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In: Recent Advances in Companion Animal Behavior Problems, K. A. Houpt (Ed.) Publisher: International Veterinary Information Service (www.ivis.

org), Ithaca, New York, USA.

Small Animal Maternal Behavior and its Aberrations ( 13-Jun-2000 )


K. A. Houpt
Animal Behavior Clinic, College of Veterinary Medicine, Cornell University, Ithaca, New York, USA. Components of Normal Maternal Behavior Licking and Nursing - The bitch in labor is not very responsive to her pups, but once the puppies have been delivered she begins licking them. She may extract the placenta by pulling on the umbilical cord. Like most litter-bearing, nesting-building mammals she ingests the afterbirth. Licking is the most obvious signs of maternal behavior and it serves three functions: 1) dries the puppies, 2) stimulates their respiration, and 3) guides them to the teats. For the first 14 days in kittens and 21 days in puppies, licking also serves to stimulate urination and defecation which does not occur spontaneously. During the first three days the bitch is in almost constant contact with the puppies, although nursing takes place during only half of that time. During the next two weeks contact times decreases markedly, but now the puppies suckle during a greater percent of the contact time. After the puppies eyes open and they are able to locomote contact time increases because they can follow the bitch [1]. Feline maternal behavior is similar to canine, but the queen licks even more, at first indiscriminately licking herself, the floor where birth fluids have spilled and the kittens [2]. For the first two days, the queen stays with the kittens most of the time taking "breaks" every two hours to stretch, eat and eliminate. Gradually these breaks become longer. On her return she will lick the kittens which arouses them to suckle. Nursing may occupy 70% of her time during the first week and then decreases. Between 20 and 30 days the queen approaches her kittens as frequently as they approach her, but after that the kittens do most of the approaching, indicating that weaning has begun [3]. Retrieving - Bitches usually retrieve the puppies not by picking them up, but by licking the pup's head. The pup will orient toward the bitch and in effect, follow her tongue. Queens are much more likely to pick up their kittens by the scruff of the neck and carry them, but if the owner tries to move the queen and kittens from the site of parturition, the queen may carry each kitten back to the original place with its amniotic fluid odors. Later the queen may spontaneously move the kittens to a new nest several times over the first few weeks after parturition. The tendency to move the kittens from one nest to another peaks during the third week [4]. A unique aspect of feline maternal behavior is that cats may nest together and communally nurse their kittens. This may explain why it is easier to cross-foster a neonate onto a queen than onto a bitch. Weaning - By two months most bitches have weaned their puppies, but some may do so much earlier. Queens may nurse their kittens less and less, especially after the first six weeks, but intermittent suckling may persist for months even when the kittens are eating solid food. Controls of Maternal Behavior Maternal behavior involves: a variety of hormones; experience as a mother; hereditary tendencies and the stimulus of the neonate. Genetic - Recently several genes have been identified as important in maternal behavior in mice. A null mutation of the prolactin receptor gene produces a defect in maternal behavior in mice as well as deficits in learning [5]. The Mest gene [6], has been identified as important in maternal behavior because deletion of the gene in mice resulted in lack of maternal behavior and lack of placentophagia, a normal component of maternal behavior in the mouse. The paternally imprinted Peg3 gene also causes aberrant maternal behavior in the daughters [7]. Deficiency of the normal estrogen receptor gene function led to poor mouse pup retrieval and cannibalism [8]. Examination of the canine and feline genomes and comparison of the genes of rejecting and non-rejecting dogs and cats might be worthwhile. Hormonal - The physiology of maternal behavior involves: Vaginal-cervical stimulation, as a result of the passage of the puppy through the birth canal, causes oxytocin release via spinal afferents with neural connections to the hypothalamus. The cells that produce oxytocin are located in the hypothalamus. These cells have axons that carry the hormone either to the

posterior pituitary, where it is released into the peripheral blood stream, or to other parts of the brain, including the olfactory bulb. In the olfactory bulb, oxytocin stimulates the release of monoamines which in turn initiates a sensitive period during which the bitch will identify the smell of the puppies as her own. The period during which a bitch will form a bond with a specific puppy is probably less than 24 hours. Apparently, a drop in estrogen and progesterone, an increase in oxytocin (and possibly prolactin), cervical stimulation and the presence of a small creature with a foreshortened face and wet with amniotic fluid are all factors involved in maternal behavior. Puppy or Kitten Characteristics - Puppies and kittens can stimulate all of the senses of their mothers and each of the senses seems to be involved in the induction of maternal behavior. Neonatal puppies and kittens, like most carnivores, are born very small in size relative to their dams. Compare the relative size of singleton foals or calves to their dams with that of each of a litter of puppies. Therefore, small size is an important visual signal. Neonates are furry and wet; the wetness is amniotic fluid, the taste and smell of which may be particularly important. The importance of amniotic fluid in maternal behavior and pup acceptance is illustrated by the experiments of Abitbol [9]. All pups were removed immediately at birth and return 1.5 hours later. All pups that had been washed clean of amniotic fluid were rejected; all those that had not been washed were accepted. A third group was washed, returned to their dam who rejected them, but after they had been wiped with amniotic fluid, she accepted them. Experiential - Puppy rejection usually occurs in primiparous bitches indicating that experience with being a mother at least once seems to be very important. Multiple rejection episodes are rare, possibly because owners do not breed a bitch a second time who has refused to nurse her puppies. Rejection of kittens is rare in either primiparous or multiparous queens. Occasionally rejection can escalate to cannibalism (see Maternal Cannibalism below). In some cases, the bitch eats the placenta and chews the umbilical cord, but she may keep on chewing up the cord and begin consuming the puppy. Cats are more likely to cannibalize an injured kitten than a neonatal one. Either bitches or queens may ignore a sick or abnormal neonate. This is probably because they do not have the correct peri-natal characteristics. They are not warm. They dont vocalize or move. It is unlikely that the mother makes a diagnosis and determines whether or not the neonate can survive before abandoning or cannibalizing it. Aberrant Maternal Behavior Insufficient Maternal Behavior - Lack of cervical stimulation. Caesarian section is frequently associated with rejection of puppies. In this case, the bitch was a Fila Brasileiro, a large, particularly aggressive breed of dog originating from Brazil. Following the surgery, the pups were introduced to the bitch in her cage in the Intensive Care Unit. She immediately killed a puppy. The owners took the remaining puppies and handled them before re-presenting them to the bitch who they had moved to their van. Apparently the combination of a more familiar place and the owner's scent was enough to inhibit aggression and allow the bitch to recognize the pups as her own. Maternal Cannibalism - A Persian cat was donated after she had killed her last two litters. She was three years old and had had four litters. The first two litters were raised normally, but she had killed all of her last two litters. She was suspected of killing two kittens of her mother's latest litter. On presentation, the cat was thin, flea infested and had dermatitis. She was fed ad libitum for three weeks before the birth of the kittens. She delivered six kittens and appeared to be cleaning and nursing them normally. Eight hours later she delivered a seventh, live kitten that she killed. She then began to consume its head. hereafter, she wore an Elizabethan collar to prevent her from reaching the kittens. She still allowed the kittens to suckle, but could not lick them so they were stimulated to eliminate with a cotton tipped applicator stick. The collar was removed periodically to allow her to groom herself. Once during this period she began to lick a kitten's head and then began to bite it. Although the kittens suckled and she produced some milk, the kittens failed to thrive and died over the course of 10 days despite some supplemental feeding. Postmortem examination of one kitten revealed that it was emaciated and undernourishment was the presumed cause of death. The cat was subsequently spayed and sold as a pet. Aggression - Some aggression by the bitch toward her puppies is normal, especially after the second week when they begin to initiate contact with her. Aggression can take the form of growling, snapping, catching the puppy's head in her mouth and shaking it or pouncing on it.A Labrador Retriever had shown normal maternal behavior with her first litter, but several years had passed before she was bred again. In the meantime, she had been living with several cats. The bitch objected to the cats walking over her and would growl until they left. When her second litter was born she licked them and allowed them to suckle, but if a puppy crawled over her, she would bite it. She killed several puppies before the owner intervened. In this case the solution was to muzzle the bitch so that she could not bite. Because a muzzle also prevented her from licking the puppies, the owner had to take the responsibility of stroking each puppys urogenital area in order to stimulate urination and defecation.

Hypocalcemia (lactation tetany) - should always be ruled out as a cause in cases of aggression in lactating bitches. The aggression is usually directed, not to the puppies but to other people and animals. The bitch will develop hyperthermia and tetany which can be relieved by calcium treatment and weaning of the puppies. Aberrant Retrieving - A Jack Russell Terrier was presented for carrying her pups from place to place rather than settling to nurse them. In this case the cause was probably not so much a failure of maternal behavior as interference with it. There were several other dogs in the household who had access to the bitch and her new litter. When confined to a room alone with her litter, the bitch showed normal maternal behavior. Excessive Maternal Behavior Hormonally Induced Retrieving and Nursing - The case involved a two-cat household. One cat had a litter of four kittens. Coincidentally, the second cat had just been spayed (within 24 h of the kittens birth). The second cat had been the socially dominant one in the household. When the kittens were born, the spayed cat lured them away. She would groom the kittens by licking them on the head until they would move from their mothers side to hers. She would allow them to suckle, but, of course, did not produce enough milk. Her teats were elongated and slightly hyperemic. The owners were concerned that the kittens would not receive enough nourishment. The solution was simple: the queen and her kittens were kept in a separate room to which the spayed female did not have access. Intraspecific Suckling Induced Maternal Behavior - The cat was a nulliparous, 10-month-old domestic shorthair that had been spayed 6 weeks before the onset of maternal behavior. A 6-week-old female domestic shorthair kitten had been introduced into the household. For the first week, the older cat hissed and swatted at the kitten. Then she ceased to show aggression and allowed the kitten to suckle. The owner reported that nursing was observed whenever she noticed the cat during the first month, then less frequently. Physical examination revealed that milk could be expressed from the mammary glands, which were larger than normal. Blood progesterone concentration was 0.03 ng/ml. Normal value for spayed cats is 0.03 ng/ml and for lactating queens is 0.3-2.5 ng/ml. This evaluation indicated that the cat did not have a functional reproductive tract and that inappropriate gonadal hormone concentrations were not responsible for the behavior or milk production [10]. Pseudopregnancy following ovariectomy in dogs has been suggested to be due to elevated prolactin caused by progesterone withdrawal. Whether a similar phenomenon occurred in this queen was not determined. Interspecific Suckling Induced Maternal Behavior - A particolor spayed female cocker spaniel allowed two Himalayan kittens to suckle when they were 6 weeks old. A year later, one of the Himalayans, now full grown, continued to suckle on the compliant cocker. Prolonged Kitten-Dependent Aggression - A domestic short haired cat had a litter of kittens and showed no aggression to the resident dog. When the kittens were 6 weeks old, visitors came with a strange dog. The queen attacked the strange dog, but then began to attack the family dog. If the owner tried to pull the cat off the dog, the cat would re-direct aggression to the owner. The cat was hospitalized and spayed. She showed no aggression toward dogs while she was hospitalized either before or after spaying. Meanwhile, her kittens had been put in a barn to live. Later, the mother cat was also placed in the same barn where she was aggressive to the kittens at first. Within a few days, she ceased being aggressive to the kittens, but would attack any dog that entered the building. Hormonally and Visually Induced Maternal Aggression - A 2-year-old, 11 kg (24 lb) female Cocker Spaniel dog, was evaluated because of aggression that began 4 days after ovariohysterectomy. In addition, the dog had a history of intermittent triggered episodes of aggression towards people. The dog underwent ovariohysterectomy and, 4 days after surgery, began nesting on the owners bed and guarding stuffed toys. The owner was bitten once trying to get the dog off the bed, and the dog growled at the owner whenever she approached the bed "nest" or any of the dogs stuffed animals. The owner was managing the problem by removing all of the offending toys from the house and keeping the dog in a crate outside the bedroom at night. This indicates the importance of the visual component of maternal behavior; without the puppy-like toys she no longer showed maternal aggression. Her mammary glands were enlarged and milk could be expressed. Presentation of her toys immediately stimulated aggressive guarding. The diagnosis was pseudocyesis [11,12]. Because of the maternal aggression, mibolerone (, 300 mcg, PO, q 24 h for 5 days) was prescribed. A follow-up telephone call was made to the owner 5 weeks after initial consultation. The owner reported that maternal aggression and other signs of pseudocyesis had completely resolved [13].

These cases indicate that there can be failure of maternal behavior if one or more of the genetic, hormonal or offspringrelated factors are missing. Conversely, maternal behavior can often be elicited by only one or two of those factors.

References
1. Rheingold HL. Maternal behavior in the dog. In: Rheingold HL, ed. Maternal Behavior In Mammals. New York: John Wiley & Sons, 1963; 169-202. 2. Deag JM, Manning A, Lawrence CE. Factors influencing the mother-kitten relationship. In: Turner DC, Bateson P, eds. The Domestic Cat: The Biology of Its Behaviour. Cambridge: Cambridge University Press, 1988; 23-39. 3. Schneirla TC, Rosenblatt JS, Tobach E. Maternal behavior in the cat. In: Rheingold HL, ed. Maternal Behavior in Mammals. New York: John Wiley & Sons, 1963; 122-168. 4. Feldman HN. Maternal care and differences in the use of nests in the domestic cat. Anim Behav 1993; 45:13-23. 5. Lucas BK, Ormandy CJ, Binart N, Bridges RS, Kelly PA. Null mutation of the prolactin receptor gene produces a defect in maternal behaviour. Endocrinology 1998; 139(10):4102-4107. - PubMed 6. LeFebvre L, Viville S, Barton SC, Ishino F, Keverne EB, Surani MA. Abnormal maternal behaviour and growth retardation associated with loss of the imprinted gene Mest. Nat Genet 1998; 20:163-169. - PubMed 7. Li L-L, Keverne EB, Aparicio SA, Ishino F, Barton SC, Surani MA. Regulation of maternal behavior and offspring growth by paternally expressed Peg3. Science 1999; 284:330-333. - PubMed 8. Ogawa S, Taylor JA, Lubahn DB, Korach KS, Pfaff DW. Reversal of sex roles in genetic female mice by disruption of estrogen receptor gene. Neuroendocrinol 1996; 64:467-470. - PubMed 9. Abitbol ML, Inglis SR. Role of amniotic fluid in newborn acceptance and bonding in canines. J Matern Fetal Med 1991; 6 (1):49-52. 10. Houpt KA, Concannon P, Collier K, Bryant N. Animal behavior case of the month. J Amer Vet Med Assoc 1993; 203 (1):58-59. 11. Okkens AC, Dieleman SJ, Kooistra HS, et al. Plasma concentrations of prolactin in overtly pseudopregnant Afghan hounds and the effect of metergoline. J Reprod Fert Suppl 1997; 51:295-301. 12. Voith VL. Functional significance of pseudocyesis. Mod Vet Pract 1980; 61:75-77. 13. Misner TL, Houpt KA. Animal Behavior Case of the Month. J Am Vet Med Assoc 1998; 213: 1260-1262. All rights reserved. This document is available on-line at www.ivis.org. Document No. A0805.0600.