Canine reproduction

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Canine reproduction is the process of sexual reproduction in domestic dogs.

Canine sexual anatomy and development[edit]

See below[where?] for a glossary of terms used in this article.

General[edit]

In domestic canines, sexual maturity (puberty) occurs between the ages of 6 to 12 months for both males and females, although this can be delayed until up to two years of age for some large breeds. Pregnancy is possible as soon as the first estrus cycle, but breeding is not recommended prior to the second cycle.[1] As with other domesticated species, domestication has selectively bred for higher libido, and earlier and more frequent breeding cycles in dogs than in their wild ancestors.

Male[edit]

Penis bone (os penis) of a dog. Arrow shows the urethral sulcus.
A young Cocker Spaniel, with an erect, ejaculating penis.
A male wolf in a defensive posture
Male repro system labelled.jpg

Like most male mammals, the development of secondary sexual characteristics in domestic dogs is dependent on the production of testosterone by the testes. Secondary sex characteristics include increased muscle mass, penile enlargement, anal hypertrophy, and development of a spherical swelling at the base of the dog's penis, called the bulbus glandis. Testosterone levels are also responsible for the sex drive of domestic dogs, which is not cyclical. Male dogs are receptive to mating at any time, even if the female is not in estrus.

Female[edit]

The anatomy of female dogs is similar to that of many other mammals. They have two ovaries located caudal to the kidneys in the abdominal cavity. They have a bicornuate (or two-horned) uterus which ends at the cervix, a short canal which connects to the vagina. The cervix is muscular with fibrous tissue support, and its opening closes in a stellate pattern. The vagina and urethra opens into the vestibule. The clitoris lies under the hood inside the vulva. The hood extends down and forms the outer boundaries of the vestibule as the labia minora. Females often have a vaginal stricture or hymen, which is a remnant of where the vagina and vestibule fused together during embryonic development. This structure is often asymptomatic and generally is not complete leaving an opening from the vagina to the vestibule. It is forced open further during mating.

In domesticated species one of the first and strongest effects seen from selective breeding is selection for cooperation with the breeding process as directed by humans. One of the behaviors noted is the abolition of the pair bond seen in wild canines. The ability of the female domestic dog to come into estrus at any time of the year and usually twice a year is also valued. The amount of time between cycles varies greatly among individual dogs, but a particular dog's cycle tends to be consistent through her life. Conversely, wild species generally experience estrus once a year, typically in late winter.

Most dogs come into season for the first time between 6 and 12 months, although some larger breeds delay until as late as 2 years. Like most mammals, the age that a female first comes into season has multifocal contributions of genetic, hormonal, dietary and nutritional, and behavioral signals to both physical and sexual maturation. gonadal sex steroids, growth hormone, insulin-like growth factor (IGF-1) and leptin constitute prime determinants of evolving body composition and the onset of puberty.[citation needed] The relationship between body fat and body mass correlates well with the onset of puberty in most mammals.[citation needed] They then experience estrus about every seven months until old age. Female dogs do not experience menopause, although their cycles will become irregular and fertility becomes unpredictable as they become older. Dogs over around 7 or 8 years are not usually considered appropriate for breeding, but can still remain fertile.

The reproductive cycle[edit]

Female cycle[edit]

A female dog's vulva in heat

The average length of the reproductive cycle for females is 2–4 weeks. Females reach sexual maturity (puberty) between 8 and 18 months of age. There is a tremendous variability in the maturation age between breeds, and even within a breed of dog.[2]

The first stage of the reproductive cycle is proestrus, in which eggs in the ovaries begin to mature and estrogen levels begin to rise. During this stage males are attracted to non-receptive females. Initially, the vulva lips will swell up and become pliable and there will be small amounts of bloody vaginal discharge along with signs of frequent urination and restlessness. Proestrus generally lasts 9 days.[2]

Estrus is the next stage, in which estrogen levels are high, mature eggs are released from ovaries, and the females mentally and physically become receptive to copulation. It is only during estrus that copulation will result in pregnancy.

During proestrus and estrus, females may have a clear to bloody discharge. This stage is also known as "heat." The length of these cycles varies greatly between individuals. Proestrus and estrus can last anywhere from 5 days to 21 days.[2]

Diestrus is the period following mating. Diestrus lasts approximately 56 to 58 days in a pregnant female, and 60 to 100 days in a non-pregnant female. During both of these periods, progesterone levels are high. Because the hormonal profile of a pregnant female and a female in diestrus are the same, sometimes a non-pregnant female will go through a period of pseudo-pregnancy. At that time she may gain weight, have mammary gland development, produce milk, and exhibit nesting behaviours.

Anestrus is the period of reproductive quiescence. The female has no attraction to or from the male. Anestrus generally lasts four to five months.[2]

Copulation[edit]

Dogs copulating on a beach

As with most tetrapods, canine copulation involves the male mounting the female from behind, a position informally referred to as "doggy style". When a male canine is interested in mounting a female, he will sniff the female's vulva. If the female is unreceptive, she may sit, lie down, snap, retreat, or otherwise be uncooperative. If the female is receptive, she will stand still and hold her tail to the side, a stance referred to as "flagging". The male will often continue examining the female's rear, before mounting her from behind while attempting penetration with his penis.

At the time of penetration, the canine penis is not erect, and only able to penetrate the female because it includes a narrow bone called the "baculum", a feature of most placental mammals. When the male achieves penetration, he will usually hold the female tighter and thrust deeply. It is during this time that the male's penis expands and it is important that the bulbus gland is sufficiently far inside for the female to be able to trap it. Unlike human sexual intercourse, where the male penis commonly becomes erect before entering the female, canine copulation involves the male first penetrating the female, after which swelling of the penis to erection occurs, which usually happens rapidly.[3]

Male canines are the only animals that have a locking bulbus glandis or "bulb", a spherical area of erectile tissue at the base of the penis. During copulation, and only after the male's penis is fully inside the female's vagina, the bulbus glandis becomes engorged with blood.[4] When the female's vagina subsequently contracts, the penis becomes locked inside the female.[5] This is known as "tying" or "knotting". While characteristic of mating in most canids, the copulatory tie has been reported to be absent[6] or very brief (less than one minute)[7] in the African Wild Dog, possibly due to the abundance of large predators in its environment.[8]

When the penis is locked into the vagina by the bulbus glandis (when the stud is "tied"), the urgency subsides[clarify] and the male will usually lift a leg and swing it over the female's back while turning around. The two stand with their hind ends touching and the penis locked inside the vagina while ejaculation occurs, decreasing leakage of semen from the vagina.[9][10][11] After some time, typically between 5 and 20 minutes[12] (but sometimes longer), the bulbus glandis disengorges, allowing the mates to separate. Virgin dogs can become quite distressed at finding themselves unable to separate during their first copulation, and may try to pull away or run. Dog breeders often suggest it is appropriate for handlers to attempt to calm the mating dogs if they show anxiety once this stage is reached.Similar mounting behavior, which may include pelvic thrusting,[13] is common to canines of both sexes. Mounting, with or without thrusting, should not be confused with "copulatory mounting", in which thrusting continues only until a "tie" is achieved. The familiar thrusting action is in reality simply the dog seeking the bitch's vulva with his penis. Many dogs and of course inexperienced domestic ones don't really know what they are trying to achieve and are simply acting on basic urges, and are often unsuccessful during many attempts. As soon as the penis does enter the vagina however, the dog feels an overwhelming drive to push in deeper as much as possible, and will often engage in a frantic climbing action with their hind legs, which they have to do because the swelling or erection of the penis takes place very quickly. Failure to do so often results in a slipped mating, which is not as reliable because not enough prostatic fluid passes from the male to support the sperm in the females utereus for long periods. As soon as the bulbus has swelled and the female has locked on to it, the dog becomes much more passive, and even sometimes apparently uninterested, despite the fact that a lot is going on out of sight. Thrusting becomes unnecessary, because the female muscles undergo contractions, which stimulate ejaculation of sperm, followed by prostatic fluid until the muscles eventually release, allowing the male to withdraw.[citation needed]

Gestation and litters[edit]

A pregnant mongrel
A wild dog from Sri Lanka nursing her four remaining puppies.

Gestation in a dog is 63 days in length, if measured from the day of ovulation. Since it is difficult to determine the exact date of ovulation, errors are often made in calculating gestation period.[14] Canine sperm can live for 10 to 11 days in the uterine tubes (fallopian tubes) so if a bitch is bred 10 days before the oocytes (eggs) can be fertilized, she will appear to have a gestation length of 70 days. If she is bred on the day the oocytes can be fertilized, her gestation length will appear to be 60 days long.

A general rule of thumb is that a mammal will produce half as many offspring as the number of teats on the mother. This rule is altered in domesticated animals since larger litters are often favoured for economic reasons and in dogs, particularly, the great range of sizes and shapes plays a role in how many healthy puppies a female can carry. A female dog usually has 10 teats/ nipples, though this does not means she can necessarily provide sufficient nutrition for 10 puppies in one litter.

An average litter consists of about five to six puppies, though this number may vary widely based on the breed of dog. Size of the breed is correlated with litter size. Miniature and small breeds average three to four puppies in each litter, with a maximum litter size of about 5-8. Large and giant breeds average 7 puppies per litter but can have a maximum litter size of about 15.[15] In one study, the Rhodesian Ridgeback had the highest average litter size with 8.9 pups per litter while the Pomeranian and Toy Poodle had the lowest with 2.4 pups per litter.[15]

The number of puppies also varies with the mother's age. In smaller breeds, both young and old age are associated with smaller litter size. In larger breeds, only old age is associated with smaller litter size.[15] Use of artificial insemination is also associated with smaller litter size, with frozen semen having a stronger effect than fresh semen.[15] The father's sperm count, the timing of the breeding, and many other factors may also affect litter size.[citation needed]

Some veterinarians say that mating a stud and bitch every other day is the way to a full litter.[citation needed] Others will say that mating every day is much better.[citation needed] This reduces the chance of having one puppy being born prematurely or much later than the other pups of the litter.

Some breeds have been developed to emphasize certain physical traits beyond the point at which they can safely bear litters on their own. For example, an English Bulldog has wide shoulders and narrow hips, thus the breed requires artificial insemination and, later, a cesarean section for giving birth.[citation needed]

Since a mother can provide nutrients and care to only a limited number of offspring, humans must assist in the care and feeding when the litter exceeds approximately eight puppies.[citation needed]

A large scale study in Norway showed that across all breeds, about 4% of pups will be stillborn and a further 4% will die within the first week (early neonatal mortality). Between 8 days and 8 weeks, 1% will die. Litter size, breed size and age of the bitch is associated with increased risk. High risk breeds for stillborn includes the Dogue de Bordeaux (14.2%), St. Bernard (12.3%), Chow Chow (12.1%), Pembroke Welsh Corgis (11.7%) and Dalmatian (10.6%). The Basenji, Italian Greyhound, Australian Terrier, Irish Soft Coated Wheaten Terrier and the Bichon Havanaise had few to no stillborns (0-0.6%). High risk breeds for early neonatal mortality includes the Rhodesian Ridgeback (11.6%), Dogue de Bordeaux (10.4% ), Dalmatians (8.8%) and Icelandic Sheepdog (8.7%) while the Basenji and Tibetan Terrier had no early neonatal mortality and the Border Terrier and Danish-Swedish Farmdog had <1% early neonatal mortality.[16]

Common causes of early neonatal mortality are bacteria infection, fetal asphyxia and fading puppy syndrome. Other causes may include elective euthanasia because of congenital defects or failure to meet breed standards.[16]

Other multi-breed studies have put stillborn rates at 6.5-7% and early neonatal mortality at 11.5-19.8%.[16]

Clinical issues[edit]

Female dogs are at risk for endometritis and pyometra in the postpartum period and after estrus or vaginitis. Signs and symptoms include fever, lethargy, loss of appetite, excessive thirst, restlessness, a foul smelling vaginal discharge which may or may not be bloody, infertility, or they may be asymptomatic.[17][18][19][20] Uterine infections should be treated expeditiously if suspected. Contrary to common belief, uterine infections can strike any intact bitch, whether she has been bred or not, and whether it is her first season or not although it is more common as dogs become older.

Dog breeding[edit]

Timing[edit]

Breeders and veterinarians have various methods for determining the best time to breed a dog. Breeders rely on both the visible signs of estrus and modern testing methods when they are trying to decide the best time to breed. Visible signs of estrus (or heat) include vaginal bleeding, vulvar swelling and the female dog responding to a male dog by standing and "freezing" to allow the male dog to mount her. The three most commonly used medical methods for determining estrus are: serum progesterone and Luteinizing hormone(LH) as well as a vaginal smear. The first two test for the level of those hormones in the blood, and a “smear” checks the amount of cornified epithelial cells present in the vaginal secretions.

Many breeders prefer the LH and progesterone tests because they are highly accurate while the smear method can be unreliable (especially when done by a vet who has limited experience performing this test). However the smear method is still widely used because it is much cheaper, and it's less stressful for the dog because no blood has to be drawn.

Before the advent of modern testing a breeder might mate the two dogs every two to three days during the female's estrus to ensure that fertilization had occurred. Today, most breeders will track a female's cycle (usually by progesterone blood tests) and breed her only during a 3-day window when she is most fertile and most receptive to the male.

These littermates were born to an Australian Shepherd mother who had roamed free, suggesting different fathers.

A female dog allowed to roam freely during estrus can end up producing puppies from multiple fathers. Breeders might occasionally breed a female to more than one desirable male for various reasons, in which case the only reliable way to determine parentage of the puppies is through DNA testing of the pups and mother. These litters are called 'dual sire' litters.

Procedure[edit]

Natural breeding can easily be accomplished between most dogs as long as the female dog is in an estrus during the attempt. Simply placing both dogs in the same environment for a few days will usually result in a pregnancy. If, due to breed characteristics or the stud only being available for a short time, natural breeding is not desirable, artificial insemination can be used. This is often done at a veterinarian's office.[citation needed] An artificial vagina is prepared, which is a conical thin latex sleeve ending in a sterile collection tube. The inside of the latex sleeve is lightly lubricated. The male is allowed to sniff a female in estrus. Experienced studs cooperate readily in the process. New studs often require encouragement in the form of manual stimulation.[21] Generally the male will mount the female, and the collector quickly directs the male's penis into the latex sleeve. The male ejaculates and the semen is collected in the tube. The semen is then drawn up into a long thin pipette.[4] The pipette is threaded through the female dog's cervix and the semen deposited in her uterus. There is ongoing research into techniques for chilling or freezing canine semen. Currently, for high quality breedings, one of the mates is often flown to the location of the other for this procedure.[citation needed]

Breeding[edit]

Purebred dog breeding arose in response to jobs for which a specific type of dog was needed, whether hunting, guarding, herding, or other work and were also bred simply for their physical attractiveness and appearance as well. Most of the work qualities no longer serve any useful purpose in current Western society. Different qualities were needed for these various jobs, such as a soft mouth for retrievers or a herding instinct for sheep dogs. To fix the genetic breed features so that two dogs of the same breed could reproduce themselves, most breeds have historically started with inbreeding. Those fixed qualities are today referred to as the breed standard. Standards are set and approved by each national breed club. Many standards are quite specific and not open to interpretation, such as height, ear type (prick versus drop), tail, coat, and other conformation features. Other aspects of each breed may be open to interpretation. Breeders may focus on conformation, temperament, or working qualities, such as hunting, pointing, herding, or rescue. Currently, the main goals for most breeders are to improve their chosen breed for show as well as producing puppies for sale as pets. Many commonly advertise their dogs on the internet, selling and shipping, often by plane, for pet and show purposes.

Professional breeders are not only aware of their breed standards, but some attempt to improve their own line by either linebreeding or by introducing new lines (outcrossing). Professional breeders may test for genetic defects before breeding for such things as hip dysplasia, various eye conditions, thyroid problems, and epilepsy.

Cross breeding[edit]

Designer breed dogs are Mixed-breed dogs that are intentionally bred from parents of two established breeds. Studies have shown that cross-bred dogs have a number of desirable reproductive traits. Scott and Fuller[22] found that cross-bred dogs were superior mothers compared to purebred mothers, producing more milk and giving better care. These advantages led to a decreased mortality in the offspring of cross-bred dogs; however, the qualities of cross bred dogs are not predictable. For example, F2 Labrador x poodles ("labradoodle") can inherit the coat of either a Labrador, a poodle, or a remix.

Spaying and neutering[edit]

Spaying (females) and castrating (males) refers to the sterilization of animals—usually by removal of the male's testicles or the female's ovaries and uterus—to eliminate the ability to procreate, and reduce sex drive. Castration has also been known to reduce aggression in male dogs, but spaying has been shown to occasionally increase aggression in female dogs.[23]

Animal control agencies in the United States and the ASPCA advise that dogs not intended for further breeding should be spayed or neutered so that they do not have undesired puppies.[24] Spaying and castrating can decrease the risk of hormone-driven diseases such as mammary cancer, as well as undesired hormone-driven behaviors. However, certain medical problems are more likely after neutering, such as urinary incontinence in females[25] and prostate cancer in males.[26] Some object to spaying and castrating as the sterilization could be carried out without the excision of organs. Spaying may also be done for ethnic or religious reasons, as male dogs sometimes mate with each other (anal sex) if not introduced to a female for an extended period of time.

Dogs shown in the conformation ring are not allowed to be either neutered or spayed. It disqualifies them from being shown as they must be intact and unaltered.

Female cats and dogs are seven times more likely to develop mammary tumors if they are not spayed before their first heat cycle.[27]

Studies[28][29][30][31] have shown that spaying or neutering is associated with serious health and behavioural consequences:

Altered Females:

Increased aggression can be shown in altered females if they have previously displayed aggression prior to surgical alteration .In a study by O’Farrell and Peachy, female dogs less than 11 months of age that had previously shown signs of aggression are more likely to have an increase in aggression after being spayed.[32] These increases in aggression may be due to the sudden change in hormone concentrations that are the result of alteration. While spaying female dogs does not “induce” aggression it can increase aggression (especially dominance aggression) and facilitates indiscriminate appetite in young altered females and can include them rapidly eating meals or eating food-associated items such as trash.[32][33] When females display dominance aggression it is often directed towards owners. Behaviors displayed include: guarding of toys, food, or resting places, a tense/rigid posture, erection of ears and tail, bearing of teeth, growling, and snapping or biting. These behaviors are usually an attempt to form some type of “dominance hierarchy” within the family. Some dogs may show selective dominance aggression towards one family member but not another.[32] Dominance aggression can sometimes be caused when an owner attempts to flip the pet into a submissive position (like on its back). Dominance aggression is also not limited to humans, canines exhibiting dominance aggression can also show this behavior toward other animals.

Altered males:

In nearly 2/3 of the cases that involve interdog aggression castration can help decrease aggression. Castration also decreases other male-typical behavioral traits such as mounting, roaming, and urine marking. Specifically, male puppies that are neutered between 7 and 10 weeks are three times less likely to display behavioral problems compared to canines neutered at 6 months or older.[34] Most dominantly aggressive dogs are male which causes many people to neuter their male canine companion. Removing testosterone can decrease the intensity of a canine’s reaction to stimulus. Testosterone does not cause a behavior to occur but its absence may decrease the occurrence of a “bad” behavior.[34]

See also[edit]

References[edit]

  1. ^ [1], Dr B Eilts, Louisiana State University School of Veterinary Medicine, "Normal Canine Reproduction" retrieved 10 April 2013
  2. ^ a b c d [2], Dr B Eilts, LSU Veterinary Medicine, "The Normal Canine Estrous Cycle" retrieved 10 April 2013.
  3. ^ Dan Rice (3 October 2008). The Complete Book of Dog Breeding. Barron's Educational Series. pp. 51–. ISBN 978-0-7641-3887-4. Retrieved 7 February 2013. 
  4. ^ a b "Semen Collection from Dogs". Arbl.cvmbs.colostate.edu. 2002-09-14. Retrieved 2012-01-29. 
  5. ^ Bekoff, M.; Diamond, J. (May 1976). "Precopulatory and Copulatory Behavior in Coyotes". Journal of Mammalogy (American Society of Mammalogists) 57 (2): 372–375. JSTOR 1379696. 
  6. ^ Kleiman, D. G. (1967). "Some aspects of social behavior in the Canidae". American Zoologist (American Society of Zoologists) 7 (2): 365–372. doi:10.1093/icb/7.2.365. Retrieved 2011-05-14. 
  7. ^ Creel, S. (1998-08-27), "Social organization and effective population size in carnivores", in Caro, T. M., Behavioral ecology and conservation biology, Oxford University Press, pp. 246–270, ISBN 978-0-19-510490-5 
  8. ^ Kleiman, D. G.; Eisenberg, J. F. (November 1973). "Comparisons of canid and felid social systems from an evolutionary perspective". Animal Behavior (Elsevier) 21 (4): 637–659. doi:10.1016/S0003-3472(73)80088-0. PMID 4798194. 
  9. ^ Social Behaviour In Animals
  10. ^ Biological Exuberance: Animal Homosexuality and Natural Diversity
  11. ^ The Illustrated Encyclopedia of North American Mammals
  12. ^ Ruvinsky, A.; Sampson, J. (2001). The genetics of the dog. CABI. pp. 564 (see p. 407). ISBN 978-0-85199-520-5. OCLC 45707635. 
  13. ^ Roger Abrantes. Dog Language. Dogwise Publishing. pp. 207–. ISBN 978-1-61781-045-9. Retrieved 6 May 2013. 
  14. ^ [3], Dr B Eilts, Louisiana State University Veterinary Medicine, "Canine Pregnancy" retrieved 10 April 2013.
  15. ^ a b c d Borge, K. S.; Tønnessen, R.; Nødtvedt, A.; Indrebø, A. (2011). "Litter size at birth in purebred dogs—A retrospective study of 224 breeds". Theriogenology 75 (5): 911–919. doi:10.1016/j.theriogenology.2010.10.034. PMID 21196028.  edit
  16. ^ a b c Tønnessen, R.; Borge, K. S.; Nødtvedt, A.; Indrebø, A. (2012). "Canine perinatal mortality: A cohort study of 224 breeds". Theriogenology 77 (9): 1788–1801. doi:10.1016/j.theriogenology.2011.12.023. PMID 22365700.  edit
  17. ^ Teunissen, G. H. (1952). "The development of endometritis in the dog and the effect of oestradiol and progesterone on the uterus". Acta endocrinologica 9 (4): 407–420. PMID 13007336.  edit
  18. ^ Okano, S.; Tagawa, M.; Takase, K. (1998). "Relationship of the blood endotoxin concentration and prognosis in dogs with pyometra". The Journal of veterinary medical science / the Japanese Society of Veterinary Science 60 (11): 1265–1267. doi:10.1292/jvms.60.1265. PMID 9853312.  edit]
  19. ^ "Pyometra - Dogs | Thickening of the Uterus". PetMD. Retrieved December 9, 2013. 
  20. ^ "Endometritis Symptoms and Treatment in Dogs". wikiPet. Retrieved December 9, 2013. [4]
  21. ^ Veterinary Medicine. Veterinary Medicine Publishing Company. 1989. Retrieved 9 February 2013. 
  22. ^ John Paul Scott, John L. Fuller. Dog Behavior. 
  23. ^ Heidenberger E, Unshelm J (1990). "[Changes in the behavior of dogs after castration]". Tierärztliche Praxis (in German) 18 (1): 69–75. PMID 2326799. 
  24. ^ "Top 10 reasons to spay or neuter your pet". American Society for Prevention of Cruelty to Animals. Retrieved 2013-12-09. 
  25. ^ Arnold S (1997). "[Urinary incontinence in castrated bitches. Part 1: Significance, clinical aspects and etiopathogenesis]". Schweiz. Arch. Tierheilkd. (in German) 139 (6): 271–6. PMID 9411733. 
  26. ^ Johnston SD, Kamolpatana K, Root-Kustritz MV, Johnston GR (2000). "Prostatic disorders in the dog". Anim. Reprod. Sci. 60-61: 405–15. doi:10.1016/S0378-4320(00)00101-9. PMID 10844211. 
  27. ^ Morrison, Wallace B. (1998). Cancer in Dogs and Cats (1st ed.). Williams and Wilkins. ISBN 0-683-06105-4. 
  28. ^ The Negative Aspects of Neutering
  29. ^ Golden retriever study suggests neutering affects dog health
  30. ^ Sanborn, Laura J. (May 14, 2007). "The Long Term Effects of Spay/Neuter in Dogs" (PDF). The NAIA Library. National Animal Interest Alliance. Retrieved December 9, 2013. 
  31. ^ Moore, G. E.; Guptill, L. F.; Ward, M. P.; Glickman, N. W.; Faunt, K. K.; Lewis, H. B.; Glickman, L. T. (2005). "Adverse events diagnosed within three days of vaccine administration in dogs". Journal of the American Veterinary Medical Association 227 (7): 1102–1108. doi:10.2460/javma.2005.227.1102. PMID 16220670.  edit
  32. ^ a b c Bonnie Beaver (1999). Canine Behavior: A Guide for Veterinarians. 
  33. ^ Peter Borchelt (1983). "Aggressive Behavior of dogs kept as companion animals: Classification and influence of sex, reproductive status and breed". Applied Animal Ethology 10 (1 & 2): 45–61. 
  34. ^ a b V. O'Farrel and E. Peachy (1990). "Behavioural effects of Ovariohysterectomy on Bitches". Small Animal Practice 31: 595–598. 
  • Siegal, Mordecai (1995). (editor), ed. UCDavis Book of Dogs. HarperCollins. ISBN 0-06-270136-3. 

Further reading[edit]

External links[edit]