Exaggerated signaling in a solitary mammal: evidence from brown bears (Ursus arctos)

Abstract

Potential exaggeration in animal communication, though rare, challenges assumptions about the reliability of communication systems. While signals typically convey accurate information, some individuals may exaggerate their traits to gain competitive or reproductive advantages. Among mammals, scent and visual marks are primary communication modes, generally constrained by anatomy and expected to reflect body size honestly. However, manipulating these signals could help subadult or subordinate individuals avoid larger rivals. Using Cantabrian brown bears (Ursus arctos) as a model, we investigated exaggerated marking and its frequency. Over 117,552 h of camera-trap monitoring (2021 to 2024) at 14 marking sites, we recorded 164 individual bears. Seven males (4.3%) engaged in potentially exaggerated marking by climbing marking sites or using platforms to mark higher than their natural height. Of these, 57.1% were adults, and 42.9% were subadults. Elevated marking occurred at 14.3% of sites, mostly during the day. These findings suggest that brown bears can manipulate 'index signals' once considered unfakeable, adding complexity to their communication system. This study provides a cautious perspective on the dynamics of exaggerated signaling, offering insights into the evolutionary maintenance of honest communication systems in nature.

Variation in survival or reproductive success among individuals drives the emergence of evolutionary strategies that confer fitness advantages. However, because evolutionary interests may diverge during conspecific interactions, such as mating, these differences can lead to selection asymmetries between the interacting individuals (Mokkonen and Lindstedt 2016). In evolutionary stable strategies, which generally govern game-theoretical scenarios, the rules of the game depend partly on the actions of the individuals involved. But is it reasonable to assume that individuals always adhere to these rules? Anti-social behaviors, including dishonest signaling, where individuals convey signals at levels not necessarily commensurate with their quality (Dawkins and Guilford 1991) have proven to play a pivotal role in evolution (Maynard 1964). Consequently, it is crucial to consider the possibility of the emergence of novel behaviors that, relative to the previous “state of play,” violate the rules of the game (Rose 1978).

Animal communication can be conceptualized as a signaling game between 1 or multiple signalers and receivers. This process is shaped by the costs and benefits associated with signaling by senders and responding by receivers (Dawkins and Guilford 1991; Harper and Maynard 2003; Bradbury and Vehrencamp 2011; Rek 2014). Specifically: (i) senders, who initiate the communication game, expect benefits resulting from behavior of the receiver, which ultimately outweighs any costs associated with signaling; and (ii) receivers derive benefits from assessing and responding to signals, which must be reliable to be advantageous for receivers. However, dishonesty in animal communication persists and remains one of the most debated topics in the field (Wilson and Angilletta 2015; Mokkonen and Lindstedt 2016). While signaling systems are generally expected to collapse if signals are not, on average, honest (Harper and Maynard 2003), both honest and dishonest strategies can coexist (Szalai and Számadó 2009; Mokkonen and Lindstedt 2016). This coexistence has drawn significant attention to signal constraints and mechanisms of prevention of dishonest signaling, particularly in recent decades (Johnstone and Grafen 1993; Whiting et al. 2009; Laidre and Johnstone 2013; Mokkonen and Lindstedt 2016; Harris et al. 2020).

A common scenario of dishonest signaling occurs when less competitive individuals pretend to be more competitive (Szalai and Számadó 2009), leading to the emergence of dishonest signaling, where behavior of a signaler is consistently misinterpreted to its advantage (Johnstone and Grafen 1993). In some instances, individuals may evolve signals that mimic traits associated with strength or size (e.g., appearing larger, size being a common proxy for dominance status) to deter stronger opponents and/or gain access to mating opportunities (Smith and Harper 1995; Harper and Maynard 2003).

The use of chemical and visual cues are among the most common modes of communication in mammals, conveying individual information such as identity, sex, age, reproductive and dominance status and quality (e.g., weight and body size) (Goodenough et al. 2009; Laidre and Johnstone 2013; Sharpe 2015). Body size, which influences various aspects of animal behavior, is thought to play an important role in these signals (Andersson 1994). For instance, the assessment of competitors or dominant individuals may explain why adult males are more likely to elevate their scent marks than juveniles and females (Alberts 1992). Evidence suggests that conspecifics can derive accurate information about size of a signaler from the height of its marks (Mcguire et al. 2018). As a result, scent and visual marks that convey information about size of an individual are generally expected to be constrained and therefore often honest, meaning they accurately reflect attributes of the signaler such as its size, since marking behavior is constrained by anatomy (Goodenough et al. 2009; Gosling and Roberts 2001).

For example: (i) adult male giant pandas (Ailuropoda melanoleuca) are more likely to elevate scent marks than subadults or adult females, suggesting that elevated marks primarily benefit adult males (White et al. 2002); and (ii) the handstand marking posture, adopted by some mammal species, e.g., dwarf mongooses (Helogale parvula) and African civets (Civettictis civetta), enables individuals to place scent marks a full body length above the ground, thereby directly communicating body size (Ewer and Wemmer 1974; White et al. 2002; Sharpe 2015). The information provided by visual cues would be combined with chemical cues, ultimately providing a more complete picture of the marker. Although signalers performing potential exaggeration would likely be exposed during close-range encounters through direct assessment of body size, exaggerated visual and chemical cues may nonetheless influence interactions at a pre-encounter stage by discouraging approach by potentially dominant individuals.

Direct observations have been a critical first step in describing the diverse aspects of animal communication. However, most of our current understanding of how dishonest signalers persist within populations of honest signalers comes mostly from theoretical models of communication (Hamblin and Hurd 2009; Botero et al. 2010). Limited evidence suggests that scent marks used by males may serve as potential exaggerations of signaler attributes. For example, small male dwarf mongooses and domestic dogs (Canis lupus familiaris) have been observed to bluff their size by scent-marking higher than expected (Sharpe 2015; Mcguire et al. 2018). Although animal signaling is generally predicted to be reliable, it does not need to be completely honest for recipients to still pay attention to the signals (Laidre and Johnstone 2013). Consequently, as long as dishonest signaling occurs at a sufficiently low frequency to preserve overall signal reliability, or remains difficult for receivers to detect, signaling systems can remain evolutionarily stable (Grafen 1990; Laidre and Johnstone 2013; Wilson and Angilletta 2015). Under these conditions, sender strategies that exaggerate quality can coexist with honest signaling within the same population (Botero et al. 2010).

Most animals use multiple signals, often combining chemical and visual modalities (Johnstone 1995; Harper and Maynard 2003). Among mammals, brown bears (Ursus arctos) communicate through both visual and chemical signals, which are known to serve multiple—non-mutually exclusive social functions—including mate attraction, long-term communication hubs, density-dependent signaling, individual identification, and potentially anti-parasitic functions (Clapham et al. 2012; Lamb et al. 2017; Sergiel et al. 2017; González-Bernardo et al. 2021; Revilla et al. 2021; Blaise et al. 2023; Penteriani et al. 2021, 2023a). The most common channel of social communication in brown bears is scent marking, primarily achieved through bipedal dorsal rubbing. This behavior involves the back, shoulders, flanks, neck, and/or head, which deposit secretions from sebaceous and possibly apocrine glands in the skin (Tomiyasu et al. 2018). Other forms of scent marking include urination, anogenital gland secretions, and pedal marking (Clapham et al. 2013, 2014; Lamb et al. 2017; Sergiel et al. 2017; González-Bernardo et al. 2021; Morehouse et al. 2021; Revilla et al. 2021; Tattoni et al. 2021). These chemical signals encode information such as age, sex, and individual identity, as detected in the cutaneous glandular secretions of brown bears (Clapham et al. 2023).

Recent studies have shown that Brown Bear communication is more complex than previously thought, incorporating visual alongside chemical signals (Penteriani et al. 2021, 2023a). For instance, physical marks left on focal tree trunks, such as trunk debarking, are integrated into typical chemical Brown Bear communication sequences. These visual signals may thus complement chemical marking by providing additional information about specific classes of bears during certain times of the year. Notably, visual marks are made exclusively by adult males during the mating season (Penteriani et al. 2023a). This type of marking has been interpreted as conveying information about size of the male to conspecifics including females, subordinates, and subadult males sharing the same area (Penteriani et al. 2021, 2023a). Visual marks are typically placed at the maximum height a Brown Bear can reach when standing (Fig. 1a, b).

Fig. 1.

Male brown bears (Ursus arctos) create visual marks at the highest height they can reach when standing upright (Fig. 1a, b), likely to convey information about their size to females, subordinate males, and/or subadult males. Fig. 1c shows a visual mark nearly 3 m high, an elevation unattainable for any Cantabrian Brown Bear standing on the ground. The broken branch beneath the mark (Fig. 1d) indicates that a bear climbed the tree to leave the mark higher than would otherwise be possible. Photo credits: (a) A. Hartasánchez, (b) V. Penteriani, (c) E. González-Bernardo, and (d) V. Penteriani.

Previous descriptive and experimental studies on Brown Bear intraspecific communication (González-Bernardo et al. 2021; Penteriani et al. 2021, 2023a) in the Cantabrian Mountains (NW Spain) suggest that visual marks may be exaggerated to inflate body size of a signaler. Figure 1c shows a visual mark left by a bear at a height of nearly 3 m, an elevation impossible for any Cantabrian Brown Bear to reach, even when standing. The broken branch located below the mark (Fig. 1d) might suggest that the bear climbed the tree to mark at a height greater than what could be achieved from standing on the ground, which raises the question: was this individual a male attempting to exaggerate his size to attract females in heat or to confound potential rivals?

Here, we aimed to: (i) determine whether brown bears exhibit exaggerated signaling when marking, that is, mark higher than their natural height on a rubbing tree—natural height refers here to the maximum height typically achieved by a bear during bipedal marking from the ground, without climbing or using any external support, and under normal conditions, this height is anatomically constrained by size and morphology; and (ii) estimate its frequency relative to honest signaling. We hypothesize that exaggerating body size by placing scent and visual marks higher than the typical range could be particularly advantageous for less competitive males such as subadult or subordinate individuals, as it may reduce the likelihood of direct conflicts. While such exaggerated signaling is unlikely to remain effective during direct encounters, it may nonetheless discourage approach by dominant individuals during long-distance assessment, thereby lowering the probability of close-range interactions. In contrast, large, dominant individuals likely have less incentive to engage in exaggerated signaling and are more easily recognized by females as suitable mates, and their greater competitive abilities reduce their motivation to avoid direct conflicts compared to smaller males.

Methods

Study area

We conducted our study in the Cantabrian Mountains, spanning the provinces of Asturias and León in northwestern Spain. The landscape is predominantly composed of forests with deciduous species such as oaks (Quercus petraea, Q. pyrenaica, and Q. rotundifolia), European Beech (Fagus sylvatica), and Sweet Chestnut (Castanea sativa) trees. The region also features shrubland, pastures, and a mosaic of agricultural crops, infrastructure, and human settlements (Penteriani et al. 2023a).

Data collection and experimental protocol

To investigate exaggerated signaling, we constructed stable platforms using stone piles and wooden structures (Fig. 2) at 13 already known, active rubbing trees and 1 wooden pole previously used by bears for marking (both chemical and visual) in recent years (González-Bernardo et al. 2021; Penteriani et al. 2021, 2023a). The aim of these platforms was to facilitate opportunities for exaggerated marking in individuals already predisposed to this behavior by enabling them to climb off the ground and place marks at heights exceeding those that they would normally be able to reach based on their body size. To avoid potential bias related to differences in platform height, for example, platforms allowing greater elevation being used more frequently, all platforms were constructed to approximately the same height (∼80 cm). The platforms were active from 15 March to 15 July, coinciding with the peak period of Brown Bear marking behavior in the Cantabrian Mountains (González-Bernardo et al. 2021; Penteriani et al. 2021, 2023a). To minimize the risk that bears might use these platforms simply because they were positioned where bears typically stood, the platforms were always placed on the left or right side of the location where bears positioned their feet when standing to leave marks. The exact position of a bear when marking was determined based on footprints left on the ground and through 4,898 camera-trap days at these same rubbing trees (Penteriani et al. 2021, 2023a). Camera-traps (Browning Dark Ops HDProX https://browningtrailcameras.com/collections/dark-ops-series and EREAGLE E1 and EREAGLE E3 Trail Camera http://www.ereagle.com/Index.asp) were deployed at each platformed site for the entire duration of the study (n = 1,845 camera-trap days), approximately 3–5 m from the focal marking site. These camera-traps were programmed to record 1-min videos whenever triggered by presence of a bear during both day and night, with a one-second delay between recordings. Each video included date and time information. All sites were visited monthly throughout the study period to service the camera traps (i.e., downloading memory cards and checking batteries) and to ensure that the platforms remained intact. No bait was used to attract bears: the study relied solely on the spontaneous marking activity of local bears. Observations were conducted at the wooden pole for 4 consecutive years (2021 to 2024), at 4 trees for 2 consecutive years (2023 to 2024), and at 10 trees during 1 year (2024).

Fig. 2.

Examples of 4 platforms constructed at active rubbing trees in the Cantabrian Mountains (northwestern Spain). Photo credits: V. Penteriani and A. Hartasánchez.

The sex of adult individuals was determined using external reproductive organs, swollen mammae, the presence of cubs, or any distinctive individual traits when a previously identified bear (A.H., D.C., J.D., and V.P., personal observations) visited the platformed site. Individuals were categorized into 7 classes (Penteriani et al. 2023a): adult male, adult female, unknown adult, female with cubs, subadult male, subadult female, and unknown subadult. Specific characteristics such as fur marks, coloration, body morphology, and previously collected camera-trapping data facilitated classification of the different individuals into their sex and age groups (Zarzo-Arias et al. 2018; Penteriani et al. 2021, 2023a, 2023b). A bear was identified as a subadult based on morphological traits (e.g., ears that are disproportionately large and close together compared to the head, elongated head, neck, and shoulders, a thin neck, and long legs relative to body size) and its size in comparison with other bears frequenting the same rubbing tree (Zarzo-Arias et al. 2018; Penteriani et al. 2021, 2023a, 2023b). The orientation of bears in front of the camera during rubbing, combined with repeated observations from multiple angles, allowed reliable determination of both sex (e.g., visible male genitalia) and age class (subadult vs adult) for the majority of individuals. To evaluate whether the probability of performing exaggerated signaling was associated with the number of conspecifics, we initially fitted a binary logistic regression using R 4.4.2. (R Core Team 2024). In this model, we considered marking behavior as a Bernoulli distributed response variable (0 = a specific site was always marked in a specific year at their normal height; 1 = a specific site in a specific year was at least once marked by an individual using the artificial platform or climbed to mark sites higher than their natural height), with the number of males and females recorded at the specific sites as continuous predictor variables. However, due to the small and unbalanced sample (7 exaggerated signaling vs 17 non-exaggerated signaling events), model assumptions were likely violated. Since the number of conspecifics could not be categorized, we opted for a non-parametric test based on permutation procedures using the “coin” package (Hothorn et al. 2008), which allowed us to test for association without relying on distributional assumptions or categorization of continuous predictors. Our research adhered to ASM guidelines (Sikes et al. 2016) and was approved by the local authorities (AUTO/2021/172). No adverse effects of the presence of camera traps in the surrounding of marking sites were observed. Bears showed a variety of social and marking behaviors in front of the cameras.

Results

Over 117.552 h of camera-trap videorecording from 2021 to 2024, we documented 164 different brown bears visiting 14 marking sites (mean = 6.8 bears per marking site per year). The reported hours correspond to the total recording time from all cameras, not only to clips associated with bear visits. The number of visiting bears refers to all bears recorded by camera traps, not only those that specifically interacted with the rubbing trees. Adult males were the most common class, representing 62.8% of the observed individuals (this value increased up to 78.7% when including individuals classified as possible males). Subadults of unknown sex accounted for 18.9%, while adult females represented 11.6% of observations (this value rises to 25.6% when including possible females).

We recorded 7 different bears performing exaggerated signaling, defined as individuals that marked higher than their natural height by using a platform or climbing at the marking site (Figs 3, 4; Supplementary Data SD1; Supplementary Data SD2). All signalers performing exaggerated signaling were males: 4 were adults (57.1%) and 3 were subadults (42.9%). Exaggerated signaling occurred at 2 (14.3%) sites: (i) the wooden pole (6 individual bears, 85.7%); and (ii) a tree in a pine forest (1 bear, 14.3%). At the wooden pole, bears engaged in both chemical and visual marking in the following years: 2021 (1 adult and 1 subadult); 2022 (1 subadult); 2023 (1 adult); and 2024 (1 adult), while exaggerated signaling at the pine tree was recorded in 2021. However, in June of that year, the camera-trap was stolen when 1 bear left visual marks higher than the typical Brown Bear height (Fig. 1c). Although uncertain, we hypothesize the bear was an adult male because only adult males were observed leaving visual marks by debarking tree trunks (Penteriani et al. 2021, 2023a). All but 1 of the observed exaggerated signaling events occurred during the day and were distributed across all months of the study: 3 events occurred in April; 2 in June; and 1 each in May and July. Further, we observed that the probability of performing exaggerated signaling did not significantly changed with the number of bears visiting a marking site (χ² = 0.09, df = 1, P = .759), neither when the visitors included more males (χ² = 1.31, df = 1, P = .252), nor when the visitors included more females (χ² = 3.99, df = 1, P = .05).

Fig. 3.

The 3 images on the top of the figure (a–c) depict an adult, large male leaving both chemical (a–b) and visual (c) marks on a wooden pole. This individual did not use the platform on the left side of the pole. Three images on the bottom (d–f), show an adult, but smaller individual (d), using the platform to reach and leave both chemical (e) and visual (f) marks at the same height (or even higher) than the larger male. Supplementary Data SD1, SD2, and SD3 include all screenshots used in this figure. Photo credits: A. Hartasánchez.

Fig. 4.

Four-panel image showing 2 Brown Bear subadults (upper and lower left) and 2 adult males (upper and lower right) leaving chemical marks by rubbing on the pole. The red line indicates the difference in height achieved by bears that used the platform (left side of the pole). In the bottom panels, subadults reached the same height as adults by climbing directly on the pole, without using the platform. This climbing behavior is comparable to that observed for the visual marks shown in Fig. 1c and 1d. Supplementary Data SD1, SD2, and SD3 include all screenshots used in this figure. Photo credits: A. Hartasánchez.

However, even considering the total number of bears visiting the rubbing trees, the overall percentage of signalers performing exaggerated signaling was low at 4.3%. The frequency of elevated marking was extremely low compared to the number of normal marking events recorded at each monitored site [n = 149 total marking events, mean ± standard deviation (SD) = 6.8 ± 5.3, range = 0 to 17 marking events per tree]. Because males are the primary signalers and are more likely to compete during the mating period, exaggerated signaling was more frequent when analyses were restricted to males present at marking sites in years when exaggerated signaling was observed. Under a conservative estimate that included only individuals confidently identified as males, the percentage of exaggerated signaling was 19.2% (range = 9.1% to 25%). When a less conservative estimate was applied, including both confidently identified males and possible males, this percentage was 15.3% (range = 11.1% to 25%).

Discussion

Our study documents the strategic elevation of chemical and visual marks in brown bears, a behavior that can be interpreted under several non-mutually exclusive frameworks within mammalian communication systems. One possible explanation is signal exaggeration, but alternative interpretations such as optimized signal placement or context-dependent multifunctionality are also compatible with our data. Among these frameworks, the observed pattern is also compatible with forms of signal exaggeration described in other taxa, where individuals may alter signal presentation in ways that influence receiver perception. If elevated marking reflects a form of signal exaggeration, its low frequency in our dataset would be consistent with theoretical frameworks on the maintenance of honesty in animal communication (Grafen 1990; Harper and Maynard 2003; Szalai and Számadó 2009; Laidre and Johnstone 2013; Wilson and Angilletta 2015; Mokkonen and Lindstedt 2016), which predict that high prevalence of dishonest or exaggerated signals would undermine the overall reliability of the communication system (Mokkonen and Lindstedt 2016). However, while such behaviors are compatible with theoretical models of dishonest signaling, the absence of direct evidence on receiver responses requires a cautious interpretation. Exaggerated marking was rare and spatially restricted, occurring at only 2 sites during the study. Although such clustering could suggest an influence of local structural features, elevated marking also occurred at a natural tree without any platform, supporting the conclusion that this behavior is not purely an experimental artifact and can occur under natural conditions. Such spatial clustering is expected in systems where rare or context-dependent signaling strategies occur, particularly in species with uneven social or demographic structures. Repeated use of particular locations by the same individuals may amplify otherwise infrequent behaviors, reducing concerns about site effects or pseudo-replication. Elevated marking may therefore arise from multiple, non-mutually exclusive mechanisms including strategic exaggeration of signal height, optimized placement to enhance detectability or persistence of chemical cues, and context-dependent multifunctional signaling. While the experimental platforms may have facilitated access to elevated positions, their presence does not appear to be a necessary condition for the expression of this behavior. Given the localized occurrence of exaggerated signalers, we propose that understanding the dynamics of exaggerated signaling requires further investigation into the social environment surrounding marking areas. For instance, it would be valuable to explore whether the prevalence of exaggerated signaling correlates with the density of highly competitive or less competitive individuals within a given marking area.

As hypothesized, subadults and likely subordinate individuals visually smaller than adult males visiting the same marking sites, as assessed from repeated video observations (Supplementary Data SD1; SD2; authors personal observations), appeared to be disproportionately represented among individuals performing elevated marking. These assessments were based on repeated video observations rather than direct morphometric measurements and should therefore be interpreted as qualitative rather than quantitative. The motivation for dominant, larger males to engage in deceptive signaling is expected to be lower, as their status and competitive abilities already afford them reproductive and social advantages. By manipulating marking sites, these signalers could potentially mask or exaggerate their true competitive ability, thereby influencing receiver perception (Hurd and Ydenberg 1996). If receivers interpret mark height as an index of body size, such behavior might alter their assessment decisions, for example by discouraging dominant males from engaging in potentially costly encounters. Under this interpretation, elevated marking would be consistent with the broader concept of “deception,” an evolutionary strategy in which signalers gain a fitness advantage by exploiting aspects of receiver perception (Earley 2010; Mokkonen and Lindstedt 2016). Signaling operates as a game of diminishing returns: for individuals with established high quality, further elaboration of signals yields minimal additional benefit. Exaggerated or dishonest signaling, therefore, holds evolutionary value only for the lower-competitive ability sector of the population (Earley 2010).

This scenario is particularly relevant in brown bears, where females select their mates based on condition-sensitive traits such as body size (Bellemain et al. 2006) that may serve as indicators of genetic quality. In bears, body size is age-dependent, with a strong correlation between male age and size (Bellemain et al. 2006; Swenson et al. 2021, 2023). Consequently, females that choose the largest males also tend to select the oldest (Bellemain et al. 2006). Additionally, considering the asymmetries in interactions between bears (Swenson et al. 2021, 2023) such as differences in resource-holding potential, reproductive investment, and levels of promiscuity, a greater fitness benefit for deceptive traits is expected in the less-competitive individual (Mokkonen and Lindstedt 2016). When interests diverge, variance in reproductive success increases and, consequently, the benefits to deceiving conspecifics increase (Mokkonen and Lindstedt 2016).

Instances of subordinate individuals attempting to deceive dominants have been observed across taxa, including stomatopod crustaceans (e.g., Gonodactylus bredini), fiddler crabs (Uca annulipes), birds, for example, American Goldfinch (Spinus tristis) and mammals (White et al. 2002; Sharpe 2015). For example, in scent-marking behavior, lighter dogs mark higher relative to their body size compared to heavier dogs (Mcguire et al. 2018). Similarly, in dwarf mongooses, males that were small for their age deposited their scent marks higher than expected for their size, breaking the typical correlation between mark height and body size (Sharpe 2015). In both dwarf mongooses and brown bears, the primary motivation for smaller males to send exaggerated signals seems to be to convince potential rivals of their competitive strength, thereby avoiding direct confrontations that could escalate into harmful fights. If elevated marking functions as a form of exaggeration, it could be more advantageous for smaller individuals, as larger and more competitive males have less incentive to exaggerate their marks. Subadult and, more generally, small bears may also be more physically capable of accessing elevated positions on natural substrates and experimental platforms. This biomechanical capacity likely interacts with strategic exaggeration, potentially facilitating the expression of elevated marking rather than serving as an alternative or competing explanation.

Conversely, females in these species generally lack the motivation to bluff about their size. In brown bears, females do not compete for mating opportunities and intra-sexual competition among them is rare (Swenson et al. 2021, 2023), and in female dwarf mongooses intra-sexual competition is restricted to group mates so females can assess size of a rival directly.

An additional interest in the deceptive behavior of bears lies in their ability to manipulate the so-called ‘index signals’, that is, signals traditionally considered “unfakeable” because they are intrinsically tied to anatomy through physical constraints (Searcy and Nowicki 2005; Laidre and Johnstone 2013; Weaver et al. 2017). Our results are consistent with the possibility that classic index signals (which are considered intrinsically honest because they are constrained by anatomy) could be manipulated, and suggest that the presence of occasional dishonest signaling may not necessarily undermine the reliability of the communication system. These observations highlight a potentially important aspect of signal dynamics in mammalian communication. For honest signaling to emerge, certain cues must already exist in the population, such as morphological traits that evolved for non-communicative purposes but that yet reveal relevant individual features (Szalai and Számadó 2009). One of the most recognizable cues is body size, which often correlates with competitive ability and quality. As a result, it is a trait worth heeding, and it may subsequently evolve into an honest signal (Szalai and Számadó 2009). However, despite the low frequency of individuals performing exaggerated signaling, which helps maintain honesty in Brown Bear chemical and visual communication, the ability of some individuals to mislead conspecifics about their size undermines, at least partially, the investment that stabilizes signal reliability. This investment, such as the developmental costs associated with achieving larger body size, is typically paid throughout growth of an individual and development (Laidre and Johnstone 2013).

On the other hand, it is worth noting that if individuals performing exaggerated signaling do not incur any costs, such as might occur if the combination of chemical and visual marks reduces the likelihood of direct confrontations between males of different sizes, there is a possibility that such signaling could persist within the population (Dawkins and Guilford 1991). In this scenario, these individuals might avoid some costly encounters with larger males, without incurring penalties for performing exaggerated signaling. Because the primary costs typically arise from probing by receivers, and probing itself entails costs, receivers may be limited in their ability to respond. Consequently, occasional exaggerated signaling could persist without necessarily having major fitness consequences for the signalers (Smith and Price 1973).

The finding that male bears: (i) chemically mark more frequently than females (Clapham et al. 2012, 2014; Lamb et al. 2017; Tattoni et al. 2021; Penteriani et al. 2023a); (ii) are the only sex to leave visual marks (Penteriani et al. 2021, 2023a); (iii) tend to mark rubbing trees at the maximum height they can reach (Penteriani et al. 2021, 2023a); and (iv) exhibit a positive association between the mark height of bears performing exaggerated signaling and their competitive disparity to rivals is consistent with the possibility that bears may extract information about size (and presumably competitive ability and mating quality) from the height of scent deposits and visual marks. Since intra-sexual competition and mating are major drivers of scent marking in mammals (Gosling and McKay 1990; Gosling and Roberts 2001; Muller and Manser 2007; Jordan et al. 2011; Stockley et al. 2013; Sharpe 2015), it would be surprising if elevated-marking species do not utilize mark height for these purposes. This interpretation is supported by our findings, which show some bears using artificial platforms to investigate the height of chemical marks left on rubbing sites (Supplementary Data SD3). Not only do visual marks give an immediate representation of individual size, but the height of a scent mark may also convey information about size. Assessment activities around scent marks may reflect efforts to memorize the odoriferous attributes of large, high-status individuals, as suggested for other species such as mice (Hurst 1989) and giant pandas (White et al. 2002). For instance, pandas remained farther away from areas where male urine was placed to mimic a handstand posture than male urine placed at ground level, indicating avoidance of areas marked by highly competitive males (White et al. 2002).

It seems unlikely that some bears adopt this marking strategy to enhance scent dispersal and signal range (Alberts 1992) for several reasons. First, marking sites are typically located in sheltered environments such as dense forests, where air movement—essential for extensive odor diffusion—is limited. Second, chemical marking by individuals performing exaggerated signaling is frequently accompanied by visual marking, whose effectiveness in terms of conspicuousness would not significantly benefit from being a few dozen centimeters higher than actual height of the bear in a dense environment with generally low visibility. Finally, if depositing marks at greater heights truly provided advantages in scent dispersal or visibility, it would be expected that most individuals across different bear classes and sexes would adopt this strategy.

The discrepancy between the truth about the signaler and the receiver assessment add complexity of an already intricate system like animal communication. As Szalai and Számadó (2009: 957) aptly stated at the beginning of the century “Signaling is not black or white where the majority of the population have to be honest signalers. Various strategies can coexist and this coexistence cannot be excluded in nature. When researchers seek out this variety, a more diverse picture of signaling will emerge.” Animals are constantly engaged in an evolutionary struggle to accurately interpret conspecific signals while avoiding manipulation or deception. The “handicap principle” suggests that 1 partial solution is for receivers to rely on costly signals, which are less likely to be faked (Johnstone and Grafen 1993). However, signals with no apparent or low costs, such as those used by brown bears for communication, may be more vulnerable to exaggerated or potentially deceptive signaling, and under some conditions such signals could potentially persist within a stable signaling system (Johnstone and Grafen 1993). Even so, constraints faced by receivers appear limited, and the potential impact of these signals on receiver fitness may be minor. On the contrary, it may help reduce direct confrontations. If this is indeed the case, combined with the observed low prevalence of exaggerated signaling, it might explain why natural selection has not imposed restrictions that would eliminate those signaling rules that led to misinterpretation of a signal.

To conclude, while our experiment indicates that bears can manipulate the height of chemical and visual marks, these findings are best interpreted as hypothesis-generating rather than as strong evidence for dishonest signaling. The extreme rarity and spatial clustering of elevated marking events in our dataset suggest that, whatever its functional significance, this behavior likely represents a context-dependent and infrequent component of Brown Bear communication rather than a dominant signaling strategy. Our results highlight an intriguing behavioral capacity in bears that warrants further experimental and observational work, particularly studies that explicitly quantify receiver responses.

Author contributions

Vincenzo Penteriani (Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing—original draft, Writing—review & editing), Carla Osterburg (Formal analysis, Investigation, Writing—review & editing), Rafael Benjumea (Investigation, Writing—review & editing), Enrique González-Bernardo (Investigation, Writing—review & editing), Alfonso Hartasánchez (Investigation, Methodology, Resources, Writing—review & editing), Héctor Ruiz-Villar (Investigation, Writing—review & editing), Ana Morales-González (Investigation, Writing—review & editing), David Cañedo (Investigation, Writing—review & editing), Juan Díaz García (Investigation, Writing—review & editing), and María del Mar Delgado (Formal analysis, Funding acquisition, Investigation, Writing—review & editing)

Supplementary data

Supplementary data are available at Journal of Mammalogy online.

Supplementary Data SD1 . This video documents 6 out of the 7 exaggerated signaling events in which subadult and adult brown bears marked higher than their actual body size would have allowed. This was achieved either by using the platform or by directly climbing on the marking site. https://youtu.be/MAdjHTtn4Ns

Supplementary Data SD2 . This video shows examples of brown bears leaving marks that correspond honestly to their real body size. These bears actively avoid using the platforms, demonstrating natural marking behaviors without attempting to exaggerate their height. https://youtu.be/XDAr21TCVZE

Supplementary Data SD3 . This video illustrates an unanticipated behavior in which bears used the platforms to sniff chemical marks left by other bears. This activity suggests that chemical signals may also provide information on the height of the individual that rubbed at the marking site. https://youtu.be/NbCJki0Q6to

Funding

V.P., E.G.-B., and M.M.D. were financially supported by the I + D + i Project PID2020-114181GB-I00 funded by MCIN/AEI/10.13039/501100011033 and by the European Union. V.P. and M.M.D. were financially supported by Grants for Research Groups of Public I + D+i Organizations in the Principality of Asturias (IDE/2024/000779; SEKUENS and EU funds).

Conflict of interest

None declared.

Data availability

Data are included as a Supplemental Data file.