home range and large numbers of trees, Yasuní spider monkeys appeared to integrate spatial, value, and temporal information when deciding where to feed.