Although many animal species have demonstrated an ability to differentiate between more and less when presented with different amounts of food, they have done so primarily using vision. In this study, by contrast, elephants showed that they can detect differences between various quantities of food using only their sense of smell. Thus, elephants may be unique in their use of olfaction in cognitive tasks. This research suggests that it is important for psychologists to incorporate into experimental designs the ways in which different animals interact with their environment using all of their senses. Such species-specific paradigms would ensure comparisons about cognition across taxa are fair and relevant.

Animals often face situations that require making decisions based on quantity. Many species, including humans, rely on an ability to differentiate between more and less to make judgments about social relationships, territories, and food. Habitat-related choices require animals to decide between areas with greater and lesser quantities of food while also weighing relative risk of danger based on group size and predation risk. Such decisions can have a significant impact on survival for an animal and its social group. Many species have demonstrated a capacity for differentiating between two quantities of food and choosing the greater of the two, but they have done so based on information provided primarily in the visual domain. Using an object-choice task, we demonstrate that elephants are able to discriminate between two distinct quantities using their olfactory sense alone. We presented the elephants with choices between two containers of sunflower seeds. The relationship between the amount of seeds within the two containers was represented by 11 different ratios. Overall, the elephants chose the larger quantity of food by smelling for it. The elephants’ performance was better when the relative difference between the quantities increased and worse when the ratio between the quantities of food increased, but was not affected by the overall quantity of food presented. These results are consistent with the performance of animals tested in the visual domain. This work has implications for the design of future, cross-phylogenetic cognitive comparisons that ought to account for differences in how animals sense their world.

At the grocery store, the “10 items or less” checkout line is always the shortest; as we go to pay for our goods, we quickly check our cart to see if we qualify. Whether we are shopping for groceries or splitting a bill at dinner, we make decisions daily based on quantities. Many studies have investigated our own capacity for understanding numbers and discriminating between relative and absolute quantities (1, 2). The ability to differentiate between two different quantities is evolutionarily significant, as animals rely on quantity judgment to make routine decisions that impact their physical and social lives. For example, they may select habitats with greater food resources (3), pursue larger groups of prey (4), seek locations with more potential mates (5), or assess group size when challenging conspecific competitors or defending against predators (6⇓⇓–9).

In tasks that ask an animal to differentiate between two different amounts of food (an individual may be presented with these different quantities based on predetermined ratios, for example, 1:2 or 3:4), species generally perform well, making relative quantity judgments in favor of the larger quantity [e.g., nonhuman primates (10⇓–12), pinnipeds and cetaceans (13, 14), birds (15, 16), canines (17), bears (18), elephants (19⇓–21)]. Remarkably, however, quantity discrimination testing has almost always focused on the visual domain [but see studies on beetles (22) and voles (23) that tested for this capacity in a limited social, olfactory context, on chimpanzees for tests in the auditory domain (24), and on dogs for tests in which they failed to differentiate quantities of food when they could smell but not see it (25)]. This tendency is largely due to the field of comparative cognition’s long history of drawing species-level comparisons from a primate-centric, and thus primarily visual, perspective (26). The result is that it becomes difficult to draw direct comparisons across taxa; failure on a given cognitive task may be due not to a lack of a capacity but to an experimental bias that assumes a particular animal relies on vision.

Most investigations into how complex cognition has evolved convergently in taxa that have no recent common ancestor have centered on animals that share comparable visual perspectives, such as nonhuman primates and corvids (27, 28). But, as large-brained, socially complex animals, elephants are also an interesting model species for psychologists interested in convergent cognitive evolution. In addition, studying the elephant’s capacity for quantity discrimination has ecological validity. Elephants often travel to find high-quality food and water, depending on seasonal availability, social status, human risk, and environmental change (29⇓–31). It would thus be evolutionarily advantageous for them to be able to make calculated decisions about food availability that result in the conservation of time and energy.

However, while elephants do use vision [for example, in close, social contexts where they may react to each other’s body language (32)], they use it primarily as a complement to their more dominant senses of hearing, smell, and touch. This sensory difference makes it challenging to design experiments to investigate the elephant’s cognition (33⇓–35). In previous quantity-discrimination tasks based on visual cues, elephant studies have produced conflicting results (19⇓–21). In addition, while it is well-documented that elephants use a complex array of acoustic signaling in social communication (36⇓–38), their sense of smell and how they use it to navigate their physical environment has received little attention to date (but see refs. 34 and 39⇓⇓–42). Thus, we investigated whether elephants have the capacity for quantity discrimination in a sensory domain of high ecological relevance to them: olfaction.

Results and Discussion

We tested six Asian elephants (Elephas maximus) for their capacity to make relative quantity judgments using olfactory information alone at a facility in northern Thailand (SI Appendix, Tables S1 and S2). The elephants in this study are captive animals living in a tourism-based facility with a high degree of animal welfare standards and a full-time veterinary staff. A sliding table was used to present each subject with two buckets containing a varying amount of sunflower seeds. First, the elephants had an opportunity to smell the two locked buckets on the table through perforated lids. Then, the buckets were withdrawn, unlocked, and presented again so the elephants could choose one of the two (Fig. 1). The elephants were first pretested to ensure that they could recognize 4 g of sunflower seeds—the smallest amount of food tested across the study—and would choose this quantity over none. The elephants all reached criterion (80% correct within a set of 12 trials) in three or fewer sets (mean = 1.67 sets). Next, the elephants were given a “solid-lid” control condition to rule out the potential effect of the elephants perceiving nonolfactory information about the quantities of food presented (one set of 12 trials with solid lids only, 24 g of seeds vs. none). They were then trained on a small ratio (1:8, i.e., 4 vs. 32 g of seeds) to ensure that they understood that both buckets could contain food [these elephants had extensive previous experience with object-choice tasks in which only one bucket had food (34, 43)]. The elephants all reached criterion (80% correct within a set of 12 trials) in eight or fewer sets (mean = 2.67 sets).

Fig. 1. General setup during the experimental condition. (A) Two experimenters pushed the sliding table containing two buckets up to the elephant so that he/she could investigate each bucket using his/her trunk alone. (B) In the investigation phase of each trial, the bucket lids were locked and opaque, so that the only sensory information the elephants could gather about the food was olfactory and they could only gather this information by smelling through the small holes in the bucket lids. (C) After smelling the bucket lids, the table was withdrawn and then, after the lids were unlocked and replaced with upside-down solid lids, pushed back up to the elephant again so he/she could make a choice by removing the lid of a single bucket. (D) The elephant’s eye view of a bucket after a choice had been made shows a small container with sunflower seeds, an inner, orange pail to prevent visual information from being obtained from the outside, and an outer, opaque bucket onto which the lids were attached. Illustrations by Nuttayapond Doungcharoen (artist).

The elephants then proceeded to complete experimental test trials in which we investigated whether they could discriminate between pairs of quantities by smell. Six test quantities (multiples of 4 g up to 24 g of seeds) were used. We constructed the overall experiment to evaluate the elephants’ performance distinguishing between pairs of quantities with varying ratio values (e.g., 12 g vs. 16 g has a ratio value of 3:4 or 0.75) and varying ratio disparities (i.e., the absolute difference between the two numbers in the ratio; the ratio 1:3 has a disparity of 2 units, for instance). Subjects completed 10 sets, with each set consisting of one trial of each of the 11 ratios produced by pairing the six test quantities (1:2, 1:3, 1:4, 1:5, 1:6, 2:3, 2:5, 3:4, 3:5, 4:5, 5:6). For three of these ratios (1:2, 1:3, 2:3), multiple pairings of the six test quantities were possible; for example, 1:2 could be presented as 4 g vs. 8 g or 12 g vs. 24 g. Given this, each subject completed five sets with the lower-quantity pairings for these three ratios (4 g vs. 8 g for 1:2; 4 g vs. 12 g for 1:3; 8 g vs. 12 g for 2:3) and five sets with the higher-quantity pairings for these three ratios (12 g vs. 24 g for 1:2; 8 g vs. 24 g for 1:3; 16 g vs. 24 g for 2:3). The use of different quantities of the same ratio allowed us to determine whether the total quantity or magnitude of food present influenced the elephants’ performance. Although a third pairing (8 g vs. 16 g) was possible for the ratio 1:2, we chose not to test this intermediate pairing to standardize analysis by including two pairings for each of the three ratios. For 1:2, to increase the odds of identifying an existing magnitude effect, we opted to use the two pairings with the greatest discrepancy between them (4 g vs. 8 g compared with 12 g vs. 24 g).

After all 10 sets of the experimental condition, the subjects completed four different conditions in the following order: (i) a repeat of the solid-lid condition to determine if the elephants had learned to follow any inadvertent cues about the food’s location (one set of 12 “0 g vs. 24 g” trials), (ii) a “metal-bucket” condition that controlled for potential confounds of residual olfactory cues in the plastic testing buckets by testing in metal buckets instead (two sets of the 11 different ratio trials), (iii) a “double-blind” condition that controlled for the potential of an experimenter cuing inadvertently toward the greater quantity by ensuring the experimenters at the sliding table did not know which bucket contained which quantity (two sets of the 11 different ratio trials), and (iv) a “residual-odor” condition that further controlled for the potential effect of accumulated residual odor within the baited containers used in the test trials (two sets of 12 “14 g vs. 14 g” trials). These conditions were conducted after the experimental condition for two reasons: (i) to avoid confusion on the part of the elephants due to too many changes to the paradigm in the middle of the experiment, and (ii) in the case of the metal-bucket and double-blind conditions, to confirm that the results would be consistent regardless of bucket material and experimenter bias, respectively.

To analyze the elephants’ success in choosing the higher quantity by both ratio value and ratio disparity, we constructed two logistic regression mixed models to test for an effect of each (see Materials and Methods for details). The modeling approach we used included data from all trials and used a random term for individual ID to allow for variation between individuals in intercept. This retains the structure of the experimental design and, subsequently, none of the models failed to converge (see SI Appendix, Statistical Analyses for details on nonsignificant covariate terms).

The experimental, metal-bucket, and double-blind condition sets each consisted of one trial of each of the 11 ratios, and thus were included alongside all other trials in the models and analyzed as a factor with three levels. First, there was no significant difference between success in the experimental condition and either the metal-bucket or double-blind conditions across trials [success/ratio model: likelihood ratio test (LRT) χ2 = 0.29, df = 2, P = 0.87; success/disparity model: LRT χ2 = 0.33, df = 2, P = 0.85], indicating that success for the elephants was not affected by container type or experimenter cues. This allowed us to look at success by ratio, disparity, and magnitude across all three of these conditions combined.

Overall, the elephants chose the greater quantity of food across the different ratio values using olfaction alone. The likelihood of success (selecting the bucket with more food) over the 154 trials varied significantly by ratio (Fig. 2 and SI Appendix, Table S3). Specifically, the elephants’ likelihood of success decreased as the quantities of food in the ratio became closer (i.e., the overall ratio value approached 1; likelihood ratio test for model with terms for linear and quadratic ratio and model without those terms: χ2 = 21.86, df = 2, P < 0.0001). When testing the model with both linear and quadratic terms for ratio against the model with a linear term only, there was no significant difference, indicating a linear relationship between food ratio and success (SI Appendix, Table S3; LRT χ2 = 0.14, df = 1, P = 0.70). The elephants as a group scored significantly better than chance on 5 out of 11 ratios (1:3, 1:5, 1:6, 2:5, 3:5; SI Appendix, Table S1). Although none of the covariates in the model significantly improved the model fit, sex (male vs. female) was significant within the ratio model (SI Appendix, Table S3).

Fig. 2. Probability of success by ratio of food as a decimal value. Points indicate raw data, while the line represents predicted values based on the model of success by ratio. Both raw data and predicted probabilities are displayed, with the former shown by individual elephant. Shaded coloration indicates predicted variation in success around each ratio based on the model. Raw data are indicated by symbol, with each elephant represented only once at each ratio value.

To assess magnitude effects, we compared whether the elephants performed differently when presented with single vs. double or triple (e.g., 4 g vs. 12 g and 8 g vs. 24 g, or 4 g vs. 8 g and 12 g vs. 24 g) versions of the same food ratios in the experiments (e.g., 1:3 and 1:2, respectively). Magnitude was a nonsignificant term [LRT χ2 = 1.18, df = 1 (as the variable was treated as a two-level factor with levels single and double/triple), P = 0.28], indicating that at the same ratio, the combined magnitude of food presented did not influence the likelihood of success.

We also tested for an association between probability of success and disparity between the two food quantities. Results showed that overall, the elephants’ likelihood of success varied significantly across different pairwise disparities; there was a significant increase in success as disparity increased (LRT χ2 = 27.70, df = 1, P < 0.0001; Fig. 3 and SI Appendix, Table S4). As in the ratio model, none of the covariates in the disparity model significantly improved the model fit, but sex (male vs. female) was significant within the disparity model as well (SI Appendix, Table S4).

Fig. 3. Probability of success by disparity of food quantities. Points indicate raw data, while the line represents predicted values based on the model of success by disparity. Both raw data and predicted probabilities are displayed, with the latter shown by individual elephant. Shaded coloration indicates predicted variation in success around each disparity based on the model. Raw data are indicated by symbol; each elephant may be represented more than once at each disparity, as several ratio values shared the same disparity. A jitter of 0.1 has been added to better visualize the data points, but all disparities are whole-number values.

The solid-lid (0 g vs. 24 g) and residual-odor (14 g vs. 14 g) control conditions tested the same ratios across all trials. Thus, these conditions were analyzed separately from the aforementioned models. With the solid-lid condition, we were interested in whether the elephants could find food when olfactory information was obstructed (i.e., odors from the food currently present in the bucket were trapped under a solid lid). With the residual-odor condition, we were interested in whether the elephants could find food when olfactory information was manipulated (i.e., different amounts of residual odor from previously stored food were introduced). The elephants performed significantly better with the ratio 1:6 (the next-largest disparity after 0:6) across the experimental + metal-bucket + double-blind conditions (mean = 12/14, SD = 1.79) than they did in the solid-lid control (Wilcoxon paired-samples test, one-tailed: W = 21, n = 6, P = 0.016). One-tailed tests were used for Wilcoxon tests because of strong a priori predictions that elephants would score significantly better on experimental than control trials, specifically due to the fact that the latter aimed to exclude or control for the olfactory cues that we predicted would promote the elephants’ ability to discriminate quantity. As a group, their mean performance on solid-lid controls of 12.17 out of 24 trials correct (SD = 1.94) approximated chance levels (12 out of 24 trials correct), suggesting the elephants could not find the greater quantity when olfactory information was occluded. When comparing the mean success for each elephant across all of the ratios in the experimental + metal-bucket + double-blind conditions with their success in the residual-odor control, the elephants as a group performed significantly better in the former (W = 19, n = 6, P = 0.031). As a group, their mean performance of 12.5 out of 24 trials correct (SD = 1.76) on residual-odor trials approximated chance levels (12 out of 24 trials correct), suggesting the elephants could not perceive an olfactory difference when the same food quantities were presented within two buckets that had accumulated disparate residual odors.

Our findings show that elephants are able to discriminate between quantities using olfactory information alone. As a group, the elephants’ performance was worse with an increase in ratio value, better with an increase in ratio disparity, and remained consistent when the magnitude of the quantities increased at the same ratio. Thus, using olfaction, the elephants performed similarly to other species tested with vision and appeared to both make approximations about food quantity and recognize the relative difference between two amounts (44⇓–46). Prior research suggests that animals are able to cognitively represent quantity through approximation, and thus recognize the relative difference between two amounts rather than the exact quantity each represents (e.g., refs. 44 and 45). An alternative, yet not necessarily mutually exclusive, model, referred to as “object file,” suggests that individuals can represent small numbers (four or less) as separate memory files and thus differentiate smaller quantities as exact amounts rather than as approximations (47). Interestingly, previous results for elephants were mixed in this regard. Some research suggests that Asian elephants may have a larger object-file capacity (19) or some other unique counting mechanism (21) that may allow for greater precision within quantity judgments. On the other hand, two studies on African elephants (20, 48) suggest that the elephants perform similarly, through approximation, to other animals. Most importantly, Irie-Sugimoto et al. (19) and Irie et al. (21) argue that Asian elephants’ performance on relative quantity judgments do not seem to be affected by disparity, magnitude, or ratio value.

Our results, however, follow the approximation model and thus Weber’s law; the elephants’ performance increased as the disparity increased, but increases in magnitude were not associated with diminished performance. Thus, our research shows that within the olfactory domain, the Asian elephants’ performance is similar to most other species tested in the visual domain. Differences in the results across these studies on Asian and African elephants may be due to discrepancies in methodology or possible species-level differences (19⇓–21, 48), but our research suggests that greater attention to olfaction is nonetheless needed in cognitive tasks across elephant species.

In terms of biological variables that could be associated with success in the experiments, none of the covariates in the models, including age and sex, significantly improved the models’ fit. Sex (male vs. female), however, was significant within both the ratio and disparity models (SI Appendix, Tables S3 and S4). Although it is difficult to interpret these results given the small sample size, this would be a very interesting area for future research with a larger sample size of both males and females. If this sex difference exists in the wild, it may be due to sex-specific nutritional and reproductive differences: Larger-bodied male elephants may have consistently greater energy needs (excluding the high-energy periods of peak lactation and gestation in females) and need to locate estrous females over long distances (7, 49, 50). If these are contributing factors, the potential sex differences in quantity discrimination may either disappear or reverse in social olfactory tasks due to the female-centric nature of elephant social dynamics.

Interestingly, an animal’s ability to count or approximate the quantity of objects in an array likely differs mechanistically between the visual and olfactory domains (51). While an exact count of discrete objects (e.g., sunflower seeds) is possible visually, it seems unlikely that an object’s odor could be “countable” as a discrete unit. Olfaction is also a difficult domain in which to test cognition because, unlike vision, olfactory information cannot easily be removed following its presentation. One additional concern we had in implementing this study was that residual olfactory information could have hindered each elephant’s ability to choose larger quantities across trials. The elephants’ poor performance on the residual-odor condition and nonsignificant difference in performance between the experimental and metal-bucket conditions, however, suggest this was not the case. The results across all four control conditions indicate the elephants (i) were only using olfactory information presented in the buckets to find food (the solid-lid condition), (ii) were not using inadvertent cues provided by the experimenters (the double-blind condition), and (iii) were not affected by olfactory cues other than those resulting from the actual presence of the two different quantities of sunflower seeds (the metal-bucket and the residual-odor conditions). These results, taken together, suggest the elephants were able to discriminate between the two discrete quantities using only the olfactory difference between them.

The primary purpose of this study was to investigate whether or not the elephants could discriminate quantity using smell; one remaining question is how they did it. One potential answer to this question is that the elephants simply smelled the quantity closer to their trunk, as the higher quantities would be slightly higher in the bucket. This is unlikely, given their success on relatively small differences in the presented quantities where the height difference was negligible. In addition, in a post hoc control done with two of the tested elephants in which we raised presented quantities to the same height within the buckets, the elephants still chose the larger quantity significantly above chance (both Bleum and Lanna chose the larger quantity in 19 of 24 trials: binomial test, P = 0.007). Future research would be crucial in understanding the precise mechanisms that elephants and other olfactory animals use to discriminate quantities, and the ecological significance of such an ability. For instance, elephants’ acute sense of smell could help them make important foraging and social decisions from far-enough distances so as to mitigate potential risk in human-dominated landscapes (52). It would also be important to study these effects in wild elephants, as the current study focused on captive animals living in unique environments with access to diverse food resources provided by human caretakers. Although we expect that the capacity for olfactory-based relative quantity judgment would be consistent across individuals within the Asian elephant species regardless of life experience, differences in how this capacity is expressed and how it affects the elephant’s decision-making process would be interesting to compare in wild and captive animals.

As the study of cognition in animals continues to grow as a field, it is becoming increasingly important that experimental designs become more species-specific. Research into the minds of animals should account for differences in sensory perspectives to ensure fair comparisons of cognitive capacity, rather than rely on approaches that are unfairly biased toward the primate-centric, visual perspective. In addition, understanding how elephants use their sense of smell in the cognitive decision-making process could be applied to human–elephant conflict-mitigation strategies in Asia and Africa that must balance the ecological and behavioral needs of both humans and elephants to be successful in the long term (52).