Urine marking in male domestic dogs: honest or dishonest?

Transcription

1 Urine marking in male domestic dogs: honest or dishonest? B. McGuire, B. Olsen, K. E. Bemis & D. Orantes Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY, USA Journal of Zoology. Print ISSN Keywords domestic dog; scent mark; over mark; dishonest signal; competitive ability; male male competition; body size; shelter. Correspondence Betty McGuire, Department of Ecology and Evolutionary Biology, Cornell University, Ithaca, NY 14853, USA. Tel: +1 (607) ; Fax: +1 (607) Editor: Nigel Bennett Received 29 May 2017; revised 12 June 2018; accepted 2 July 2018 doi: /jzo Abstract Scent marking is a common mode of communication in mammals. Such marking is thought to communicate information about the signaler s size and corresponding competitive ability and accurately reflect the signaler s attributes (i.e., an honest signal). However, new data suggest that scent marking can be dishonest in certain circumstances. Via two studies, we tested the hypothesis that urine marking is a dishonest signal in adult male domestic dogs, which raise a hindlimb when marking vertical objects. In Study 1, we tested whether raised-leg angle (i.e., during a urination, the angle between a dog s raised leg and the axis normal to the ground) is a proxy for urine mark height (n = 15 dogs) and, in Study 2, we tested whether small dogs exhibit larger raised-leg angles than large dogs (n = 45 dogs). We videotaped urinations of adult male dogs and, afterwards, measured height of urine marks (Study 1) and degree of raised-leg angles (Studies 1 and 2). In Study 1, we found significant positive relationships between both raised-leg angle and height of urine mark and body size (using either body mass or height at withers) and height of urine mark; raised-leg angle was a stronger predictor than either measure of body size. In Study 2, we found a significant negative relationship between body size (using either body mass or height at withers) and average raised-leg angle. Our findings support raisedleg angle as a proxy for urine mark height and provide additional evidence that scent marking can be dishonest. Assuming body size is a proxy for competitive ability, small adult male dogs may place urine marks higher, relative to their own body size, than larger adult male dogs to exaggerate their competitive ability. We did not control for over marking, which also may explain our findings. Introduction Scent marking, a common mode of communication in mammals, conveys several types of information, including individual identity, sex, age, reproductive status, social status, health, quality, kinship, and histocompatibility (Sharpe, 2015). Properties of marks, such as olfactory content (Alberts, 1992; Gosling & Roberts, 2001) and spatial arrangement (Gosling & Roberts, 2001), convey information. With respect to spatial arrangement, many mammals elevate their scent marks (Sharpe, Jooste & Cherry, 2012). Increased detection via olfaction and vision may explain why some mammals elevate their scent marks. The ground physically restricts diffusion, so both size of mark and likelihood of detection by olfaction are increased when scent marks are elevated (Alberts, 1992). Elevated marks are disentangled from other scents that saturate the substrate (Alberts, 1992) and conveniently located at nose-height of receivers (Gorman & Mills, 1984). Deposition of scent marks on conspicuous, elevated landmarks may create visual cues that increase detection (Eisenberg & Kleiman, 1972). Increased detectability, however, may not be the sole explanation for elevated scent marks. White, Swaisgood & Zhang (2002) state that increased detectability should benefit all sex and age classes. If this is true, then increased detectability cannot explain dimorphic marking postures in which members of one class typically deposit elevated scent marks and members of another class low-lying marks. For example, adult male pandas (Ailuropoda melanoleuca) are more likely than adult females and subadults to deposit elevated scent marks; this suggests that elevated marks are uniquely beneficial to adult males (White et al., 2002). Competitor assessment may explain why adult males, in comparison to juveniles and females, are more likely to elevate their scent marks. Receivers may extract information about a competitor s size from the vertical placement of their scent marks (Alberts, 1992). Alberts (1992) cites the handstand marking posture as evidence because it enables some mammals (see Sharpe et al., 2012 for species) to place scent marks a full body length above the ground, thereby directly communicating body size. Data from White et al. (2002) for pandas and Sharpe (2015) for dwarf mongooses (Helogale parvula) provide additional support: in both species, males and females spend more time investigating higher scent marks. According to these authors, it would be beneficial for male receivers to avoid particularly large conspecifics and female receivers to catalogue the scent of large prospective mates. This reasoning assumes that larger individuals have higher Journal of Zoology 306 (2018) ª 2018 The Zoological Society of London 163

2 Urine marking in male domestic dogs B. McGuire et al. competitive ability, which is supported for diverse species (Huntingford & Turner, 1987; Gosling & Roberts, 2001). Scent marks that convey information about size and corresponding competitive ability of the signaler may be honest (i.e., accurately portray the signaler s attributes, including size and competitive ability) or dishonest (i.e., inaccurately portray the signaler s attributes). Gosling & Roberts (2001) hypothesized that, in general, male scent marks are honest. They reasoned that females use scent marks to evaluate the quality of prospective mates and, because females are the higher investing sex, this would only be evolutionarily beneficial if male scent marks are honest signals. Additionally, it seems likely that scent marking is restricted by the signaler s anatomy and physiology, just as the frequency of acoustic communication is restricted by the caller s size (Fitch & Hauser, 2002), thereby honestly reflecting the signaler s attributes. However, more recent evidence suggests that scent marks can be dishonest signals: male dwarf mongooses that are small for their age communicate their size and competitive ability dishonestly by scent marking higher than expected (Sharpe et al., 2012). In domestic dogs (Canis lupus familiaris), urination is the most common form of scent marking and urinary behavior varies greatly across sex, age, and size classes (Cafazzo, Natoli & Valsecchi, 2012; McGuire, 2016; McGuire & Bemis, 2017). Adult males typically use the raised-leg posture, juvenile males use the lean-forward posture during which no hindlimb is raised, and most females use the squat posture (Sprague & Anisko, 1973). By raising a hindlimb during urination, adult male dogs are more likely than adult females and juveniles to deposit an elevated mark. Adult males urinate more frequently and direct more urinations onto vertically oriented targets than do adult females (McGuire, 2016). Small dogs urinate more frequently and direct more urinations than large dogs, which may indicate a preference by small dogs for communicating through scent marking rather than direct interactions that could be risky (McGuire & Bemis, 2017). We further explore contexts in which scent marks may be honest or dishonest and do so for the first time with respect to urine marking in domestic dogs. We evaluated raised-leg angle and body size as predictors of urine mark height to determine if raised-leg angle could serve as a proxy for height of urine mark (Study 1). Then, using raised-leg angle as a proxy for urine mark height and body size as a proxy for competitive ability, we compared height of urine mark and the signaler s competitive ability (Study 2). Assuming that urine mark height communicates body size and corresponding competitive ability to conspecifics, Study 2 tested the hypothesis that urine marking is a dishonest signal in male dogs. Given that small dogs urinate more frequently and direct more urinations than large dogs (McGuire & Bemis, 2017) and would seem to benefit more from exaggerating their size, we predicted that small male dogs would exhibit larger raised-leg angles than large male dogs. Materials and methods Dogs and housing We scored the raised-leg marking posture of male dogs at two animal shelters, Tompkins County SPCA (Ithaca, NY, USA) and Cortland Community SPCA (Cortland, NY, USA). Dogs came to the shelters as strays, transfers from other shelters, or were owner-surrendered; most were mixed-breeds. All dogs had undergone temperament testing by shelter staff, received veterinary care, and were in good physical health at the time of observation. Body mass and estimated age of each dog were obtained from veterinarian records. We measured height at withers for each dog. We analyzed adult males because juvenile males typically do not raise a hindlimb during urination (Sprague & Anisko, 1973; Gough & McGuire, 2015; McGuire, 2016) and senior dogs are more likely to experience orthopedic issues such as hip dysplasia (Lavrijsen et al., 2014), which could hinder the raised-leg posture. Dogs ranged in age from 10 months to 7 years (median = 3.0 years). We excluded from Study 2 two large 1-year-olds because they displayed juvenile urinary behavior by predominantly using the lean-forward posture and included one small (23 cm) 10-month-old because small dogs undergo puberty earlier than large dogs (Pineda, 2003) and he displayed adult urinary behavior by exclusively using the raised-leg posture. Dogs varied in body mass (range: kg, median = 26.3 kg) and height (range: cm, median = 54.0 cm). We included both intact and neutered adult males because both display the raised-leg posture (Beach, 1974). We observed 15 dogs in Study 1. For Study 2, we included relevant data from the 15 dogs in Study 1 plus data from 30 additional dogs (different response variables were analyzed in Studies 1 and 2). Housing arrangements for dogs are detailed in Gough & McGuire (2015); we provide an abbreviated description here. Tompkins SPCA held dogs in individual cubicles, which ranged in size from 5.2 m 2 to 7.3 m 2. Dogs were typically walked or taken to an outdoor enclosure every two or three hours. We observed dogs that had not been outside for at least 2 h. Cortland SPCA held dogs in individual cages that ranged in size from 2.3 m 2 to 4.5 m 2, were divided by chain-link fences, and accessed via chain-link doors. Dogs were walked by staff or volunteers once or twice per day and rotated through two outdoor pens. Walking procedures At Tompkins SPCA, the walking area included the shelter s yard and a nearby agricultural field (16.6 ha; N, W). Vertically oriented objects such as dense vegetation ( m in height), trees, and buildings lined the yard. Trees, pond reeds, benches, and a chain-link fence were within the yard. The agricultural field had walking paths lined with vertically oriented vegetation and trees. At Cortland SPCA, the walking area included a gravel parking lot and the shelter s yard (0.3 ha; N, W). Vegetation ( m in height), trees, buildings, and a fire hydrant lined the walking area. A planter (approximately 0.5 m in height), two metal posts, and a dumpster were within the walking area. Given size differences in walking areas, walk duration was 20 min at Tompkins SPCA and 10 min at Cortland SPCA. Dogs set the pace of walks, explored freely, and investigated prospective marking targets as they pleased. In Studies 1 and 164 Journal of Zoology 306 (2018) ª 2018 The Zoological Society of London

3 B. McGuire et al. Urine marking in male domestic dogs 2, Betty McGuire (BM) typically walked the dogs and Katherine Bemis (KB) or Destiny Orantes (DO) followed behind the dogs at approximately three meters and filmed continuously with an iphone 7 (model MN9G2LL/A, Apple Inc., Cupertino, CA, USA). In Study 2, Boomer Olsen (BO) filmed using a high-speed camera (Exilm FH20) mounted to a monopod (Quik Pod Ultra; 0.5 m in length). Only one dog displayed an interest in the camera and/or monopod. BO filmed this dog at a distance such that it no longer responded to the camera (approximately 20 m). Due to adoptions during our period of data collection, we walked some dogs once and some multiple times (Study 1: 1 walk, 6 dogs; 2 3 walks, 4 dogs; 4 5 walks, 4 dogs; 6 walks, 1 dog; Study 2: 1 walk, 19 dogs; 2 3 walks, 14 dogs; 4 5 walks, 5 dogs; >8 walks, 7 dogs). All procedures were carried out under protocol , which was approved by Cornell University s Institutional Animal Care and Use Committee. Video analyses We used video analysis software (ImageJ) to view footage and quantify raised-leg angle by drawing a virtual angle on paused video (Fig. 1). The first ray was drawn from the knee of the dog s raised-leg to the vertex at the base of the dog s tail. The second ray was drawn parallel to a vertical object in the background (thus, the second ray was normal to the ground). The vertical objects used for reference included buildings, light posts, and fences. If no vertical object existed in the background, then the urination was not analyzed. The ground itself was not used for reference because its orientation was not always obvious from the video recordings. To control for potentially restrictive effects of target size on raised-leg angle, only urinations on vertical targets that exceeded the dog s height (e.g., walls, posts, trees, vertically oriented vegetation) were analyzed. We archived a screenshot of each raised-leg posture and the superimposed angle drawn in ImageJ. Statistical analyses All statistical analyses were completed in JMP Pro (version ). Study 1 At least three factors influence the relationship between raised-leg angle and height of urine mark. First, size of dog affects absolute height of urine mark (i.e., no matter the raised-leg angle, a large dog would likely mark higher than a small dog). Second, height of urine mark depends on distance between dog and target (e.g., holding the raised-leg angle constant, dogs that are farther from the target will deposit urine at lower heights than dogs that are closer). We could not directly measure distance from planted hind-limb to target without disrupting marking behavior. We instead controlled for target shape, which partially affects how close dogs can stand (i.e., dogs can wrap their legs around poles and stand very near but, when marking walls, there must be space between the dog and the wall to accommodate the raised leg). We classified targets as cylinder-shaped (e.g., poles and tree trunks), wall-shaped (e.g., walls, fences, stacked pallets), and borders of tall grass (because grass borders are not solid, we separated this type of target from wall-shaped). Third, strength of urine stream affects height of urine mark (i.e., a weak stream will decrease in height before reaching the target). We could not practically and reliably measure this variable. BM, KB, and DO measured heights of urine marks and BO, who was blind to heights of urine marks, measured raised-leg angles. Height of urine mark (cm) was measured from the ground at the base of the object being marked to the highest point of the mark. We pooled dogs from Tompkins SPCA (n = 11) and Cortland SPCA (n = 4) for statistical analyses due to small sample size at Cortland SPCA; previous analyses revealed similar patterns of scent marking behaviors at both shelters (Gough & McGuire, 2015; McGuire, 2016). We ran two general linear mixed effects models with height of urine mark as the response variable, size of dog (using body mass in one model and height at withers in the other because these variables were highly correlated; R 2 = 0.91, F 1, 14 = , P < ), raised-leg angle, and target type as fixed factors, and dog as a random effect. We did not include neuter status in our models because 14 of the 15 males were neutered at the time of their walks; the remaining dog was walked twice while intact and twice after neutering. Supporting Information Table S1 includes body mass, height at withers, number of walks, and number of angles by target type for each of the 15 dogs observed. Figure 1 Screenshot of video analyses as described in the methods. The first ray was drawn along the dog s raised leg to the vertex at the base of the dog s tail. The second ray was drawn parallel to the post (thus, the second ray is normal to the ground). Study 2 Measuring urine mark height is challenging because dogs sometimes miss targets, especially poles and tree trunks of small diameter, and marks can be hard to locate on tall grass or targets wet from rain. Thus, we chose to use raised-leg angle as a proxy for urine mark height in Study 2. Using raised-leg angle measurements (range: angles per dog, median = 5 angles per dog) from video analyses, we calculated mean raised-leg angle (deg) for each dog, which we refer to as Journal of Zoology 306 (2018) ª 2018 The Zoological Society of London 165

4 Urine marking in male domestic dogs B. McGuire et al. average raised-leg angle. We then conducted linear regressions with average raised-leg angle (deg) as the response variable and either body mass (kg) or height at withers (cm) as predictor variables. Body mass and height at withers were highly correlated (R 2 = 0.84, F 1, 43 = , P < ) and therefore included in separate models. Residuals were checked for normality via Shapiro-Wilk test and homogeneity of variance via Levene s test using a median split method. Average raisedleg angle was cubed to meet both normality and homogeneity of variance assumptions. For these analyses, we pooled dogs from Tompkins SPCA (n = 19) and Cortland SPCA (n = 26) because shelter identity was not a significant predictor when included in the linear regression models. We also excluded neuter status because it was not a significant predictor when included in the models. Note that we tested the effect of neuter status using 38 neutered dogs, two intact dogs, and intact data from the five males that were neutered over the course of our observations; thus, for the analysis, we had 38 neutered males and 7 intact males. Age did not predict average raised-leg angle, so we excluded age from the models. Results Study 1 In the first model, raised-leg angle was a significant predictor of height of urine mark (F = , d.f. = 1, 61.9, P < ) as was body mass (F = , d.f. = 1, 8.8, P < 0.007). Type of target did not predict height of urine mark (F = 1.076, d.f. = 2, 87.1, P = 0.35). In the second model, raised-leg angle was a significant predictor of height of urine mark (F = , d.f. = 1, 24.8, P < ) as was height at withers (F = , d.f. = 1, 5.5, P < 0.002). Type of target did not predict height of urine mark (F = 1.265, d.f. = 2, 91.1, P = 0.29). In these analyses, we had limited ability to control for distance between dog and target and inability to control for strength of urine stream. These two factors are best controlled by analyzing the relationship between raised-leg angle and height of urine mark during a single urination. Figure 2 compares two raised-leg angles from a video of a single urination by Patches (Supporting Information Video S1). Patches first held his raised leg at 115 degrees (Fig. 2a). We calculated the corresponding height of urine mark to be 15.3 cm. As the video plays, Patches further elevates his raised leg without shifting his planted hindlimb or moving closer to the target. Simultaneously, the urine stream and urine mark on the tree trunk move upward. Patches then holds his raised leg at 120 degrees (Fig. 2b). We measured the height of the corresponding urine mark, from the base of the tree trunk to the highest point of the urine mark, to be 17.8 cm. Thus, Figure 2 directly demonstrates the positive relationship between raised-leg angle and height of urine mark while best controlling for both distance between dog and target and strength of urine stream. Study 2 A male dog s body mass significantly predicted average raisedleg angle (cube-transformed; Table 1; Fig. 3a). Similarly, a male dog s height significantly predicted average raised-leg angle (cube-transformed; Table 1; Fig. 3b). For ease of (a) (b) cm 17.8 cm Figure 2 Screenshots from a video of Patches, who was observed in Study 1. Horizontal lines compare height of urine mark and height of raised-leg. (a) Patches first held his raised leg at 115 degrees, resulting in a urine mark at 15.3 cm. We approximated height of urine mark by calculation. (b) At a later time during the same urination, Patches shifted his raised leg to 120 degrees, resulting in a urine mark at 17.8 cm. We measured height of urine mark from the base of the tree to the highest point of this second mark. [Colour figure can be viewed at zslpublications.onlinelibrary.wiley.com] 166 Journal of Zoology 306 (2018) ª 2018 The Zoological Society of London

5 B. McGuire et al. Urine marking in male domestic dogs Table 1 Relationship between body mass (kg) and height at withers (cm) of adult male domestic dogs and average angle of the raised-leg urinary posture. Shown are results from regression analyses in which body mass and height were predictor variables and average raised-leg angle (either cube-transformed or nontransformed) was the response variable. Body mass and height were included in separate models because they were highly correlated. Degrees of freedom for all analyses = 43; N/A = not applicable; data analyzed in Study 2 Average angle 3 (deg 3 ) Average angle 3 (deg 3 ) Average angle (deg) Average angle (deg) Intercept (b; P) ; < ; < ; < ; < Body mass (kg) (b; P) ; N/A 0.559; N/A Height (cm) (b; P) N/A ; N/A 0.340; R F interpretation, non-transformed average raised-leg angle is plotted against body mass (Fig. 3c) and height (Fig. 3d). Although regression tests using nontransformed average raised-leg angle did not meet the normality assumption, these regression outputs and conclusions were very similar to those obtained using transformed data (Table 1). In all analyses, the relationship between body size (using either body mass or height at withers) and average raised-leg angle was negative (Table 1; Fig. 3). Supporting Information Table S2 contains body mass, height, number of walks, number of raised-leg angle measurements, and average raised-leg angle (SD) for each dog. Discussion We found that raised-leg angle was the strongest predictor of height of urine mark (Study 1). Consistent with our prediction that small dogs would exhibit larger raised-leg angles than large dogs, we found a significant negative relationship between an adult male dog s body size (using either body mass or height at withers) and average raised-leg angle (Study 2). As body mass negatively predicted average raised-leg angle, we expect that light dogs place scent marks higher, relative to their own body size, than heavy dogs. Our results are consistent with Sharpe et al. (2012), who found that particularly light male dwarf mongooses marked higher than expected. Our findings and those of Sharpe et al. (2012) suggest that vertical placement of scent marks could be used dishonestly to exaggerate the signaler s body size and competitive ability. This conclusion differs from that of Gosling & Roberts (2001), who maintain that scent marking by male mammals is cheat-proof (i.e., honest). In Study 1, we found that body size positively predicts urine mark height. This suggests that conspecifics may derive accurate information about the size of signalers from heights of urine marks. However, we also showed that raised-leg angle positively predicts urine mark height (Study 1) and, on average, small dogs perform larger raised-leg angles than large dogs (Study 2). Thus, even though height of urine mark does reflect size of signaler in part, small dogs seem to cheat by using larger raised-leg angles to deposit higher urine marks, thereby exaggerating their size. It is possible that scent marking is honest in some contexts and dishonest in others; this may vary with identity of the signaler, type of information communicated, and property of the scent mark. For example, the olfactory content of scent marks appears to be an honest indicator of health status of males: female mice (Mus musculus) can distinguish between healthy and parasitized males by differences in the odor of their urine marks (Kavaliers & Colwell, 1993; Zala, Potts & Penn, 2004). On the other hand, scent mark height appears to be a dishonest indicator of the signaler s body size and corresponding competitive ability of males in some species: small male dwarf mongooses placed anogenital scent marks higher than expected (Sharpe et al., 2012) and small male dogs exhibited larger raised-leg angles than large dogs (present study). Additionally, even though heights of anogenital marks by male dwarf mongooses were dishonest, heights of those by females were honest (Sharpe et al., 2012), showing that honesty of scent mark height can vary with sex of signaler. Height at withers also significantly and negatively predicted average raised-leg angle, which contrasts with data by Sharpe et al. (2012) for male dwarf mongooses; they found a nonsignificant negative correlation between body length and average scent mark height. Due to differing marking postures, body length of male dwarf mongooses is equivalent to height at withers of male dogs; male dwarf mongooses use the handstand posture to place anogenital marks (i.e., stand on their forelimbs; see Sharpe et al., 2012) whereas male dogs use the raised-leg posture when urine marking (i.e., three limbs remain planted on the ground while a single hindlimb is raised; Fig. 1). Nevertheless, our findings and those of Sharpe et al. (2012) are similar in that body mass is a stronger predictor of average raised-leg angle in male dogs and average scent mark height in male dwarf mongooses than height at withers or body length, respectively. This may be because body mass is a proxy for competitive ability in dogs and other mammals (Scott & Fuller, 1965; Gosling et al., 1996; Taylor, Reby & McComb, 2010) but height is not. Furthermore, our finding that body mass is a better predictor than height at withers of raised-leg angle suggests that raised-leg angle, and by extension relative scent mark height, communicates competitive ability in domestic dogs. This is consistent with the hypothesis that scent marks provide an important means for competitor assessment (Gosling & Roberts, 2001). Our findings add to a growing understanding of the behavioral differences between small and large domestic dogs. Small dogs are more likely than large dogs to exhibit problematic behaviors such as separation anxiety, dog-directed fear, ownerdirected aggression, and urine marking in the home (McGreevy et al., 2013). Small dogs were less motivated than large dogs to approach audio playbacks of growls (Taylor et al., 2010) Journal of Zoology 306 (2018) ª 2018 The Zoological Society of London 167

6 Urine marking in male domestic dogs B. McGuire et al. (a) 3.5e+6 (b) 3.5e+6 Average raised-leg angle (deg)^3 3.0e+6 2.5e+6 2.0e+6 1.5e+6 1.0e+6 Average raised-leg angle (deg)^3 3.0e+6 2.5e+6 2.0e+6 1.5e+6 1.0e+6 5.0e Body Mass (kg) 5.0e Height (cm) (c) 150 (d) 150 Average raised-leg angle (deg) Average raised-leg angle (deg) Body Mass (kg) Height (cm) Figure 3 Plots of response variables (y-axis) versus predictor variables (either body mass or height at withers; x-axis); shading depicts 95% confidence intervals. (a) Average raised-leg angle (cube-transformed) versus body mass. (b) Average raised-leg angle (cube-transformed) versus height. (c) Average raised-leg angle (non-transformed) versus body mass, which is plotted for ease of interpretation. (d) Average raised-leg angle (nontransformed) versus height, which is plotted for ease of interpretation. and a model of a Labrador retriever (Leaver & Reimchen, 2008). During walks outside, small dogs urine mark more frequently than large dogs (McGuire & Bemis, 2017) and exhibit larger raised-leg angles (present study). Among other explanations for these behavioral differences (McGreevy et al., 2013), direct social interactions could be particularly costly to small dogs, given their lesser competitive abilities, thereby prompting hesitant behaviors (Leaver & Reimchen, 2008; Taylor et al., 2010); indirect behaviors, such as leaving a scent mark in the absence of a receiver (McGuire & Bemis, 2017); and larger raised-leg angles and, by extension, relatively high scent marks. It may be uniquely beneficial for small dogs to communicate indirectly (McGuire & Bemis, 2017) and exaggerate their body size and competitive abilities through relatively high scent marks if this enables them to avoid direct conflict. In contrast, large dogs have less incentive to avoid direct conflict due to their greater competitive abilities. Alternatively, over marking may explain our findings. Over marking is used by mammals to cover deposits by conspecifics in favor of displaying their own scent (Johnston, Chiang & Tung, 1994) and is a common behavior in dogs that may, in combination with adjacent marking (i.e., depositing a scent mark adjacent to that of a conspecific), constitute 63% of all urinations (Lisberg & Snowdon, 2011). If a large dog places a scent mark at the height of its hip, a small dog would need to place its urine higher, relative to its own hip, to over mark the large dog s deposit. This requires the small dog to perform a larger raised-leg angle than the large dog (per Study 1). Compared to large dogs, small dogs will encounter more marks that are higher in relation to their own body size for them to over mark; this could explain the negative relationship between body size and average raised-leg angle. Physical constraints may prevent heavy dogs from performing large raised-leg angles, thereby contributing to trends in 168 Journal of Zoology 306 (2018) ª 2018 The Zoological Society of London

7 B. McGuire et al. Urine marking in male domestic dogs our data. For example, heavy dogs may be limited to small raised-leg angles that counterbalance their body mass. During a raised-leg urination, the planted hindlimb of the dog will often lean in the direction opposite the target (see Fig. 1 for an example). It is feasible that a small raised-leg angle, versus a large raised-leg angle, would provide a greater counterbalancing force to offset the lean; this could then be more important in heavier versus lighter dogs. We did not control for the potential importance of raised-leg angle as a counterbalancing mechanism. Companion animals do not compete for survival and reproduction like free-ranging dogs or other wild canids (Bradshaw, Blackwell & Casey, 2016), perhaps making competitor assessment less relevant for dogs in homes or shelters. However, even though outcomes of competitive interactions may be of lesser consequence, companion dogs frequently exhibit agonistic behaviors such as growling and chasing (Bradshaw, Blackwell & Casey, 2009) and intensely investigate each other s urine marks (Lisberg & Snowdon, 2009). Data from Lisberg & Snowdon (2009) indicate that investigation of urine is an important means of competitor assessment in companion dogs, as they found that dogs of lower social status spent more time than dogs of higher social status investigating urine marks of unknown conspecifics. Our findings for male shelter dogs add to those of Sharpe et al. (2012) for free-ranging male dwarf mongooses in showing that some male mammals engage in dishonest signaling via vertical placement of scent marks. Nevertheless, our study and that by Sharpe et al. (2012) were observational. Thus, to further characterize the relationship between scent mark height and signaler s body size, it would be beneficial to conduct experimental studies across multiple species in which over marking is controlled. Future studies should also characterize the responses of dogs to urine marks placed at different heights, similar to work done by White et al. (2002; pandas) and Sharpe (2015; dwarf mongooses). Acknowledgments We thank Stephen Parry for statistical advice, Stacy Farina for advice on video cameras and software, and Lauren Ferris for helpful discussions. Claudia Gerecke, Rebecca Meyer, and William Fry helped with data collection. We also thank Cortland SPCA and Tompkins SPCA for their participation. This research was supported by the Einhorn Discovery Fund, College of Arts and Sciences, Cornell University. References Alberts, A.C. (1992). Constraints on the design of chemical communication systems in terrestrial vertebrates. Am. Nat. 139, S62 S89. Beach, F.A. (1974). 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