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/lp/springer-journals/conspecific-scent-marks-may-influence-underground-site-selection-by-a-ssZeaki5zQ
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- Springer Journals
- Copyright
- Copyright © The Author(s) 2023
- ISSN
- 0340-5443
- eISSN
- 1432-0762
- DOI
- 10.1007/s00265-023-03305-x
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Abstract
Conspecific cues often provide social information on habitat quality that is considered when deciding to settle at a specific site. The type of sensory cues useful for this will depend on the environment. For amphisbaenians, reptiles adapted to an underground life with highly reduced sight, chemoreception is especially useful to recognize conspecifics. Here, we first analyzed the lipophilic compounds from precloacal gland secretions of the amphisbaenian Blanus cinereus, showing that there were sex- and size-related variations in the proportions of the three major compounds. Then, we tested in the laboratory whether there was an underground site selection based on conspecific chemical cues (substrate scent marks) in two different contexts. In loose substrates, both male and female amphisbaenians tended to choose first the scent-marked substrates more often when the individual that produced the scent, independently of its sex, was relatively larger than the focal individual. In contrast, inside semi-permanent galleries, males, but not females, chose the scent-marked gallery more often when the scent donor, independently of its sex, was relatively smaller. These results suggest that the proportions of compounds in scent marks may allow amphisbaenians to estimate the body size of the producer and that this information affects their site selection decisions. However, the different substrate-dependent responses suggest a different meaning and usefulness of scent marks depending on the context. Significance statement The presence of your conspecific in a site may indicate that this is a “quality” site to live in. If you are blind and live under - ground, smell is one of the best options for detecting conspecifics and assessing how good are your surroundings. Here, we test whether a blind amphisbaenian reptile that spends its life buried in sandy substrates uses conspecific chemical stimuli to choose where to settle. We found that this decision is influenced by the microhabitat type, sex, and the size difference between the individual that sniffs and the producer of the scent. Amphisbaenians seem to detect and assess conspecific traits based on the differences in compounds in their odors. Therefore, using conspecific scent to assess habitat quality may help fossorial animals to live underground. Keywords Communication · Chemosensory cues · Habitat selection · Social information · Amphisbaenians · Fossoriality Introduction Animals’ survival and reproductive success depend on their ability to locate necessary resources and avoid potentially detrimental situations. Hence, the evolutionary success of many taxa seems to be associated with the development of Communicated by T. Madsen specific sensory modalities to locate resources and avoid risks (Stevens 2013). For instance, bats and cetaceans rely * José Martín jose.martin@mncn.csic.es on echolocation for foraging and avoiding obstacles (Thomas et al. 2004), and color vision is the basis of mate choice Departamento de Ecología Evolutiva, Museo Nacional in many birds and fishes (Endler et al. 2005). One impor- de Ciencias Naturales, CSIC, José Gutiérrez Abascal 2, tant use of the sensory abilities of an animal occurs when E-28006 Madrid, Spain Vol.:(0123456789) 1 3 29 Page 2 of 11 Behavioral Ecology and Sociobiology (2023) 77:29 deciding whether to select or avoid a habitat or a specific site whose composition differs between sexes (López and Martín to settle. In many species, conspecific cues are often used 2005, 2009). The microscopic morphology of these glands as “social or public information” about habitat quality (e.g., suggests that, as amphisbaenians move inside tunnels, the Stamps 1988; Farrell et al. 2012; reviewed in Danchin et al. secretion plugs are abraded against the substrate releasing 2004; Wagner and Danchin 2010; Buxton et al. 2020), and semiochemicals (Jared et al. 1999). These substrate scent the detection and assessment of these cues are based on dif- marks might be important in intraspecific communication ferent types of sensory modes. Nevertheless, the evolution of and home range recognition (Cooper et al. 1994; López et al. sensory modalities is influenced by the restrictions imposed 2000). Moreover, behavioral studies show that some amphis- by the characteristics of each local environment (Wiley and baenians are capable of short-range detection and discrimi- Richards 1978; Alberts 1992b; Shine 2005; Bradbury and nation between chemical cues of females and males (Cooper Vehrencamp 2011; Stevens 2013). et al. 1994; López and Martín 2009), familiar and unfamiliar Chemoreception is a widespread sensory modality conspecifics (Martín et al. 2020, 2021b), or self-recognition among vertebrates, and chemical stimuli are used for dif- (López et al. 1997; Martín et al. 2020). Together, these stud- ferent purposes (Müller-Schwarze 2006; Wyatt 2014). For ies have brought to light the importance of chemoreception example, fathead minnows employ odors to attract females for the fossorial lifestyle of amphisbaenians. However, it and recognize shoal mates (e.g., Cole and Smith 1992; remains unknown whether and to what extent chemical cues Brown and Smith 1994), and some mammals use gland of amphisbaenians or other fossorial reptiles could be used secretions or urine for conspecific discrimination (e.g., as underground substrate scent marks. These scent marks Swaisgood et al. 1999; Johnston 2003). In reptiles, chem- might act as potential indicators of habitat quality, when oreception is essential for the different aspects of their individuals select a specific site, and might also be used to biology (for a review see Mason and Parker 2010; Martín mark territories or to locate mates. and López 2011). Many reptile species employ chemical Here, we investigated whether chemical cues (sub- cues for detecting prey (e.g., Cooper 1995; Recio et al. strate scent marks) from conspecifics affected under- 2020) and predators (e.g., Amo et al. 2004; King et al. ground site selection by the amphisbaenian Blanus 2008) or for navigation (Chelazzi and Deflino 1986). cinereus. We first examined potential sex- and size- Chemical cues also play a prominent role in intraspecific related variations in lipophilic chemical compounds communication and reproduction of many reptiles (Martín from precloacal gland secretions of this species. Then, and López 2011). In this regard, chemical signals allow we designed two different laboratory approaches to test for reptiles’ sex and familiar discrimination and self- (i) whether adult individuals selected or avoided loose recognition (Alberts 1992a; López et al. 2003; Gonzalo substrates or semi-permanent galleries with scents from et al. 2004; Ibáñez et al. 2012). Furthermore, chemical conspecifics and (ii) whether the sex and size of the con- signals may provide information about the characteris- specifics affected the site selection. In previous studies, tics of potential competitors (Greene et al. 2001; Martín using tongue-flicks as the primary behavioral response and López 2007; Ibáñez et al. 2012) or potential mates suggesting chemical discrimination, it was shown that, in (Martín and López 2000; Greene et al. 2001; O’Donnell addition to conspecific discrimination, male B. cinereus et al. 2004). Finally, reptiles use chemical senses to follow were attracted to female odors but responded aggres- conspecific scent trails for mating (LeMaster et al. 2001; sively by biting cotton swabs bearing the scent of other Bull and Lindle 2002; Shine et al. 2005) or for locating males or specific compounds from precloacal secretions overwintering hibernacula (Brown and MacLean 1983). of males (Cooper et al. 1994; López et al. 1997; López Amphisbaenians are a major distinctive group of reptiles, and Martín 2009). Hence, we hypothesized that (i) males morphologically and functionally adapted to a fossorial life would select substrates and galleries with female odor (Gans 1978). One of the adaptations for living underground while avoiding substrates scent-marked by other males. is a reduced vision (Gans 1978). Hence, chemoreception However, we also anticipated (ii) an effect of body size, may be particularly important for these fossorial reptiles with males avoiding substrates with the scent of rela- (Cooper et al. 1994). In fact, several studies have shown tively larger males, but not those with the scent of rela- that amphisbaenians use their vomeronasal system to detect tively smaller males. Also, given the relatively small odors of prey (López and Salvador 1992; Semhan et al. amount of precloacal secretions produced by these ani- 2010; López et al. 2014), predators and potentially harmful mals, we expected that (iii) the potential effect of scent species (López and Martín 1994, 2001), and different habi- marks would be more pronounced inside semi-permanent tat chemical cues (López et al. 2002; Martín et al. 2021a). galleries, where secretions would be deposited repeat- Some amphisbaenians have precloacal glands that produce edly over the same surfaces, than in loose substrates holocrine secretions, especially during the breeding season, where secretion would be scattered and more randomly distributed, being difficult to detect and identify. 1 3 Behavioral Ecology and Sociobiology (2023) 77:29 Page 3 of 11 29 in a freezer at −20 °C until being analyzed. During each of Methods the sampling events, we also obtained blank control vials using the same procedure but without collecting secretion. Study animals and maintenance These amphisbaenians were measured as indicated above and immediately released at their capture sites. We did not During March and April 2021, we captured under stones collect secretions from the individuals maintained in cap- 25 adult male and 19 adult female B. cinereus amphisbae- tivity to allow their secretions to scent-mark the substrates nians in an oak forest near Navacerrada (40°43′ N, 04°01′ used in the behavioral tests (see below). W; Madrid, Spain). Animals were weighed (body mass: Samples of precloacal secretions were analyzed using gas males: mean ± SE = 5.3 ± 0.3 g; females: 5.4 ± 0.4 g), chromatography coupled to mass spectrometry (Trace 2000 and their snout-vent length (SVL) was measured (males: GC-MS, Finnigan-ThermoQuest). Analytical procedures mean ± SE = 188 ± 3 mm; females: 189 ± 5 mm). After were similar to those used in the previous studies (López capture, we transported in the same day the amphisbaeni- and Martín 2005). Tentative identification of compounds ans to “El Ventorrillo” MNCN-CSIC field station (5 km was made by comparison of the mass spectra in the NIST/ from the capture site), where they were kept individually EPA/NIH 2002 library and using the information from previ- in indoor terraria (40 × 30 × 30 cm) with a 10-cm depth ous descriptive studies where identifications were confirmed substrate of loose coconut fiber. Amphisbaenians were using standards (López and Martín 2005, 2009). We deter- fed mealworm pupae (Tenebrio molitor) three times a mined the relative proportion of the major compounds as week. Amphisbaenians could attain an optimal body tem- the percentage of the total ion current by integrating the perature by thigmothermy with the substrate (López et al. peak areas in the chromatogram using the Xcalibur soft- 1998), which was warmed using a heating cable placed ware (Finnigan Co.). Before statistical comparisons, the below the terraria and connected to a thermostat set at 22 relative areas were transformed following the formula °C. This temperature was close to the substrate tempera- Ln[(proportion)/(1 − proportion)], to correct the problem tures selected by B. cinereus in a thermal gradient (mean of non-independence between proportions (Aebischer et al. ± SE = 20.7 ± 0.5 °C , range = 17.8–23.6 °C; López 1993; García-Roa et al. 2018). We used separated general et al. 1998). Water was provided daily by moistening the linear models (GLMs) to test for differences in transformed substrate with a water spray. Although amphisbaenians relative proportions of the three major compounds found spent all the time buried in the fiber substrate, we kept a (dependent variable) between sexes (fixed factor) and in rela- natural photoperiod with sunlight entering through two tion to body size (log10-transformed SVL; continuous fac- large windows. tor) and including the interaction between sex and size in the To be able to monitor the location of buried amphis- models. When the interaction was significant, we calculated, baenians in the experiments without further disturbance, separately for males and females, Pearson’s linear correla- they had been individually marked with PIT tags (Bio- tion coefficients between the proportion of the compound mark MiniHPT8; Biomark, Inc., Boise, ID, USA; length and body size. = 8.4 mm, diameter = 1.4 mm, weigh = 0.03 g) implanted subcutaneously in the upper right side of the body. This Site selection tests marking procedure has been tested in other amphisbaenian species, showing no long-term negative consequences for To test whether the presence of scents of conspecifics depos- animals (Recio et al. 2019). At the end of the trials, all ited on substrates affected the selection of novel sites by animals were released in an apparently healthy state to amphisbaenians, we considered two different situations that their field capture sites where PIT tag marks were useful mimic natural conditions. In the field, this species selects for further population monitoring. preferentially sandy substrates in which amphisbaenians are not usually able to form semi-permanent galleries, as the loose sandy substrate often collapses immediately after an Chemical analyses of precloacal secretions individual passes burrowing through it (Martín et al. 1991). However, semi-permanent galleries are observed in rela- In the same study area, we captured additional individual tively harder (less sandy) substrates and under rocks that the amphisbaenians (10 males and 10 females) to harvest their species uses for thermoregulation and foraging (López et al. precloacal gland secretions. Immediately after capture, we 1998; JM pers. observ.). Thus, Experiment 1 consisted of a gently pressed around their precloacal pores with forceps choice test between two areas of loose substrates differing to collect the secretion of pores directly in the glass vials only in the fact that one of them had been used by conspecif- with Teflon-lined stoppers. Vials were kept in an ice box ics, presumably scent-marking this substrate with chemical during daily morning field work and in the midday stored 1 3 29 Page 4 of 11 Behavioral Ecology and Sociobiology (2023) 77:29 cues, while the other area was a clean substrate. In contrast, disturbance was possible by detecting the signal of its PIT in Experiment 2, we examined the underground selection of tag (see above) using a hand-held portable reader (Biomark semi-permanent galleries. To simulate these galleries, we 601 Reader) placed above the substrate. Three behavioral employed a T-maze approach with two arms (plastic tubes), variables were recorded for each individual: (a) the “First one of them previously marked with conspecific odor. choice” (i.e., the location of the individual in the first meas- In both experiments, amphisbaenians were tested with ure, 15 min after being released), (b) the number of “Times” the scent of other individuals located at least 50 m from the that the individual was recorded in the scent treatment side responding individual, which, considering the low dispersal during all the trial, and (c) “Final choice,” only estimated ability of amphisbaenians (Martín et al. 2021c) and because for those individuals for which a visit to the scent treatment amphisbaenians were kept in separated individual cages side was recorded at least once in each of the three trials in the laboratory, ensured that they had not had previous (corresponding to the three treatments; N = 19; 10 males, 9 contact and could be considered unfamiliar. To minimize females). Regarding the “Final choice,” we considered that observer bias, blinded methods were used when all behav- the scent treatment side of the cage was chosen when the ioral data were recorded and/or analyzed. proportion of times located in this half of the testing cage in relation to the total number of recordings after first visiting Experiment 1: loose substrate choice it was higher than expected by chance (probability of success = 0.5; tested using two-tailed binomial tests with binom.test Experiment 1 was conducted between the 20th and 30th of function in the stats package; R Core Team 2022). April with all the individuals captured and maintained in At the end of each test, amphisbaenians were returned to captivity (N = 44; 25 males, 19 females). We carried out their home cages, and testing cages were cleaned with abun- experiments individually in testing plastic cages (71 × 46 × dant water and left to dry for more than 12 h before the next 37 cm) with their bottoms covered with a layer of clean loose trial, when new clean or scent-marked substrates were used. substrate of coconut fiber about 5 cm deep. These testing cages were divided into two areas of equal surface (46 × 33 Experiment 2: semi‑permanent gallery choice cm) with a 5-cm wide gap between them. In each of these areas, we added an additional amount of coconut fiber that We carried out T-maze experiments between the 30th June differed in the chemicals it contained. On one of the halves and 2nd July with only part of the amphisbaenians main- of the cage (“control side”), randomly chosen, we added an tained in captivity (15 males, body mass: mean ± SE = 4.9 additional amount of 200 g of clean coconut fiber. This clean ± 0.3 g, SVL: mean ± SE = 185 ± 5 mm; 14 females, body fiber had been stored in the facilities where amphisbaenians mass = 5.0 ± 0.4 g, SVL= 189 ± 5 mm). Underground were maintained, inside empty cages of the same type as semi-permanent galleries were simulated by using two trans- those housing the amphisbaenians, and exposed to the same parent plastic tubes (length = 25 cm; internal diameter = conditions of temperature and humidity. On the other half 16 mm) joined by a T-shaped opaque plastic piece (length of the cage (“scent treatment side”), we added a substrate = 6 cm; width = 4 cm; internal diameter = 12 mm). Both chosen among three treatments: (a) “Male,” (b) “Female,” or tubes differed in the chemicals they contained. One of the (c) “Control.” In “Male” and “Female” treatments, we added tubes was always clean, while the other had been previously 200 g of coconut fiber taken from one home cage where scent-marked with one of three possible treatments: “Male,” another unfamiliar male or female conspecific had been kept “Female,” or “Control.” Scents from “Male” or “Female” individually for at least 2 weeks. In the “Control” treatment, were obtained by leaving a conspecific male or female inside we added 200 g of clean coconut fiber on the treatment side. the tube for at least 12 h before each trial and removing All individuals were tested once per treatment on consecu- it immediately before the tests. Each tube had a longitudi- tive days (one treatment per day), following a randomized nal fissure that allowed air to enter inside it and to prevent block design with a counterbalanced order of presentation. condensation. In the “Control” tests, both tubes were clean. All trials were conducted during the morning (between 9 The side location of the tubes in the T-maze was randomly a.m. and 1 p.m., GTM) in the same room, illuminated with chosen. We performed all trials in the same environmental dim light and maintained at a temperature of 20 °C, close to conditions as in Experiment 1. the preferred temperature of this species (López et al. 1998). We started trials by gently taking an amphisbaenian from Every test began by gently taking the focal individual its home cage and releasing it on the substrate in front of the from its home cage and placing it in the middle gap of a T-shaped plastic piece with the snout facing the entrance, testing cage. Amphisbaenians explored the area for some so that the individual typically moved quickly inside the seconds and quickly buried themselves in the substrate. tubes. Then, we noted which arm (gallery) of the T-maze Then, we noted every 15 min for 2 h (8 recordings) the the amphisbaenian chose (variable “Initial choice”), i.e., position of the animal. Locating buried individuals without the arm tube where the individual’s head and first third of 1 3 Behavioral Ecology and Sociobiology (2023) 77:29 Page 5 of 11 29 the body trunk were first seen, after passing through the test was made within the “Individual” and included this as a T-shaped piece. Then, amphisbaenians typically moved random factor in the models for both experiments. forward inside this arm tube. This was the only behavioral variable recorded in Experiment 2. At the end of each test, animals were returned to their home cages, and the tubes Results were cleaned with water as we did with the testing cages. Chemical variations of precloacal secretions Statistical analyses of behavioral data The compounds found in the precloacal secretions of Modeling of behavioral data was conducted in the R statis- amphisbaenians were similar to those found in the pre- tical software (version 4.2.1; R Core Team 2022). We first vious published analyses, with cholesteryl methyl ether made contingency tables with the observed number of indi- (relative abundance, mean ± SE = 39.3 ± 3.0 %; range viduals in each treatment that made an initial choice of the = 11.2–57.0 %) and cholesterol (35.8 ± 3.0 %; range = scent-marked side or arm and those that chose the control 22.6–70.2 %) being the most abundant compounds and side or arm. Then, we performed two-tailed binomial tests with squalene also being relevant in some individuals (3.1 with binom.test function in the stats package (R Core Team ± 1.0 %; range = 0.4–15.1 %). There were also some other 2022) to test, for each scent treatment, whether the number minor compounds (less than 5 %) such as dodecanoic acid of individuals that chose a particular side or arm was differ - (3.7 %), cholesta-5,7-dien-3-ol acetate (3.3 %), or camp- ent than expected by chance (probability of success = 0.5). esterol (1.5 %). We also used Pearson’s chi-square tests for independence Relative proportions of cholesteryl methyl ether were (chisq.test function in stats package; R Core Team 2022) to significantly higher in males than in females (GLM, sex: test for differences in side or arm choice among treatments. F = 12.30, p = 0.003), and larger individuals had rela- 1.16 In addition, we fitted generalized linear mixed models tively lower proportions (SVL: F = 62.01, p < 0.0001), 1.16 (GLMM) with glmer function in the lme4 R package (Bates although the pattern of decrease in cholesteryl methyl et al. 2015) using a binomial distribution. In the models, ether with size differed slightly between sexes (interac- we initially included the “Sex” of the focal individual and tion: F = 12.33, p = 0.003) (Pearson’s correlations, 1.16 the “Scent” treatment (Male, Female, or Control) as fixed males: r = −0.92, p = 0.0009; females: r = −0.91, p = factors, the size (“SVL”) of the focal individual as a covari- 0.0003) (Fig. 1a). ate, and the “Individual” as a random factor, according to Proportions of cholesterol were significantly higher our repeated measures design. We selected the model with in females than in males (GLM, sex: F = 14.82, p = 1.16 the lowest Akaike value corrected for small sample sizes 0.0014) and varied significantly with body size (SVL: (AICc function in the MuMIn package; Barton 2020) and F = 34.97, p < 0.0001) but with a different strength 1.16 employed the likelihood ratio test (LRT) (lrtest function in each sex (interaction: F = 14.98, p = 0.0013), with 1.16 in the lmtest package; Zeileis and Hothorn 2002) as the cholesterol increasing significantly with size in females omnibus test. After obtaining the most suitable model, we (Pearson’s correlation, r = 0.92, p = 0.0002), but not sig- conducted Wald’s chi-square tests for mixed models (Anova nificantly in males (r = 0.47, p = 0.17) (Fig. 1b). function in the car package; Fox and Weisberg 2019) to Finally, proportions of squalene were significantly estimate the effects of the covariate, the fixed factors, and higher in males than in females (GLM, sex: F = 9.72, 1.16 their interactions. p = 0.007) and varied significantly with body size (SVL: In further analyses, we tested the effect of the “Size dif- F = 5.92, p = 0.027) but in a different way in each 1.16 ference” between the focal responding individual and the sex (interaction: F = 10.44, p = 0.005), with squalene 1.16 one that had donated the scent (SVL focal − SVL donor; increasing significantly with size in males (Pearson’s cor - negative numbers indicating a relatively larger donor while relation, r = 0.75, p = 0.012) but tending to decrease with positive numbers indicating a relatively small donor). We size, although not significantly, in females (r = −0.36, p performed the same analyses as above but we replaced = 0.30) (Fig. 1c). the covariate “SVL” with the covariate “Size difference.” Because in the “Control” scent treatments, there was no Experiment 1:loose substrate choice donor, and we excluded this treatment and analyzed only the trials with chemicals from another conspecific (i.e., “Male” In all scent treatments, amphisbaenians did not significantly and “Female”). Therefore, the order of stimulus presenta- select the control or the scent-marked side in their “First tion could not be considered as counterbalanced and, thus, choice” more often than expected by chance (two-tailed to control for this effect, we nested the “Day” when each binomial tests, focal males, Control: p = 0.11; Female scent: p = 0.42; Male scent: p = 0.23; focal females, Control: p = 1 3 29 Page 6 of 11 Behavioral Ecology and Sociobiology (2023) 77:29 Fig. 1 Relationships between relative proportions (% TIC area) of the ▸ three major compounds found in precloacal secretions (a cholesteryl methyl ether, b cholesterol, and c squalene) and body size (snout-to- vent length, SVL) of male (black dots, continuous line) and female (white dots, dashed line) B. cinereus amphisbaenians 0.36; Female scent: p = 0.36; Male scent: p = 0.99). Moreo- ver, there were no significant differences among the scent treatments in the number of individuals that selected as their “First choice” the scent-marked side in a loose substrate, in comparison with an expected random selection of the sides, neither in male (Pearson’s chi-square test of independence, 2 2 χ = 5.59, p = 0.06) nor female amphisbaenians (χ = 2 2 1.29, p = 0.52) (Fig. 2a). A similar lack of effect of the scent treatment was found when the “Final choice” was considered 2 2 (males: χ = 0.36, p = 0.84; females: χ = 1.50, p = 0.47). 2 2 Results of the GLMMs for the choice of a side of the cage in a loose substrate showed that none of the selected models using the Akaike criterion successfully achieved sta- tistical significance in the omnibus tests, except in the case of the “First choice” variable when the “Size difference” between the donor of scent and the focal animal and the “Scent” treatment were included in the model (LRT, χ = 12.49, p < 0.01) (Table S1). In this model, only the effect of the “Size difference” was significant (Wald’s test, χ = 7.73, p = 0.0054), but the effect of “Scent” was not (Wald’s test, χ = 2.40, p = 0.12). Therefore, both focal male and female amphisbaenians tended to choose first the scent-marked side more often when the donor individual that produced the scent was relatively larger than the focal individual, inde- pendently of the sex of the donor (Fig. 3). Experiment 2: semi‑permanent gallery choice In all scent treatments, amphisbaenians did not significantly select the control or the scent-marked arm of a gallery in their “First choice” more often than expected by chance (two-tailed binomial tests, focal males, Control: p = 0.61; Female scent: p = 0.99; Male scent: p = 0.12; focal females, Control: p = 0.42; Female scent: p = 0.79; Male scent: p = 0.79). In addition, there were no significant differences between the scent treatments in the number of individuals that selected as their “First choice” the scent-marked arm inside a gallery, in comparison with an expected random selection of the arms, neither in male (Pearson’s chi-square test of independence, χ = 3.42, p = 0.18) nor female amphisbaenians (χ = 1.35, p = 0.51) (Fig. 2b). When running GLMM models for the “First choice” of an arm inside a gallery, with “SVL” as a covariate, the model containing “Scent” seemed the most suitable according to the Akaike criterion, but the likelihood ratio test did not reach a significance (see Table S2). However, when includ- ing “Size difference” as a covariate instead of “SVL,” the 1 3 Behavioral Ecology and Sociobiology (2023) 77:29 Page 7 of 11 29 p < 0.01) (Table S2). However, in this model, only the inter- action between “Sex” and “Size difference” was significant (Wald’s test, χ = 4.02, p = 0.045), while the rest of the fac- tors and interactions did not reach a statistical significance (Wald’s tests, χ < 3.46, p > 0.063 in all cases). We ran fur- ther the GLMM analyses separately for males and females that included “Size difference” as a covariate, “Scent” treat- ment as a factor, and the “Day” nested within “Individual” as random factors. For males, we found that the model includ- ing “Size difference” had the lowest Akaike value (AICc null model = 46.35; AICc selected model = 41.22; AICc other models >> 43.64), and the omnibus test was statisti- cally significant (LRT, χ = 7.81, p = 0.0052), although the chi-square test for the “Size difference” effect did not reach significance (Wald’s tests, χ = 2.49, p = 0.11). For females, the model containing both “Scent” treatment and “Size difference” and their interaction was the most suitable under our criteria (AICc null model = 45.51; AICc selected model = 44.88; AICc other models >> 47.56; LRT, χ = 9.64, p = 0.022), but none of the factor was significant in the chi-square tests (Wald’s tests, “Scent,” χ = 0.064, p = 0.80; “Size difference,” χ = 0.016, p = 0.90; “Scent” × “Size dif- ference,” χ = 2.70, p = 0.10). Therefore, males tended to choose the scent-marked gallery more often when the donor Fig. 2 Number of individual focal male and female B. cinereus amphisbaenians that selected in their “First choice” the control or the scent-marked a side in a loose substrate (Experiment 1) or b arm in semi-permanent galleries (Experiment 2) in each scent treatment model containing both “Sex” of the focal individual, “Scent” treatment, “Size difference,” and their interactions was the most suitable and reached a significance (LRT, χ = 21.70, Fig. 4 First choice of the control or scent-marked arm in semi-perma- Fig. 3 First choice of the control or scent-marked side in a loose sub- nent galleries (Experiment 2) by focal a male or b female B. cinereus strate (Experiment 1) by focal male and female B. cinereus amphis- amphisbaenians in relation to body size difference (i.e., the SVL of baenians in relation to body size difference (i.e., the SVL of the focal the focal individual minus the SVL of the donor; negative numbers individual minus the SVL of the donor; negative numbers indicating a indicating a relatively larger donor) in treatments with scent of con- relatively larger donor) specific males or females 1 3 29 Page 8 of 11 Behavioral Ecology and Sociobiology (2023) 77:29 of the scent was relatively smaller than them, independently Our chemical analyses also showed the novel findings of the sex of the scent donor, while a lack of effect was found that there were clear relationships between the proportions for females (Fig. 4). of some major compounds in precloacal secretions of B. cinereus amphisbaenians and the body size of the pro- ducer. The behavioral experiments of site selection showed Discussion the effects of the difference in body size between the focal amphisbaenian and the producer of the scent-mark, sug- This study found some weak, but significant, effects of gesting that the proportion of compounds in scent marks substrate scent marks from conspecific on the underground may allow amphisbaenians to estimate the body size of the site selection decisions in the amphisbaenians B. cinereus. producer. For example, a large individual would have secre- These effects may be related to the observed inter-individual tions with less cholesteryl methyl ether and more cholesterol variability in compounds of the precloacal gland secretions and, in the case of males, also with more squalene. How- from which scent marks very probably originated. However, ever, the size-related responses of amphisbaenians to scent the importance and direction of these effects seemed to be marks were different inside the simulated semi-permanent independent of the sex of the producer of the scent mark. galleries and in loose substrates. As predicted, it is likely Rather, they depended on the sex of the responding animal that, in a loose substrate, the concentration of the secretion and on the microhabitat context (loose substrates vs. semi- compounds that produces the scent was low, and the scent permanent galleries), which would presumably affect the marks might be scattered, mixed, and dispersed over a large usefulness and meaning of scent marks. volume of substrate. This would occur because the conspe- Our chemical analyses first confirmed that the major cific scent donor would not be able to scent-mark repeatedly compounds found in precloacal secretions of B. cinereus the same locations, as on each occasion it passed through amphisbaenians clearly differed between sexes (see also different sections of the substrate. In that situation, in our López and Martín 2005, 2009). Detecting these chemical experiment with loose substrates, the responding individu- differences very likely allows amphisbaenians to discrimi- als might not always be aware of the presence of these scent nate between male and female scents, as it was found in marks or might not be able to identify them. This would previous experiments that measured tongue-flicking chem- explain why the responses observed in Experiment 1 (loose osensory responses (Cooper et al. 1994; López and Martín substrates) were similar in males and females and in most 2009). Based on these previous findings, we expected that, cases not significantly different. In contrast, in Experiment in the current experiments, amphisbaenians would have also 2 (inside semi-permanent galleries), the scent marks would shown differential responses to scent marks of males and be more concentrated and more clearly defined, being more females. However, we did not find that the sexual identity of easily detected by the focal individuals and providing more the producer of the scent mark affected to the site or gallery information about the producer and thus allowing the more selection decisions, neither in male nor female responses. specific sex-related responses observed. This lack of effect might be simply explained if substrate Moreover, the directions of the responses were also dif- scent marks would change their chemical characteristics ferent depending on the microhabitat context. In loose sub- after some time of being deposited, for example, because strates, amphisbaenians tended to select first the sites with of chemical transformations of the compounds by oxidation scents of relatively larger animals. This might be explained due to the humidity of the substrate (Regnier and Goodwin if amphisbaenians selected these sites simply because the 1977; Alberts 1992b; Apps et al. 2015) or by soil micro- chemical size-related characteristics in secretions of these organisms (Murphy et al. 2007). In previous tongue-flick larger individuals (e.g., with more cholesterol or more trials, amphisbaenians were able to discriminate the sexes squalene) might allow scent marks to be more easily detected when the fresh secretion was collected from a conspecific in a loose substrate, while the scent of smaller individuals and immediately offered to the responding individual just would not be easily detected, possibly leading to random in front of its snout (Cooper et al. 1994). However, com- responses. Therefore, these results might suggest that the pounds of scent marks in underground substrates might be mere detection of scent from any conspecific would indi- altered, or the scent mark might be scattered and not be eas- cate the “quality” of a new site, which would provide quick ily detected by the focal animals, which would preclude the information for making a first choice decision about whether scent mark to provide enough information to discriminate to continue exploring a new area. Similarly, many studies between sexes. Alternatively, the sexual identity of the pro- of crustaceans (Zimmer-Faust 1985), insects (Norris 1970), ducer might not be important if the mere detection of a scent fish (Bett and Hinch 2015; Galbraith et al. 2017), amphib- mark of any conspecific was enough information to indicate ians (Aragón et al. 2000a; Secondi et al. 2005; Gautier et al. the quality of a given site. 2006), and reptiles (Aragón et al. 2001, 2006; Scott et al. 2013) demonstrated an attraction for conspecific scents when 1 3 Behavioral Ecology and Sociobiology (2023) 77:29 Page 9 of 11 29 selecting a habitat (see reviews in Mason and Parker 2010; displacements around the same small areas (Martín et al. Buxton et al. 2020). 2021c), which also seems to be the case in B. cinereus In contrast, inside galleries, where freshly and unaltered (JM unpubl. data). Therefore, the usefulness of scent marks scent marks should be more evident and informative indicat- of unknown conspecifics in the underground environment ing the current presence of a conspecific, male amphisbae- indicating habitat quality of new sites might also be limited nians, but not females, avoided using galleries scent-marked if this amphisbaenians species is usually restricted to the by relatively larger individuals. This suggests that, in this same small areas where the conspecifics they can find are context, male amphisbaenians were able to assess and con- mostly familiar ones. Nevertheless, the responses to scent sider not only the presence but also the competitive ability of marks could be different depending on the familiarity or the donor as indicated by the body size of the producer of the genetic relatedness between individuals, as other amphis- scent mark, very likely again based on the chemical charac- baenian species seem able of familiar chemosensory rec- teristics of the secretions. The cost of encountering the indi- ognition (Martín et al. 2020, 2021b). Thus, in the fossorial vidual that has produced the scent mark would depend on environment, short-distance direct chemical communica- the competitive ability of both the signaler and the receiver tion between amphisbaenians, as shown on previous studies (Gosling et al. 1996a, b). Although the existence of male (e.g., Cooper et al. 1994), would be more important than combat in amphisbaenians has not been examined, previous scent marks. Nevertheless, we conclude that some infor- experiments showed that males often respond aggressively mation derived from conspecific scent marks still seems to the scent of other males (and also to high concentrations to be useful when selecting an underground new site. In of squalene alone, which is typical of secretion of males), loose substrates, disperse conspecific scents might simply but not to the scent of females (Cooper et al. 1994; López indicate the “quality” of a new site. In contrast, inside gal- et al. 1997; López and Martín 2009), suggesting that male leries, more evident scent marks might indicate the current intrasexual aggression may exist. Thus, male amphisbae- presence of an unfamiliar conspecific, which would force nians would avoid galleries used in the immediate past by male amphisbaenians to also consider the competitive abil- a relatively larger resident individual because this could ity (body size) of the producer, avoiding galleries used by behave aggressively defending its “territory” in case of an relatively larger individuals. encounter. In contrast, a relatively smaller conspecific could Supplementary Information The online version contains sup- be easily defeated. Similar size-dependent responses to scent plementary material available at https:// doi. or g/ 10. 1007/ marks of conspecifics have been found in other species when s00265- 023- 03305-x. assessing the quality of an unknown territory (Gosling et al. Acknowledgements We thank two anonymous reviewers for their help- 1996a, b; Aragón et al. 2000b, 2001; Ibáñez et al. 2012). ful comments and “El Ventorrillo” MNCN-CSIC Field Station for the Although this amphisbaenian species prefers sandy sub- use of their facilities. strates, which are easier to dig (Martín et al. 1991), it also uses semi-permanent galleries formed under stones and in Authors’ contributions All authors designed the methodology, col- lected and analyzed the data, contributed critically to the draft, and their close surroundings, which allows a quick and little gave their final approval for the publication. costly access to these stones for thermoregulation and forag- ing (López et al. 1998). Our study suggests that scent marks Funding Open Access funding provided thanks to the CRUE-CSIC might not be very useful in loose substrates but still some- agreement with Springer Nature. This work was funded by Span- ish Ministerio de Ciencia, Universidades e Innovación project times may provide some approximate first guidance informa- PGC2018-093592-B-I00 (MCIU/AEI/FEDER, UE) and Ministerio tion on site quality. In contrast, scent marks inside galleries de Ciencia e Innovación project PID2021-122358NB-I00 (MCIN/ could have a more important and direct role in intraspecific AEI /10.13039/501100011033 and ERDF A way of making Europe). communication and spatial orientation, also affecting settle- Data availability Our data are available in Figshare at: https:// doi. org/ ment decisions. Similarly, other fossorial animals that use 10. 6084/ m9. figsh are. 21583 935. galleries to move underground, such as rodents, ants, or ter- mites, use scent marks deposited inside these galleries for Declarations intraspecific communication (e.g., Vander Meer et al. 1998; Johnston 2003). Ethics approval The captures enforced all the present Spanish laws and were performed under license granted by the “Dirección Gen- The weak and sometimes little specific responses to eral de Biodiversidad y Recursos Naturales,” Comunidad Autónoma scent marks observed in this study might be explained if de Madrid (Spain) (Ref. 10/170740.9/21). The experiment followed our experimental conditions confronting amphisbaenians ASAB (2020) guidelines for the ethical treatment of animals in behav- ioral research and was in accordance with the national animal wel- with entirely new sites were not replicating a common situ- fare standards and protocols supervised by the “Comisión Ética de ation in nature for these animals. Other species of amphis- Experimentación Animal (CEEA)” of the Museo Nacional de Ciencias baenians seem to show high site fidelity, with very short 1 3 29 Page 10 of 11 Behavioral Ecology and Sociobiology (2023) 77:29 Naturales, CSIC, and the “Comité de Ética” of the Spanish National Chelazzi G, Delfino G (1986) A field test on the use of olfaction in Research Council (CSIC) (Code:901/2020). homing by Testudo hermanni (Reptilia: Testudinidae). J Herpetol 20:451–455 Competing interest The authors declare no competing interests. Cole KS, Smith RJF (1992) Attraction of female fathead minnows, Pimephales promelas, to chemical stimuli from breeding males. J Chem Ecol 18:1269–1284 Open Access This article is licensed under a Creative Commons Attri- Cooper WE Jr (1995) Foraging mode, prey chemical discrimination, bution 4.0 International License, which permits use, sharing, adapta- and phylogeny in lizards. Anim Behav 50:973–985 tion, distribution and reproduction in any medium or format, as long Cooper WE Jr, López P, Salvador A (1994) Pheromone detection by as you give appropriate credit to the original author(s) and the source, an amphisbaenı́an. Anim Behav 47:1401–1411 provide a link to the Creative Commons licence, and indicate if changes Danchin É, Giraldeau LA, Valone TJ, Wagner RH (2004) Public were made. The images or other third party material in this article are information: from nosy neighbors to cultural evolution. Science included in the article's Creative Commons licence, unless indicated 305:487–491 otherwise in a credit line to the material. If material is not included in Endler JA, Westcott DA, Madden JR, Robson T (2005) Animal visual the article's Creative Commons licence and your intended use is not systems and the evolution of color patterns: sensory processing permitted by statutory regulation or exceeds the permitted use, you will illuminates signal evolution. 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Journal
Behavioral Ecology and Sociobiology – Springer Journals
Published: Mar 1, 2023
Keywords: Communication; Chemosensory cues; Habitat selection; Social information; Amphisbaenians; Fossoriality