ISSN 1062-3590, Biology Bulletin, 2016, Vol. 43, No. 9, pp. 1–10. © Pleiades Publishing, Inc., 2016. Original Russian Text © A.Yu. Tsellarius, E.Yu. Tsellarius, E.A. Galoyan, 2016, published in Zoologicheskii Zhurnal, 2016, Vol. 95, No. 7, pp. 848–859.

Social Relationships between Males and Females in the Rock ( brauneri, ): 1. Friendly Monogyny in Males and Polyandry in Females A. Yu. Tsellariusa, *, E. Yu. Tsellariusa, and E. A. Galoyanb, ** aSevertsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 119071 Russia bMoscow State University, Moscow, 199991 Russia *e-mail: [email protected] **e-mail: [email protected] Received August 8, 2015

Abstract—A natural settlement of Brauner’s rock was observed on the Navagir Ridge (Krasnodar region) in the years 1997–2006. In various years, the settlement included from 18 to 28 adult individuals. Analysis of the frequency of affiliative behavior in the course of intersexual contacts and the frequency of males’ attendance of female’s comfort zones revealed three types of intersexual dyad relationships: (1) friendly, or A-relations (maximal values of both indices; maximal duration of interrelation; and the only reason for the termination of interrelations is death of one of the partners); (2) R-relations (minimal values of all the indices and the main reason for the termination of interrelations is female resettlement); and (3) N-rela- tions (intermediate values of indices and the main reason for the termination of interrelations is transition to another type). Both males and females could simultaneously have several R- and N-interrelations. In males, the A-relations towards only a single female was always observed. In females, the A-relations could form simultaneously with two males. Approximately one-third of the friendly connected groups were polyandrous triads (female and two males); the rest were monogamous (male and female). Apparently, in this species there is a general tendency towards social polyandry, which is restrained by certain social and/or environmental factors.

Keywords: friendly interrelations, affiliative behavior, spatial association, social monogamy, social polyandry, lizards, Darevskia brauneri DOI: 10.1134/S106235901609017X

INTRODUCTION flicts; or cooperative activity in one form or another (foraging, parental care, defense against a predator, The formation of social interactions between sexes etc.). These attributes are also inherent in social is one of the most actual problems of behavioral ecol- 1 ogy, and, in our opinion, the most intriguing aspect of monogamy (Wickler, Seibt, 1983; Gillette et al., such interrelations are intersexual relationships lack- 2000; Ulrich, Christophe, 2003), which is, strictly ing evident practical value, including reproductive speaking, a subcase of a heterosexual alliance, is much value, that are denoted as “personal affection” more common than classical homosexual alliances, (Baskin, 1976), “an informal relationship” (Panov, and, generally, has been studied much better. 1983), or “an emotional bond” (Sun et al., 2014). Social monogamy (sensu, Wickler and Seibt, 1983) Essentially, we are referring to the so-called alliances is observed in many unrelated taxa (Mathews, 2002). (sensu, Plyusnin, 1990), a type of social organization Most theories associate its origin with attempts of known for many higher vertebrates (Power, 1967; monopolization of a sexual partner (mate guarding) Baskin, 1976; Panov, 1983; Holtzman, 1984; and oth- and/or with the benefits of the aforementioned coop- ers). The most accurate description of such relation- 1 The traditional terms such as monogamy, polygamy, and poly- ships is the word “friendly”. The alliances can be andry (female polygamy) are not sufficient for description of either homo- or heterosexual, and the following is typ- interrelations between sexes since they do not reflect sex differences ical for members of any alliance: disregard of individ- of socio-sexual strategies. For example, polygamy in the classical ual distance; spatial association; specific interactions understanding implies a combination of polygamy of a male and monogamy of females in his “harem”. We use these terms in the proceeding with physical contact which performs out classic meaning to refer to the system of relationships in general, of sexual, agonistic, hierarchical or orientation context while in the context of sex strategies we use the terms (affiliative behavior); mutual support in social con- mono(poly)gyny for males and mono(poly)andry for females.

1 2 TSELLARIUS et al. erative activity (Emlen and Oring, 1977; Carter et al., sexual relationships of Brauner’s lizard and to over- 1995; Gowaty, 1996; Mathews, 2002; Chapple, 2003; view the developmental scenarios of such relation- and others). However, there are species for which ships, to study the search process and choice criteria of social monogamy is not accompanied by any kind of a social partner of individuals belonging to different cooperative activity and its attributes comprise only sexes, and to determine social factors regulating the spatial association and mutual affiliative behavior development of the friendly relationships. Since (Gillette et al., 2000). Among the higher vertebrates, females of this species form stable social relations with ter- such species are certain lizards (Bull, 2000; O’Connor ritorial males only (Tsellarius, A.Yu. and Tsellarius, E.Yu., and Shine, 2004). At the same time, social monogamy 2006), here we don’t discuss relationships between in lizards is hardly explained from the perspective of females and nonterritorial males. Following goals were any accepted hypothesis of the origin of this phenom- set in the report at hand: description of different types enon, at best requiring introduction of supplementary of social relations between males and females of hypotheses post hoc (How and Bull, 2002; Chapple, Brauner’s rock lizard; detection of peculiarities and 2003; Leu et al., 2010). All of this makes lizards a sub- quantity of different intersexual social bonds in indi- ject of great interest for study from the perspective of viduals belonging to different sexes. the theory of the evolution of intersexual sociality (O’Connor and Shine, 2004). Personalization of relationships and a relative com- AREA AND METHODS OF STUDY plexity of social organization have long been known for The studies took place within the area between lizards (Evans, 1937, 1951). Stable spatial association of Anapa and Novorossiisk, on the south flank of the heterosexual groups members is described in a number Navagir Ridge (altitudes 475 to 504 m). The flank is of species (Auffenberg, 1978; Bull, 1994; Schmidt, cleaved with the narrow valleys, the bottoms of these 1997; Mouton et al., 1999; Panov and Zykova, 1999; valleys are covered by a high dense forest of hornbeam Chapple, 2003; and others), and, in some species, there (Carpinus betulus) with the presence of beech (Fagus exists mutual affiliative behavior of spatially associated orientalis), common ash (Fraxinus excelsior), and lin- males and females (Panov and Zykova, 1999; Tsellarius, den (Tilia sp.). The thickness of the forest litter E.Yu. and Tsellarius, A.Yu., 2005). reaches up to 30 cm; the underbrush and grass vegeta- The object of our studies was a bisexual species of tion are very sparse; large boulders and outcrops of rock lizard, Darevskia brauneri (Mehely 1909)2. For bedrock are present. The air and surface temperatures this species polygynoandrous system is mainly proper; are insufficient for normal activity most of the time, however, the degree of spatial association of individual thus, lizards are in need of regular basking (Tsellarius, with different members of it’s “harem” varies, and so A.Yu. and Tsellarius, E.Yu., 2001). Probably, due to does the frequency of mutual affiliative behavior these conditions, the settled inhabitants are mostly (Tsellarius, A.Yu. and Tsellarius, E.Yu., 2005; Tsellar- observed in openings formed in the location of one or ius, E.Yu. and Tsellarius, A.Yu., 2005, 2006). Thus, two large fallen trees, where the population density is we are dealing with varying degrees of attractiveness of several times higher than in any other habitat (Tsellar- the partners and varying “degree of monogamy”. This ius, A.Yu. and Tsellarius, E.Yu., 2001). phrase appears to be paradoxical; however, it is to be The materials that form the basis for the present expected, since both essential features of social paper were collected during observations on one of the monogamy, high degree of spatial association and high openings at the bottom of the valley (Fig. 1). The total area frequency of affiliative behavior, are quantitative traits of the observation sector was approximately 2000 m2. The and, hypothetically, their values can change within the home ranges of the majority of settled individuals of range of 0 to 1. Study of such “irregular” social polyg- Brauner’s lizard were completely or at least partially ynoandry is of undeniable interest for understanding within the spot of sunlight coming through a gap in the the origins of monogamous relationships. forest canopy, that was moving throughout the day. It is not sufficient to determine the relative inclu- The area of that space was approximately 300 m2. sive fitness of society members with different social From 18 to 28 settled and temporarily settled individ- strategies to understand how one social phenomenon uals lived there in different years; i.e., the density of or another has formed. It is just as important to know the settled part of population was approximately 5–9 actual ways and mechanisms of development of social individuals per 100 m2. Further on we term this lizard relationships with conspecifics in the ontogenesis of a assemblage as a settlement. given individual. Strictly speaking, any reference to ultimative factors would be completely speculative Our studies were conducted over the course of ten until proximal mechanisms of development of the years, from 1997 to 2006. In the years of 1997–1998 given type of relationship is unknown. The aims of our and 2000–2001, constant monitoring started at the research was to describe the system of friendly inter- end of April and ended in September, while in other years observations were carried on in June and July for 2 We called this species Lacerta saxicola in our earlier works dating one or two months each year. All quantitative data on up to 2006, inclusive. lizard behavior used in the current article refer to the

BIOLOGY BULLETIN Vol. 43 No. 9 2016 SOCIAL RELATIONSHIPS BETWEEN MALES AND FEMALES 3

Year 1998

06 m

1

2 N 3 4

5 S 6

Fig. 1. Map of the study area as of 1998: 1, stream; 2, bedrock outcrops; 3, trees; 4, deadfall; 5, large boulders; 6, sunlight spot at 10:00, 14:00, and 18:00 hours (from left to right). period between mid-May and the end of August. In The area of the settlement was monitored by one or May 1997, we caught, measured, and marked most of two observers for at least an hour, usually for four to six the adult settled lizards inhabiting the opening. Fur- hours per day, during almost each of the days with ther on, we caught and marked newly arrived individ- weather suitable for lizard activity. Field glasses 8 × 30 uals and those, who have lost their mark. We used two and 10 × 50 were used for observations. The total methods of marking simultaneously. The life-long duration of visual observations for the whole period of identification number was assigned by amputation of study was 1124 person-hours, and 28 hours of video distal phalanges of one to three toes in a specific com- recording. In the current article, descriptions of 1126 bination. In addition to that, we fixed one or two col- intersexual contacts are used. We term as a contact two ored beads 2 mm in diameter in varying combinations types of situations: (1) all cases with at least one indi- on the back of the lizard in the area of the withers. It vidual visibly reacts to the presence of another; (2) if was shown that amputation of the phalanges and the no reaction is observed, the event where individuals fixing of the beads do not affect the behavior and sur- approach each other to within a distance of 0.5 m. vivability of lizards (Rodda et al., 1988; Dodd, 1993), For each period of time, observations were focused which is also evident from our observations of the marked only on a single individual. During observation, the individuals (Tsellarius, A.Yu. and Tsellarius, E.Yu., trajectory of the individual, locations of stops and 2009). While discussing specific individuals in the their duration, type of activity, locations of contacts text, we refer to their number, assigning the M index to with other individuals were plotted on a map. The males and the F index to females. In total, we marked presence of different behavioral complexes (see the 211 individuals over the period of observation. section Intersexual behavior and spatial association)

BIOLOGY BULLETIN Vol. 43 No. 9 2016 4 TSELLARIUS et al. during a contact was recorded and, in some cases, the Main text and tables contain the shortenings accord- sequence of behavioral acts of contact participants ing to the following legend: U, Mann–Whitney U test; were noted. Pictograms were used in order to increase H, Kruskal–Wallis H test; ϕ*, F-test; rsp, Spearman’s the precision and content of the notes. Video record- rank correlation coefficient; P, confidence probabil- ing was used mostly for specification of the sets of ity; Me, median. The variants were expressed as round behavioral acts of different social behavioral com- numbers for ranges. Quantitative indices that charac- plexes. terize the behavior or relationships of the studied indi- The “point of individual sighting” or registration viduals were calculated separately for each year. Thus, point is a key concept for detection of the home range the size of the dataset is, in many cases, not the real configuration (Jennrich and Turner, 1969; Rose, number of dyads or individuals, but rather the number 1982). Within the framework of the present study, we of “dyad х seasons” or “individual х seasons.” define such point as the location of an unmoving liz- ard outside of the shelter for approximately 1 min RESULTS (thus, ten minutes in uninterrupted nonmotility were counted as ten points). Stops shorter than a minute Intersexual Behavior and Spatial Association were not considered. In actual practice, precision of In analyzing the relationships of males and the fixation of the beginning and end of the unmoving females, we took into account the behavioral com- state is ±20–30 s; however, within the framework of plexes (sensu, Panov, 2005) most common in intersex- the current study, this error does not have a significant ual interactions, which were divided into four func- influence on the results. Short breaks of nonmotility tional groups. Below, we described the complexes in (rush for a fly, crawling for several centimeters, orien- their typical intensity (sensu, Morris, 1957), although, tation response, change of pose, etc.) were not taken in nature, the complexes were mainly realised in a into account. reduced form. We define the home range as an area includes all Rejecting behavior (R-behavior). In intersexual registration points , which is contoured by the method contacts with territorial males, R-behavior has been of a convex polygon (Rose, 1982). Stops during excur- registered only for females. It includes two behavioral sions (sensu, Madison, 1985), that are clearly different complexes. Circumduction, turning up the head com- from local movements, were not taken into account. bined with energetic drumming (rotation of the fore- Within the home range, registration points concen- limbs), flattening of the body in dorso-ventral direc- trate within certain areas; we further term these areas tion, and horizontal wriggling of the tail. Flight, a the comfort zones (CZ). In order to determine a CZ, a retreat outside the contact distance. Circumduction grid with cells of 0.25 × 0.25 m in the scale of the map and flight are combined in most cases. Based on the was plotted on a schematic map of home range, and context, these complexes expressing rejection of inter- distribution of registration points within the cells was actions with a male. analysed. Cells with a number of points larger than Affiliative behavior (А-behavior). It observed during expected value for uniform distribution, with confi- ≥ intersexual contacts only, in both males and females, dence probability 0.99 (Samuel and Green, 1988), always outside of sexual or agonistic context. A lizard were considered as included in the comfort zone. crawls upon and over the partner, usually the crawl is Examining the configuration of individual’s territory, accompanied by weak drumming as if the lizard we considered as a registration point the location of a slightly pats the partner with forelimbs. Female crawl- conspecific of the same sex at the moment when it ing can be preceded or accompanied by a slight short underwent the direct (not return) nonritualized aggres- bite in the head or neck of the male. If A-behavior was sion of the territory owner. observed for both lizards, a majority of the contacts We were primarily interested in dyadic relation- ended in “lying in embrace” which can last for more ships. By a dyad we imply a territorial male and a than half an hour. During the embracing, , one lizard female that had at least one comfort zone within that lies on top of the other, head to head, head to tail, or male’s territory. In the present study, we used data on crosswise, usually the partners swap around from time to dyads that existed for a period from one and a half time. We also consider as “lying in embrace” a case when months to nine years, a total of 34 dyads. The dyads only the head of one individual lies on the back of the observed included 9 males and 22 females. other one, or lizards lying side to side and one or both We conducted the required calculations in Excel, individuals lays a head or foot on the partner’s back. and used common formulas and tables (Lakin, 1973; Sexual-orientation behavior (SO-behavior). It Sidorenko, 2001) for statistical criteria and determina- observed in males only. A male, bending his neck, tion of the confidence probability level. Datasets were touches the female’s neck, back and/or sacrum, usually small, and their distribution was unknown; and/or tail with the tip of his snout, licks her, sometimes because of that, we used nonparametric statistics and slightly grabbs the female’s back or neck with his jaws, criteria, in accordance, we preferred to use median during it he may crawls on the partner. Usually, the with lim in parenthesis when characterized a dataset. male’s upper part of body is visibly lifted by the legs.

BIOLOGY BULLETIN Vol. 43 No. 9 2016 SOCIAL RELATIONSHIPS BETWEEN MALES AND FEMALES 5

Table 1. The indices for rating of intersexual relationships Index Numerator (n)Denominator (N) Affiliativeness of male, female (Am, Af), Number of contacts during which All observed contacts frequency of female rejections (FR), a certain type of behavior was observed frequency of male’s SO-behavior (SO) Duration of lying in an embrace (ED) Number of registration points of male Number of registration points embracing a female of male in female’s comfort zones in her presence Male sexual activity (SA) Number of contacts during which All contacts observed during PC-stimulation was observed the mating period Roughness of PC-stimulation (RS) Number of cases of rough PC-stimulation All cases of PC-stimulation Sexual success of a male (SS) Number of copulations All cases of PC-stimulation Male’s attendance of female’s comfort Number of registration points for a male in a Total number of male’s registration zones (ZA) female’s comfort zone points The formula for calculation of an index: (n/N) × 100.

Sexual behavior. This is male behavior directly Seasonal Dynamics of Behavior associated with copulation: precopulatory stimulation We refer to the period from the first to the last reg- of a female (PC-stimulation) and copulation per se. istered coitus as the breeding period. The length of this Includes a capture the female with mouth, massaging period varied in different years and ranges from 12 to with jaws her sacrum area combined with scratching of 19 days. For five dyads we have sufficient data for the tail’s base with the forelimb, regrasping of the comparison of the frequencies of different forms of female by her thigh, insertion of the hemipenis, and behavior during the breeding and nonbreeding peri- coitus. We distinguish two forms of sexual behavior: ods. Pairwise comparison of the frequencies of differ- rough and gentle (Tsellarius, E.Yu. and Tsellarius, A.Yu., ent forms of behavior during the breeding and non- 2006). The female assumes a passive role in mating; no breeding periods demonstrates that the only trait with specific behavior devoted to achieving coitus was consistent variation between periods is sexual activity observed, except for arching the base of the tail of the male, which is always higher during the breeding upwards. season. Other differences in repertoire during breeding Spatial association. A female’s home range overlaps and nonbreeding periods are not significant (Fig. 3). the territories of two to three males. A female’s com- The differences in male’s attendance of a female’s fort zones are usually located on all of these territories comfort zone (ZA) and/or in duration of lying in an and rarely on just a single one of them. At the same embrace (ED) may sometimes be statistically signifi- time, home ranges of females widely overlap among cant; however, the actual value of these differences is themselves. Thus, on the territory of each male com- rather low (Fig. 3). We thought fit to ignore seasonal fort zones of several females are located (Fig. 2). changes in behavior while discussing relationships Within male’s territory a network of his patrol routes between members of the dyads. existed. These routes included all stable female com- fort zones (Tsellarius, A.Yu. and Tsellarius, E.Yu., 2005). All comfort zones of a territorial male are with Types of Social Relationships no exceptions located within the comfort zones of We consider an affiliativeness and degree of spatial females (Fig. 2); if the number and location of them association to be the main characteristics of social changed, so did the number and location of male com- relationships among the dyad members. There is a fort zones (Tsellarius, A.Yu. and Tsellarius, E.Yu., strong correlation between the affiliativeness of a male 2005). In most cases, comfort zones of males were (Am), of a female (Af), and the duration of lying in an located within comfort zones of only one female embrace (ED), rsp = 0.82 – 0.89 (P > 0.99 in all cases). (82.4%, home ranges of 9 males were observed, n = 51 Therefore, ED can serve as a measure of the affilia- HR х season). In general, males spent 39 to 62% of tiveness of dyad members. Male’s attendance of a their total time of activity within comfort zones of female’s comfort zone (ZA) can be considered as an females. Most intersexual interactions occur within indicator of spatial association. If we assign the values female comfort zones or in their immediate proximity. of ZA and ED to a coordinate system, it appears that We used some simple indices (Table 1) in order to relationships are divided by these attributes into the characterize relationships between a male and a three well-differentiated groups (Fig. 4a), and only female. relationships in the M11/20 + F5 dyad during 2001–

BIOLOGY BULLETIN Vol. 43 No. 9 2016 6 TSELLARIUS et al.

Year 1998

5 M2/6 0246 m 5 18/3

18/3

8/2 8/2 M11/20

M16 8/2 26 23 23 26 M4 N

23

S

123 4567

Fig. 2. Home range structure of M4 male and collocation of females and the male comfort zones in 1998: 1, M4 home range bor- ders; 2, territory of M4; 3, comfort zones of M4; 4, patrol routes of M4; 5, comfort zones of F12 (A-partner of M4); 6, comfort zones of other females (with individual numbers); 7, territories of neighboring males. Patrol route trajectories are denoted for the period of 12:00 to 15:00 hours on June 19.

2002 do not fit into any group. We will refer to the rela- Main Features of the Different Types tionships belonging to the top group as friendly (A-rela- of Social Relationships tions), those belonging to the middle group as neutral There are distinct differences between the groups (N-relations), and those belonging to the bottom by a number of other behavior traits besides ZA and group as rejecting (R-relations). The relationship type ED (Table 2). Main peculiarities of A-relations are in a dyad can change from year to year, with preva- follows: a high affiliativeness of a male and a female is lence of the progressive motion from lower values of present by all means; female readily interacts with a ZA and ED to higher values (Fig. 4b). male (low degree of rejection); a gentle type of

Table 2. Features of the lizard behavior in dyads with relationships of various types, and duration of these relationships Duration of dyad existence, Relationship type n1 + n2 + n3 HP and behavioral features АNR Duration of existence (seasons) 3 (2–8) 2 (1–6) 1 (1–4) 8 + 13 + 16 11.5 0.99 Male’s attendance of female’s com- 61 (49–78) 34 (14–46) 7 (0–15) 8 + 10 + 17 0.99 28.5 fort zones (ZA) Lying in an embrace (ED) 56 (44–77) 16 (4–29) 2 (0–13) 8 + 10 + 17 25.1 0.99 Affiliativeness of a male (Am) 53 (48–78) 29 (3–55) 7 (0–33) 8 + 10 + 17 19.7 0.99 Affiliativeness of a female (Af) 51 (38–70) 21 (0–33) 6 (0–21) 8 + 10 + 17 20.9 0.99 Female rejections (FR) 24 (16–39) 44 (15–78) 50 (32–91) 8 + 10 + 17 12.0 0.99 Male sexual activity (SA) 14 (0–33) 17 (0–27) 14 (0–36) 8 + 10 + 17 2.5 0.71 Roughness of PC-stimulation (RS) 14 (0–33) 54 (0–100) 50 (0–100) 7 + 9 + 13 7.9 0.98 Sexual success of a male (SS) 33 (20–50) 25 (0–67) 0 (0–50) 7 + 9 + 13 3.9 0.89

BIOLOGY BULLETIN Vol. 43 No. 9 2016 SOCIAL RELATIONSHIPS BETWEEN MALES AND FEMALES 7

60 M4 + F12 A-relationships M11/20 + F8/2 N-relationships 166 contacts 31 contacts 1997–1998 1997–1998 50

40 ϕ* = 1.50 P = 0.866 ϕ* = 2.20 30 P = 0.972 ϕ * = 2.24 χ2 = 2.77, P = 0.572 P = 0.973 20 χ2 = 4.62, P = 0.798 ϕ* = 2.21 P = 0.973 10

0 SB SO Am Af VZ LH SB SO Am Af VZ LH 40 M4 + F10, 44 contacts, 1997

30 R-relationships Mating period χ2 = 4.41, P = 0.780 Index value for behavior frequency (see Table 1) (see Table frequency behavior for value Index

Nonmating period 20 ϕ* = 1.64 P = 0.899 ϕ 10 * = 1.05 P = 0.706

0 SB SO Am Af VZ LH Behavior type (see Table 1)

Fig. 3. Frequency of various behavioral complexes during the breeding and nonbreeding period in some dyads (see Fig. 4 for rela- tionship types).

PC-stimulation is prevalent. In the case of R-rela- tion or continued to the end of the monitoring and tions, affiliativeness is low, a female generally tries to likely existed for some time after. Thus, we have to use avoid interactions with the male, the male practices not the real time of the duration but the period during mainly rough PC-stimulation, and his sexual success which dyads with A-relations were observed in the is rather lower. The P value of differences of male sex- interval between May of 1997 and the second half of ual success between all three groups of relationships July of 2006, i.e., the duration of the A-relations was does not reach the threshold of 0.95; however, it is inevitably underestimated in half of the cases. How- rather high (Table 2). In the paired comparison of A- and R-relations, the differences are significant (U = ever, even under such circumstances, the duration of A-relationships appeared to be the longest. 16.0, n1 + n2 = 7 + 13, P > 0.95) In addition, different types of relations differ in the Friendly relationships are likely to last for the duration of their existence. The duration of A-rela- whole life, until the death of one of the partners, while tions is the longest (Table 2). It should be noted, the N-relations have a high probability to transform into majority of R- and N-relationships were under obser- another type of relations (of which 46.2% into A-rela- vation from beginning to end. On the contrary, A-rela- tions, and 7.7% into R-relations). In the case of R-rela- tions in four cases (of the eight cases observed) were tions the most probable outcome is the female’s either established before the beginning of our observa- refusal to use the male’s territory (Table 3).

BIOLOGY BULLETIN Vol. 43 No. 9 2016 8 TSELLARIUS et al.

Table 3. Frequency (%) of different causes of terminations of relationships Relationship type Cause of termination χ2 P A (n = 5) N (n = 13) R (n = 16) Death of one of the partners 100.0 15.4 18.8 Female’s resettlement 0.0 30.8 75.0 24.0* 0.99 Transmutation into another type of relationship 0.0 53.8 6.3 * Calculated for the absolute values.

Table 4. Percent of individuals of different sex involved into females in the settlement (both permanently and tem- intersexual relations of a certain type porarily settled) always exceeded the number of terri- Relationship type torial males by 1.8–2.4 times in different years. Sex and statistics The portion of the individuals with A-relations is ANRhigher in males than in females (Table 4). At the same Males (n = 18) 72.2 77.8 100.0 time, the male usually maintained several N- and R-relations simultaneously, but only one A-relation, if Females (n = 21) 33.3 71.4 76.2 any. For females, there could be multiple relationships ϕ* 2.490.891.69of any type (Table 5). Altogether there observed 11 Р 0.99 0.36 0.99 groups with friendly relationships, eight of them (72.7%) were pairs (a male and a female) and three groups (27.3%) were triads (a female and two males). Number of Social Relations of Females and Males In most cases each individual was a member of sev- DISCUSSION eral dyads simultaneously; i.e., it had social relation- Affiliative behavior in Brauner’s lizards is a specific ships with several individuals of the opposite sex. The behavioral complex similar to the so-called “greeting total number of relationships per male was usually ceremony” of males and females of the rock agama higher than that of females, Me = 3.5(2–7) and 2.0(1–4), Laudakia caucasica (Panov and Zykova, 1999). This respectively (U = 79.5, n1 + n2 = 18 + 21, P > 0.99). It behavior includes physical contact and realized in was obviously due to the fact that number of settled intersexual interactions only without sexual, agonistic,

80 (a) (b) 70 M90/40 + F52/4 1998 1998 2001 60 rsp = 0.83 1999 2003 M16 + F12 50

A-relationships M11/20 + F8/2 1997 40 1997 M4 + F18/3

30 1997 N-relationships 1997 M11/20 + F131 20 2001 M2/6 + F5 M11/20 + F5 2001 10 2001 2001 R-relationships 1997–1998 M11/20 + F5 Visiting of female’s comfort zones by a male (VZ) zones by comfort Visiting of female’s 0 10 20 30 40 50 60 70 80 0 10 20 30 40 50 60 70 80 Duration of lying in a hug (LH)

Fig. 4. Types of social relationships between males and females, defined by the male’s attendance of female’s comfort zones and duration of “lying in an embrace” (a), and changes in relationships during the existence of dyads (b).

BIOLOGY BULLETIN Vol. 43 No. 9 2016 SOCIAL RELATIONSHIPS BETWEEN MALES AND FEMALES 9

Table 5. Percent of individuals of different sex involved into these clusters are polyandrous (a female and two multiple relations of a certain type males), while others are monogamous (a male and a Relationship type female). In general, it seems that the system work for Sex n1 + n2 + n3 HP the polyandrous state; however, there are certain fac- ANR tors impeding the development of friendly relation- ships. As a result, the majority of clusters remain Males 0.0 28.6 72.2 13 + 14 + 18 13.27 0.99 monogamous, and some do not form friendly Females 42.9 40.0 25.0 7 + 15 + 16 0.49 0.22 relations with individuals of the opposite sex at all. orientational, or hierarchical context. Mutual affilia- ACKNOWLEDGMENTS tiveness and lying in an embrace is the one and only nonsexual cooperative activity in Brauner’s lizard. If We thank A.V. Tchabovsky and A.S. Opaev for their we are to evaluate the strength of a dyad’s bond by the advice and comments on the manuscript. We are deeply relative duration of lying in an embrace and by the grateful to B.D. Vasilyev, I.S. Darevsky, E.N. Panov, male’s attendance of the places with strong possibility G.V. Polynova, and V.A. Cherlin for their participation of the female finding, we discover that both males and in discussion of the results of the data processing during females have evidently preferred partners in their various stages of the research and to N.B. Ananyeva, “harems.” Thus, on the one hand we find dyads with L.Y. Zykova, L.M. Mukhametov, Y.G. Menshikov, very high level of positive social intradyad integration and staff of the Utrish Biological Station, Russian (friendly relationships). On the other hand we observe Academy of Sciences, for help in the organization of the dyads, in which the integration degree is close to the fieldwork. Part of the equipment was courtesy pro- zero (rejecting relationships). The presence of an vided of N.B. Ananyeva (Zoological Institute, Russian intermediate group (neutral relationships) suggests Academy of Sciences), V.A. Cherlin (Biopreparat that the observed discrecity of relationship types in the JSC), the head of Binom LP, the late Y.I. Ivanov and studied lizard community may be random. It is possi- E.N. Romanova (Binom LP). ble that a whole range of transitions between rejecting This work was supported by the Russian Founda- and friendly relations exists. However, that does not tion for Basic Research (project nos. 01-04-63064, make these extreme types of relationships less real. 05-04-49468, and 15-04-03987) and in part by the In addition to a high degree of mutual affiliative- Russian Science Foundation (project no. 14-50- ness and spatial association, friendly relationships are 00029, section АААА-А16-116021660077-3). characterized by another feature: in the case of disap- pearance of a female partner, both the intensity of the REFERENCES male’s patrolling of his territory and the frequency of visits to the comfort zones of the disappeared female Auffenberg, W., Social and feeding behavior in Varanus increase (Tsellarius, A.Yu. abd Tsellarius, E.Yu., komodensis, in Behavior and Neurology of Lizards, Green- 2005). Similar behavior was also observed in monoga- berg, N. and McLean, P.D., Eds., National Inst. Mental mous pairs in the skinks Tiliqua (Bull, 1994). Attempts Health, USA, 1978, pp. 301–331. by male to follow the “chosen” female to an alien ter- Baskin, L.M., Povedenie kopytnykh zhivotnykh (Behavior of ritory are also significant (Tsellarius, A.Yu. and Tsel- Ungulates), Moscow: Nauka, 1976. larius, E.Yu., 2006). Such changes in behavior after a Bull, C.M., Population dynamics and pair fidelity in sleepy partner’s disappearance may suggest the existence of a lizards, in Lizard Ecology, Vitt, L.J. and Pianka, E.R., Eds., positive emotional bond between the partners (Klei- Princeton Univ. Press, 1994, pp. 159–174. mann, 1977; Sun et al., 2014). Bull, C.M., Monogamy in lizards, Behav. Proc., 2000, While only one friendly relationship per male was vol. 51, nos. 1–3, pp. 7–20. observed, some females maintained such relationships Carter, C.S., DeVries, A.C., and Getz, L.L., Physiological with two males simultaneously. It is possible that, substrates of mammalian monogamy: the prairie vole under specific circumstances, the number of such model, Neurosci. Biobehav. Rev., 1995, vol. 19, no. 2, interrelations per female may be even greater. In other pp. 303–314. words, friendly monogyny is typical for males, while Chapple, D.G., Ecology, life-history, and behavior in the females are inclined to polyandry. Participation in Australian scincid genus Egernia, with comments on the friendly partnership does not exclude the possibility of evolution of complex sociality in lizards, Herpetol. Monogr., each partner to maintain several relationships of other 2003, vol. 17, pp. 145–180. social types. Figuratively speaking, we are dealing with O’Connor, D.E. and Shine, R., Parental care protects a cloud of “dots” (individuals) interconnected by mul- against infanticide in the lizard Egernia saxatilis (Scinci- tiple unstable relationships of the R- or N-type. Rela- dae), Anim. Behav., 2004, vol. 68, no. 6, pp. 1361–1369. tively scarce, very stable clusters of “dots” inercon- Dodd, C.K., The effects of toe-clipping on sprint perfor- nected by friendly relationships stand out against this mance of the lizard Cnemidophorus sexlineatus, J. Herpetol., inconstant polygynoandrous network. About a third of 1993, vol. 27, no. 2, pp. 209–213.

BIOLOGY BULLETIN Vol. 43 No. 9 2016 10 TSELLARIUS et al.

Emlen, S.T. and Oring, L.W., Ecology, sexual selection, Plyusnin, Yu.M., Problema biosotsial’noi evolyutsii (The and the evolution of mating systems, Science, 1977, vol. 197, Problem of Biosocial Evolution), Novosibirsk: Nauka, no. 4300, pp. 215–223. 1990. Evans, L.T., Cuban field studies on territoriality of the liz- Power, D.M., Epigamic and reproductive behaviour of ard, Anolis sagrei, Comp. Psychol., 1937, vol. 25, no. 1, orange-chinned parakeets in captivity, Condor, 1967, pp. 97–125. vol. 67, no. 1, pp. 28–41. Evans, L.T., Field study of the social behavior of the black Rodda, G.H., Bock, B.C., Burghardt, G.M., and Rand, S.A., lizard, Ctenosaura pectinata, Am. Museum Novitiates, 1951, Techniques for identifying individual lizards at a distance no. 1493, pp. 1–26. reveal influences of handling, Copeia, 1988, no. 4, pp. 904– Gillette, J.R., Jaeger, R.G., and Peterson, M.G., Social 913. monogamy in a territorial salamander, Anim. Behav., 2000, Rose, B., Lizard home ranges: methology and functions, J. vol. 59, no. 6, pp. 1241–1250. Herpetol., 1982, vol. 16, no. 2, pp. 353–269. Gol’tsman, M.E., Social dominance and social stimula- Samuel, M.D. and Green, R.E., A revised test procedure tion: partial problems and common approaches, in Sistem- for identifying core areas within the home range, J. Anim. nye printsipy i etologicheskie podkhody v izuchenii populyatsii Ecol., 1988, vol. 57, no. 3, pp. 1067–1068. (System Principles and Ethological Approaches to the Schmidt, A.D., Zur Verbreitung, Biologie und Okologie Study of Populations), Pushchino: Nauka, 1984, pp. 108– von Heliobolus lugubris (Sauria, Lacertidae) im Sudlichen 143. Afrika, Salamandra. B, 1997, vol. 33, no. 4, pp. 269–288. Gowaty, P.A., Battles of the sexes and origins of monog- Sidorenko, E.V., Metody matematicheskoi obrabotki v psik- amy, in Partnerships in Birds, Oxford University Press, hologii (Methods of Mathematical Processing in Psychol- 1996, pp. 21–52. ogy), St. Petersburg: Rech’, 2001. How, T.L. and Bull, M.C., Reunion vigour: an experimen- Sun, P., Smith, A.S., Lei, K., Liu, Y., and Wang, Z., Break- tal test of the mate guarding hypothesis in the monogamous ing bonds in male prairie vole: long-term effects on emo- sleepy lizard (Tiliqua rugosa), J. Zool., 2002, vol. 257, pt. 3, tional and social behavior, physiology, and neurochemistry, pp. 333–338. Behav. Brain Res., 2014, vol. 265, pp. 22–31. Jennrich, R.J. and Turner, F.B., Measurement of non-cir- Tsellarius, A.Yu. and Tsellarius, E.Yu., The dynamics of the cular home ranges, J. Theor. Biol., 1969, vol. 22, no. 2, spatial structure of populations of Lacerta saxicola in decid- pp. 227–236. uous forests of the Navagir Ridge, Zool. Zh., 2001, vol. 80, Kleiman, D., Monogamy in mammals, Quart. Rev. Biol., no. 7, pp. 1–8. 1977, vol. 52, pp. 39–69. Tsellarius, A.Yu. and Tsellarius, E.Yu., Formation and pro- Lakin, G.F., Biometriya (Biometry), Moscow: Vysshaya tection of individual space in male rock lizards. 1. Individual Shkola, 1973. territory, Zool. Zh., 2005, vol. 84, no. 9, pp. 1123–1135. Tsellarius, A.Yu. and Tsellarius, E.Yu., Formation and pro- Leu, S.T., Bashford, J., Kappeler, P.M., and Bull, C.M., tection of individual space in male rock lizards. 2.Territory Association networks reveal social organization in the and territorial relations, Zool. Zh., 2006, vol. 85, no. 1, sleepy lizard, Anim. Behav., 2010, vol. 79, no. 1, pp. 217– pp. 73–83. 225. Tsellarius, A.Yu. and Tsellarius, E.Yu., Lifespan and mor- Madison, D.M., Activity rhythms and spacing, Spec. Publ. tality factors in the rock lizard Darevskia brauneri according Amer. Soc. Mammal, 1985, vol. 8, pp. 373–419. to long-term observations on the Navagir Ridge, Zool. Zh., Mathews, L.M., Territorial cooperation and social monog- 2009, vol. 88, no. 10, pp. 1276–1280. amy: factors affecting intersexual behaviours in pair-living Tsellarius, E.Yu. and Tsellarius, A.Yu., The use of space and snapping shrimp, Anim. Behav., 2002, vol. 63, no. 4, socio-sexual relationship in the rock lizard, Sovrem. Gerpe- pp. 767–777. tol., 2005, nos. 3/4, pp. 99–110. Morris, D., “Typical intensity” and its relation to the prob- Tsellarius, E.Yu. and Tsellarius, A.Yu., Changes in the lem of ritualisation, Behaviour, 1957, vol. 11, no. 1, pp. 1– behavioral repertoire in response to the individuals of oppo- 12. site sex in the rock lizard from the Navagir Ridge, in Mouton, P., Flemming, A.F., and Kanga, E.M., Grouping Aktual’nye problemy ekologii i evolyutsii v issledovaniyakh behaviour, tail-biting behaviour and sexual dimorphism in molodykh uchenykh (Actual Problems of Ecology and Evo- the armadillo lizard (Cordylus cataphractus) from South lution in the Research of Young Scientists), Moscow: Tovar. Africa, J. Zool., 1999, vol. 249, no. 1, pp. 1–10. Nauch. Izd. KMK, 2006, pp. 308–316. Panov, E.N., Povedenie zhivotnykh i ekologicheskaya struk- Ulrich, H.R. and Christophe, B., Monogamy: Mating Strat- tura populyatsii ( Behavior and Ecological Structure egies and Partnerships in Birds, Humans and Other Mam- of Populations), Moscow: Nauka, 1983. mals, Cambridge Univ. Press, 2003. Panov, E.N., The fates of comparative ethology, Zool. Zh., Wickler, W. and Seibt, U., Monogamy: an ambiguous con- 2005, vol. 84, no. 1, pp. 104–123. cept, in Mate Choice, Cambridge Univ. Press, 1983, pp. 33– Panov, E.N. and Zykova, L.Yu., Social behavior and com- 50. munication in Rock Agama Laudakia caucasica, Russ. J. Herpetol., 1999, vol. 6, no. 3, pp. 215–230. Translated by A. Lisenkova

BIOLOGY BULLETIN Vol. 43 No. 9 2016