Theriogenology 66 (2006) 1476–1481 www.journals.elsevierhealth.com/periodicals/the
Sexual characteristics of domestic queens kept in a natural equatorial photoperiod Ticiana Franco Pereira da Silva 1,*, Lu´cia Daniel Machado da Silva 2, Daniel Couto Uchoa 3, Cynthia Levi Baratta Monteiro, Lara de Aguiar Thomaz Laboratory of Carnivore Reproduction – Veterinary School/UECE, Paranjana Ave. 1700, Itaperi, Fortaleza-Ceara´ 60715-100, Brazil
Abstract The objective of this study was to describe the sexual characteristics of domestic queens kept under natural equatorial photoperiod conditions without mating. Estrous signs were detected in 25 pubertal queens by manual stimulation and by exposure to a tomcat twice daily for 6 months (January to June). The signs observed were tail deflection, spinal flexion, rubbing or rolling, vaginal discharge, vocalization, treading of the hind legs, body or tail tremor and rigidity, blow or scratches, and discomfort on manipulation. The queen was considered in estrous when neck grip, tail deflection and attempted penile intromission by the male were allowed after mounting. From 187 cycles, there were (mean S.E.M.) 7.5 0.7 cycles detected per queen; the duration of the cycle, estrus and non-acceptance were 18.1 0.9, 7.9 0.5, and 10.3 0.9 d, respectively. Queens always maintained some signs of sexual behaviour; they remained ambivalent for no more than 24 h at a time. It was noted that 85.3% of the observations of body or tail tremor and rigidity were made during estrus; therefore, these signs were considered characteristic of sexual receptivity. There was no evidence of prolonged anestrus or of a circannual pattern to estrus cyclicity. # 2006 Elsevier Inc. All rights reserved. Keywords: Domestic cat; Queen; Sexual behaviour; Photoperiod; Equator
1. Introduction The domestic queen is seasonally polyestrous; the seasonality is related to the duration of light (the cat is positively photoperiodic) [1–3]. The manipulation of day length has routinely been used to induce estrus [1– 3] or anestrus in the queen [4,5]. However, environ-
* Corresponding author. Tel.: +55 85 31019860; fax: +55 85 31019840. E-mail address:
[email protected] (T.F.P. da Silva). 1 T.F.P. Silva and C.L.B. Monteiro were supported by grant from FUNCAP. 2 L.D.M. Silva was supported by grant from CNPq. 3 D.C. Uchoa was supported by grant from CAPES. 0093-691X/$ – see front matter # 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.theriogenology.2006.02.008
mental factors, such as sensory stimulus and audiovisual and olfactory communication, seem to affect a queen’s behavior [3]. Furthermore, although sexual behavior of domestic cats is described through classical signs, differences have been reported between queens kept under temperate and equatorial conditions. With 12 h/d of natural light and without seasonal variations, queens seem to cycle continuously. Stages of the cycle of the queen include proestrus, estrus, interestrus, diestrus and anestrus [6,7]. Queens consecutively undergo proestrus, estrus and interestrus when kept in a positive photoperiod without mating and ovulation [6]. Proestrus is defined as a period of an increase in rubbing activity and a period when males are attracted to nonreceptive females. Estrus is the period of
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breeding, when the queen often vocalizes and assumes a position with elevated pelvis, tail deflection, and the hind limbs tread actively, especially in the presence of a tom [7,8]. Interestrus is the period between estrus without signs of sexual behavior when the queen is nonovulatory [6]. Experiments have been performed previously with cats kept under natural conditions or treated with hormones [5,9] to elucidate physiological sexual behavior in an equatorial photoperiod. During a further study, induction of anestrus was performed in a group of domestic queens by manipulating light. A study was conducted in the city of Fortaleza, Ceara´ State, Brazil; 45 domestic queens were kept in individual cages in intercommunicating boxes for 135 d. During this period, 34 (75.5%) queens did not show anestrus. We, therefore, suggested that sensory stimuli had a negative effect on induction of anestrus in the queens by manipulation of light (Mattos, unpublished data). Thus, a better understanding of the estrus cycle characteristics of domestic queens kept in a natural equatorial photoperiod is needed. The objective of this study was to describe the sexual characteristics of domestic cats (without mating) during a natural equatorial photoperiod. 2. Materials and methods 2.1. Experiment location The experiment was performed in the experimental cattery of the Carnivore Reproduction Laboratory of the State University of Ceara´, located in Fortaleza city (38440 South; 388340 West). This location has semi-humid equatorial weather, approximately 12 h of light per day, and mean monthly temperature, rain and relative humidity of 28.6 8C, 12.0 mm and 80%, respectively.
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2.3. Observation of sexual behavior Estrous signs in the 25 queens were detected by manual stimulation of the hindquarters performed by a trained observer, and by presenting queens to a tomcat, in the presence of the observer. Both procedures were performed twice daily for 6 months. For the first procedure, each queen was individually placed on a table and hindquarters were stimulated manually. The signs observed were: tail deflection, spinal flexion, rubbing or rolling, vaginal discharge, vocalization, treading of the hind legs, body or tail tremor and rigidity, and any striking out, clawing and scratching, or obvious discomfort on manipulation (grunting and escape attempt). For the second evaluation, queens were placed individually with a tomcat and were considered in estrus when they allowed neck grip, tail deflection and attempts at penile intromission after mounting; in all cases, the gloved hand of the observer prevented mating. The tomcats were used in a daily rotating system, i.e., one tomcat for all cats each day. A second tomcat was used in situations of ambiguous signs, or with the females that had been more likely to show estrous signs with that particular male. The estrus cycle was defined as the interval between: (1) first observation of acceptance of attempts at intromission (provided it was followed by acceptance(s) of subsequent attempts at intromission); and (2) a subsequent first observation of sexual behavior after a period of non-acceptance for 24 h. The duration of estrus was determined by the number of consecutive days of sexual intromission acceptance without refusal of acceptance for >24 h The interestrus period was defined as a period of consecutive days of nonacceptance starting 24 h after an initial period of non-acceptance. 2.4. Statistical analysis
2.2. Animals Twenty-nine domestic cats of mixed breed were used (four adult males and 25 adult females), mean body weight of 3 kg. The females had reached puberty and experienced pregnancy and parturition. The males displayed normal libido. The cats were vaccinated against commonly occurring feline viruses, kept in individual cages, fed with commercial dry food daily (Kitekat1/E´ffem1), and had free access to water. All females had continuous audiovisual and olfactory contact with the males in the same room. In addition, the females were placed in a common solarium with objects for distraction for at least 2 h/d.
The results were expressed as mean S.E.M. A Student’s t-test was used (P < 0.05) to compare the monthly mean number of observations. The number of times that each sign was observed in each phase of the estrus cycle was counted and compared among phases by x2 (and expressed as a percentage). For all analyses, P < 0.05 was considered significant. 3. Results A total of 362 observations were done for each female during the 6 months of the experiment. For all the females, no periods of absence of all sexual behavior
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Table 1 Mean (S.E.M.) cycle duration, estrus (acceptance of mating) periods and non-estrus (no acceptance of mating) periods in domestic queens kept under a natural equatorial photoperiod (n = 25) Queen
Cycle length (d)
No acceptance of mating (d)
Estrus (d)
Number of cycles
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25
15.8 0.6 (13.0–18.5) 32.3 4.20 (24.0–43.5) 15.4 0.7 (13.0–20.5) 22.9 7.6 (13.0–68.5) 15.4 1.1 (6.5–20.0) 13.7 1.2 (5.5–18.0) 27.80 7.88 (12.0–51.0) 13.4 2.7 (2.0–32.0) 59.8 3.3 (56.5–63.0) 13.75 0.64 (11.0–18.0) 18.5 2.4 (12.5–33.0) 14.2 1.7 (5.5–25.0) 21.2 3.5 (11.5–35.5) 14.8 0.4 (14.0–16.5) 23.2 8.2 (3.0–45.5) 10.8 1.9 (1.5–16.5) 41.8 10.5 (21.0–54.0) 14.7 0.7 (14.0–16.0) 23.0 3.7 (16.0–28.5) 17.5 6.3 (4.0–66.0) 14.4 3.2 (2.0–38.5) 42.3 12.7 (17.0–57.0) 16.9 6.9 (5.5–57.5) 13.27 0.59 (10.5–17.5) 26.8 10.6 (12.0–68.0)
6.9 0.8 (3.0–11.5) 29.0 4.4 (20.5–40.0) 6.2 0.9 (13.0–11.0) 16.0 8.1 (5–64.5) 8.2 0.7 (4.5–12.0) 7.3 0.6 (10.0–5.5) 21.40 7.58 (6.0–44.0) 9.2 2.2 (1.5–26.5) 56.0 3.0 (53.0–59.0) 5.83 0.63 (2.5–9.0) 4.7 0.8 (1.5–8.0) 8.5 1.3 (1.5–16.5) 16.7 3.5 (7.5–31.0) 10.1 0.5 (8.0–12.0) 21.4 7.7 (1.5–42.5) 2.9 0.4 (1.5–4.5) 15.2 13.7 (1.5–42.5) 5.5 1.2 (3.5–7.5) 17.7 3.8 (10.5–23.5) 9.6 5.2 (1.5–51.0) 5.0 1.2 (1.5–14.0) 35.0 11.6 (12.0–49.0) 11.4 6.4 (3.5–50.0) 6.46 0.8 (1.5–10.0) 3.5 0.6 (2.0–5.0)
9.0 0.4 (7.0–11.0) 3.3 0.4 (2.0–4.5) 9.2 0.5 (12.0–4.5) 6.9 0.6 (4.0–8.5) 7.2 0.7 (0.5–9.0) 6.3 0.8 (9.0–8.0) 6.40 1.40 (1.0–9.0) 4.3 0.8 (0.5–9.0) 3.8 0.3 (3.5–4.0) 7.92 0.29 (6.5–9.5) 13.8 2.1 (8.5–25.0) 5.8 0.8 (0.5–8.5) 4.5 2.6 (4.0–5.5) 4.8 0.4 (3.5–6.5) 1.9 0.7 (0.5–3.5) 8.8 1.45 (0.5–14) 26.7 11.4 (11.5–49.0) 9.2 0.7 (8.5–10.5) 5.3 0.2 (5.0–5.5) 7.9 1.9 (0.5–18.0) 9.5 2.8 (0.5–34.0) 7.3 1.2 (5.0–9.0) 5.5 1.0 (1.5–8.0) 6.80 0.54 (4.0–10.0) 23.3 10.3 (9.0–63.0)
10 5 10 7 11 9 5 13 2 12 9 10 6 6 5 10 3 3 3 9 11 3 7 13 5
18.7 0.9 (1.5–68.5)
10.3 0.9 (1.5–64.5)
7.9 0.5 (0.5–63.0)
Total
of more than 24 h were observed. The only defining characteristic for cycle phases was acceptance or refusal of mating. Based on analysis of behavior, it was not possible to identify an interestrus (no sexual behavior), or to distinguish it from a proestrus period. During the study period, 187 complete cycles were observed (average, 7.5 0.7 cycles per queen). The duration of the cycle was of 18.1 0.9 d (range, 1.5– 68.5), the duration of estrus was 7.9 0.5 d (range, 0.5– 63.0) and the duration of no acceptance of mating was 10.3 0.9 d (range, 1.5–64.5; Table 1). Although some cats had from 9 to 13 cycles in 6 months (1.5–2.2 cycles/ month), in others the prolongation of one of the two phases led to a considerable reduction in the number of cycles/month (0.3 and 0.5 cycles/month). Queens showed no male acceptance in 32/362 observations and male acceptance in 132/362 observations. Instances of periods of refusal of intromission acceptance (not longer than 24 h) but with maintenance of other signs of sexual behavior within an estrus phase, were observed in 41% of the cycles. In only three queens (12% of the cats) was there an absence of such discontinuity in any of the estrus signs.
7.5 0.7 (2–13)
The incidences of several of the potential signs of receptivity (Table 2) differed (P < 0.05) between periods with without acceptance of intromission. Tail deflection, spinal flexion and treading the hind legs were Table 2 Incidence (% of observations) of specific signs of sexual behavior during periods without acceptance of mating vs. with acceptance of mating in domestic queens kept under a natural equatorial photoperiod (n = 25) Sign
Tail deflection Treading the hind legs Spinal flexion Vaginal discharge Rubbing or rolling Vocalization Discomfort on manipulation Blow or scratches Body or tail tremor and rigidity
Period No acceptance of mating
Acceptance of mating
63.5 57.3 60.1 45.9 29.4 26.9 94.4 89.5 14.7
36.5 42.7 39.9 54.1 70.6 73.1 5.6 10.5 85.3
For each sign, there was a difference (P < 0.05) between the two columns.
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Fig. 1. Daily number of domestic cats in estrus without mating (n = 25).
seen significantly more frequently when mating was not accepted. It was noted that 85.3% of the observations of body or tail tremor and rigidity were done in estrus; together with rolling and vocalization, these signs were considered the main indicators of sexual receptivity. The presence of vaginal secretion in cats during proestrus and estrus was observed (54.1%). Vaginal secretions were mostly characterized by a scant, transparent vaginal discharge. In our study, vaginal discharge was a discreet transparent fluid, but in some queens, an abundance of viscous transparent discharge was observed. Discomfort during manipulation and blows or scratches were characteristic signs for the absence of sexual receptivity (Table 2). Audiovisual and olfactory signs presented by the females in estrus might have been the most relevant effect on social behavior. The distribution of estrus occurrence is shown in Fig. 1. There was at least one female in estrus on each day of observation, but never more than 18 cats (72%) at one time. The number of cats in estrus differed among months, with more cats in estrus in March, than in April, June and February. In January and May, fewer (P < 0.05) queens were in estrus (Table 3).
Table 3 Mean (S.E.M.) number and percentage in estrus (accepting intromission attempts) on each observation day (according to month of observation) of domestic queens under a natural equatorial photoperiod (n = 25) Month January February March April May June a–c
Number of cats 6.9 0.42 9.4 0.5 b 13.3 0.4 c 10.9 0.7 b 7.2 0.6 a 10.7 0.5 b
a
Percentage 27.6 37.4 53.0 43.6 28.8 42.8
Within the column, entries without a common superscript differ (P < 0.05).
4. Discussion The presence of positive signs of sexual behavior in interestrus is possible [10]. However, in the present study, since hormonal concentrations were not measured, we were unable to determine the effects of hormone concentrations on sexual behavior. Estradiol, even in low concentrations, could account for the continuity of sexual manifestation in the present study [10]. Furthermore, cats in the present experiment were conditioned to a certain behavioral response when touched in the perineal area and thus may have displayed those responses independent of hormonal status. There was considerable variation in cycle lengths both among and within queens. The mean duration of the cycle was in agreement with the literature [11]. Cycles with a long duration were caused by a long phase of non-acceptance, along with some signs of sexual behavior, or by a long phase of acceptance behavior; the former could be due to a luteal phase following an induced or spontaneous ovulation [12], considering that the length of these intervals often approached the duration of the non-pregnant diestrus [13]. During another study, five queens presented ovulatory cycles, and even under the influence of progesterone, continued to exhibit some sexual behavior [14]. Since our queens were in permanent sensory contact with active males and females, ovulations might therefore have been more easily induced, especially with daily manipulation of the perineal area. The measurement of hormonal concentrations would be helpful to confirm ovulations and luteal phases. Long cycles could have also been due to anestrus. However, in anestrus, no signs of sexual behavior were present [10]. In the present study, the duration of estrus averaged 7.9 d, which seemed slightly longer than the mean duration of 5 d for queens with non-ovulatory cycles in
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another study [13]. Although a minimum duration of 2 d has been described [13], in the present study, acceptance was as short as 0.5 d, which can be explained by deviations of sexual receptivity that have been described previously [13]. Behavioral deviations may be linked to manipulation and associated stress, since experiments, such as the present one, completely modify the environment and the behavioral reaction of the animals [15]. On the other hand, an exceptionally long estrus (up to 63 d in our study) seems to be false nymphomania, probably due to overlap of consecutive follicular waves [1,16]. Regarding cycle frequency, our 18-d mean interestrus interval (with 12 h natural light/d) was consistent with the 2 cycles/month reported for 14 h of artificial light per day [1]. Tail deflection, spinal flexion, treading the hind legs, vocalization and rolling are considered classical signs of sexual behavior in queens. Additionally, the presence of vaginal secretion during estrus was observed. Although the presence of vaginal discharge in domestic cats differs among reports [5,6,14], vaginal discharge was described as a sign of estrus in cats in a previous study [5]. The body or tail tremor and rigidity observed as indicators of receptivity in the present study have not been previously described and should be considered relevant when evaluating sexual behavior in queens, especially when no male is present to detect estrus. As the end of the estrus approached, some queens began to show signs of refusal, even if they were still accepting the male. Other signs, such as urine spraying, head shaking and sniffing previously described in domestic and wild female cats during estrus [17,18], were not observed during the present study. Our observations regarding signs of sexual behavior may be useful to determine sexual receptivity and perhaps the optimal time of mating. However, our observations might have been influenced by sensory effects initiated by pheromones, audiovisual signals, and genital manipulation and therefore would not necessarily be consistent with those in isolated, nonexperimental animals. The male effect was reported to be perceptible when there is an introduction of an active male in a colony of isolated queens [3]. However, to minimize this effect in the present study, all queens were in contact with the males before and during the study. Therefore, any male effect was not the result of a novel introduction. In conclusion, domestic queens kept under a natural equatorial photoperiod in a semi-humid equatorial climate continuously exhibited some signs of sexual behavior, even when they were not accepting a male, with no evidence of an anestrus period. In addition,
body and tail tremor and rigidity were important indicators of estrus. Although the incidence of estrus varied among months, there was no suggestion of a circannual change in cyclicity during the 6-month duration of the study. Further investigations are needed to determine if temperature, humidity and rain, or other sensory stimuli, exert an effect on the number of cats in estrus. Acknowledgements The authors thank CNPq that supported part of this research, EFFE´M1 of Brazil that supplied part of the dry food, FUNCEME for the climatic data, and Fortaleza Zoonoses Control Central for the anti-rabies vaccines provided for the cats. References [1] Leyva H, Madley T, Stabenfeldt GH. Effect of light manipulation on ovarian activity and melatonin and prolactin secretion in the domestic cat. J Reprod Fertil Suppl 1989;39:125–33. [2] Leyva H, Madley T, Stabenfeldt GH. Effect of melatonin on photoperiod responses, ovarian secrection of oestrogen, and coital responses in the domestic cat. J Reprod Fertil Suppl 1989;39:135–42. [3] Michel C. Induction of oestrus in cats by photoperiodic manipulations and social stimuli. Lab Anim 1993;27:278–80. [4] Mattos MRF, Silva TFP, Pereira BS, Uchoa DC, Cardoso RCS, Silva AR, et al. Embryo transfer in the cat: first successful in Latin Ame´rica. In: II Congresso Internacional De Medicina Felina – Cimfel; 2001. abstract. [5] Silva TFP, Mattos MRF, Silva AR, Cardoso RCS, Pereira BS, Uchoa DC, et al. Sexual behaviour and ovarian response after FSHp superovulation treatment in queens (Felis catus). Rev Bras Rep Anim 2001;3(25):375–7. [6] Verstegen JP. Physiology and endocrinology of reproduction in female cats. In: Simpson G, England G, Harvey M, editors. Manual of small animal reproduction and neonatology. Chelteham: British Small Animal Veterinary Association; 1998 . p. 11–6. [7] Feldman EC, Nelson RW. Breeding, pregnancy and parturition. In: Feldman EC, Nelson RW, editors. Canine and feline endocrinology and reproduction. Philadelphia: Saunders Company; 1996. p. 547–71. [8] Banks R. Physiology and endocrinology of the feline estrous cycle. In: Morrow DA, editor. Current therapy in theriogenology. Philadelphia: W.B. Saunders; 1986. p. 795–800. [9] Aguiar L, Madeira VHL, Silva Jr FX, Silva FMO, Monteiro CLB, Silva TFP, et al. Retorno ao estro apo´s tratamento com gonadotrofina corioˆnica equ¨ina em gatos dome´sticos (Felis catus). In: XI Encontro de Iniciac¸a˜o Cientı´fica e VII Semana Universita´ria da UECE; 2002. abstract. [10] Corrada YA, Gobello MC. Reproduccio´n felina: caracterı´sticas del gato dome´stico Buenos Aires: Asociacio´n Argentina de Medicina Felina; 2000. [11] Graham LH, Swanson WF, Brown JL. Chorionic gonadotropin administration in domestic cats causes an abnormal endocrine
T.F.P. da Silva et al. / Theriogenology 66 (2006) 1476–1481 environment that disrupts oviductal embryo transport. Theriogenology 2000;54:1117–31. [12] Lawler DF, Johnston SD, Hegstad RL, Keltner DG, Owens SF. Ovulation without cervical stimulation in domestic cats. J Reprod Fertil Suppl 1993;47:57–61. [13] Root MV, Johnston SD, Olson PN. Estrus length, pregnancy rate, gestation and parturition lengths, litter size, and juvenile mortality in the domestic cat. J Am Anim Hosp Assoc 1995; 31:429–33. [14] Tsutsui T, Stabenfeldt. Biology of ovarian cycles, pregnancy and pseudopregnancy in the domestic cat. J Reprod Fertil Suppl 1993;47:29–35.
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[15] Minovich FG. Aspectos clı´nicos y terapia de las enfermedades reproductivas en las gatas. In: III Congresso Internacional de Medicina Felina; 2003.p. 1–9. [16] Minovich FG. Cuidados y complicaciones de la gestacion y parto. In: III Congresso Internacional de Medicina Felina; 2003. p. 1–7. [17] Palen GF, Goddard GV. Catnip and oestrous behaviour in the cat. Anim Behav 1966;14:372–7. [18] Moreira N, Monteiro-Filho ELA, Moraes W, Swanson WF, Graham LH, Pasquali OL, et al. Reproductive steroid hormones and ovarian activity in felids of the Leopardus genus. Zoo Biol 2001;20:103–16.
