Widget deposits a new scent mark on a brick. The bricks carry prior marks by two other male rats.
|
|
|
Widget deposits a new scent mark on a brick. The bricks carry prior marks by two other male rats. |
Urine marking -- the deposit of small drops or smears of urine on the ground, objects, and other rats -- is a form of chemical communication. One rat generates the chemical signal (a drop of urine), and another rat identifies, integrates, and responds to that signal either behaviorally or physiologically.
Urine contains a lot of information about the rat who produced it: its species, sex, age, reproductive status, sexual availability, social status, individual identity, and current stress level, as well as the age of the scent mark itself.
Both males and females urine-mark, but marking is sexually dimorphic: males mark more than females. In addition, adults mark more than juveniles, and intact rats mark more than neutered rats. Female marking tends to follow the female's 4-5 day reproductive cyclical: females mark most the night before they ovulate.
Rats urine-mark their environment, particularly objects they can readily walk upon. They mark other rats as well, and they mark over novel odors and the urine of other rats.
Urine marking is influenced by hormones. Female marking is the greatest the day before she ovulates (proestrus) and correlates with the increase in estrogen and progesterone associated with proestrus. Male marking is correlated with testosterone. Male marking increases at puberty, and is greatly reduced or eliminated by castration.
Marking is elicited by cues in the environment: by the presence of low objects in a familiar area, or objects that were moved to another location, and by the odors of other rats.
Urine marking serves several functions. It acts as a sexual attractant and advertisement to rats of the opposite sex. Males urine mark frequently, especially when they can smell receptive females. Females prefer the urine of males with high testosterone levels. Females urine mark less than males, but tend to do so on the night before they come into heat, possibly advertising their sexual availability to nearby males. Intact males prefer the odor of receptive to non-receptive females.
Urine marking may also serve as a habitat labeling system. Rats may urine mark their environment in order to maintain an optimum odor field, which may help them maintain a sense of familiarity with their area. It may be a response to novelty. Urine marking of the environment may be serve as an index of spatial knowledge.
The evidence on whether urine marking has a territorial defense function is mixed. While some studies have found that rat urine deters other rats, which would support a territorial function hypothesis, others have found that rat urine attracts other rats, which would not support this hypothesis.
Rats may mark each other for a variety of reasons, which vary with the sex, age, and hormonal status of the marker and the recipient. Females who are not yet in heat may urine mark preferred males, which may help her select a preferred mate a few days later when she comes into heat. Males mark more than females, and their marking declines after castration. Dominant males mark more than subordinates. Subordinates mark other subordinates and dominant rats differentially: they deposit more urine in fewer passes on dominant rats. Juvenile males mark adult males a great deal, but this declines as they enter puberty. Female adults and juveniles mark each other at low, steady rates.
Urine marking in rats refers to the deposit of drops or smears of urine in the environment, sometimes accompanied by secretions from preputial sebaceous glands (Birke 1978). The rat leaves these drops on surfaces, objects and other rats as it passes, by rubbing its anogenital area over the top of an object (called an anogenital drag), or by lifting a hind leg over the top of an object while walking beside it, leaving a small trail of urine along its length (called a leg lift) (Brown 1975). Rats deposit urine on each other via the crawl-over response (Grant 1963).
The urine marking position in male rats is quite subtle. It consists of a slight arching of the back, which places the penis lower and slightly forward of its position during normal walking. The rat may pause momentarily as he deposits a small quantity of urine (Price 1975).
Urine marking is a type of scent marking, a form of chemical communication, in which one rat, the sender, generates a chemical signal (the drop of urine) and transmits the signal by depositing the drop in the environment. Another rat, the receiver, identifies, integrates and responds (either behaviorally or physiologically) to the signal. It is assumed that the sender-receiver relationship is the result of natural selection, such that the sender's signal produces a response in the receiver that benefits the sender in some way (e.g. the signal attracts a mate for the sender etc.), while the receiver assesses the signal and responds in a way that most benefits the receiver (see Agosta 1992, Bradbury and Vehrencamp 1998, and Eisenberg and Kleiman 1972 for more on chemical communication).
Urine marking is very common in mammals, and it has become adapted for use in a variety of contexts and may have more than one function in any given species. In addition, it may have different functions in different species (Johnson 1973).
Chemical secretions contain an enormous amount of information (Agosta 1992). A rat who smells a urine mark can determine all sorts of things about the rat that produced it: its species, sex (Brown 1977), age (juvenile vs. adult), reproductive status (Carr and Caul 1962), familiarity (Krames and Shaw 1973), social status (Krames et al. 1969), individual identity (Brown 1988, Carr et al. 1970), and current stress level (Mackay-Sim 1980, Giesecke 1997, Valenta and Rigby 1968). In addition, rats can tell how long in the past a urine mark was deposited.
Adult rats of both sexes urine mark. Adult rats mark more than juveniles, intact adult rats mark more than neutered adult rats (Brown 1977).
Urine marking is sexually dimorphic: there are sex differences in (1) the quantity of urine marking: males mark much more than females as a general rule; and (2) in the pattern of urine marking: males urine mark all the time but do it more when they can smell a receptive female nearby. Female marking is cyclical, tracking her 4-day ovulatory cycle: females mark most on the night before estrus (Birke, 1978; Calhoun 1962, p. 151).
|
|
|
Rats deposit scent marks on objects they can easily walk on, such as these bricks. The dark stains, most easily seen on the top brick, are urine marks. |
Rats may preferentially urine mark on top of the marks of other rats (called overmarking), especially the the marks of the opposite sex: intact males prefer to overmark the odors of estrus females (Brown 1973, 1977, 1978), while intact females prefer to overmark the odors of intact males (Brown 1977). Rats tend not to overmark their own urine (Brown 1973, 1975).
Rats urine mark over preferred foods. These urine marks attract other rats to that food source -- this is one way that food preferences are culturally transmitted between rats (Galef and Beck 1985).
Rats also deposit small drops of urine on each other. This is called conspecific urine marking (conspecific means "same species"), and it occurs when one rat crawls over another and deposits "a drop or two of urine, leaving a wet patch on the fur of the other rat" (Grant 1963). Little research has been done on conspecific marking. It may be a form of social communication, but its function is still being discovered (Taylor et al. 1984, 1987).
Rat urine fluoresces under ultraviolet light, so it can be seen
with a black light.
Hormonal and neural control
Females: The rate of urine marking tracks the 4-5 day ovulatory cycle and is influenced by hormones. Female urine marking is highest during proestrus (Calhoun 1962, Matochik et al. 1992), and lowest or absent during diestrus (Birke 1978, Matochik et al. 1992). The increase in marking during proestrus is caused by a rise in estrogen followed by a surge of progesterone (Birke 1984). Urine marking can be eliminated by removal of the ovaries (Brown 1977).
Males: Male urine marking is associated with testosterone: urine marking increases greatly at puberty when the testes start secreting testosterone. Castration greatly reduces urine marking. Price (1975) found that castration reduced marking from 18 marks per 24 hours before castration to 4 marks after castration. Similarly, Taylor et al. (1987) found that castration reduced environmental urine marking to about 20% of pre-castration levels. Urine marking is restored in castrated rats by injections of testosterone (Taylor et al. 1987, Brown 1978, Price 1975)
The male also needs the peripheral nerves of the genitourinary system that control urine marking: the viscerocutaneous (Vc) branch of the pelvic nerve is in charge of voiding the bladder, while the hypogastric nerve (Hg) is involved in continence (Manzo et al 2002).
|
Does castration reduce urine marking? Yes. Males who have been castrated tend to mark less after castration than they did before. Castration does not eliminate urine marking entirely, but reduces it to about 20-22% of pre-castration levels (Price 1975, Taylor et al. 1987). |
Environmental cues
Males are sensitive to environmental cues. Males mark at low levels all the time, but when they can smell a receptive female nearby their urine marking increases. The olfactory cues from the female trigger an increase in urine marking in males. This increase in urine marking in response to the urine of a receptive female can be countered by castration (Manzo et al. 2002). Rats of both sexes increase their urine marking when they smell other rats (Birke and Sadler 1984), and novel odors in general (Hopp and Timberlake 1983).
Urine marking increases with the presence of low objects in a familiar environment (Peden and Timberlake 1990). Rats of both sexes prefer to mark surfaces and objects that are easy to walk on (Birke 1978, Brown 1973, Hopp and Timberlake 1983). They may also re-mark objects that have been moved (Harley et al. 2001).
Rat urine marks are a form of chemical communication, in which one animal produces a chemical signal that contains information and may change the behavior or physiology of a receiver. Urine marking has become adapted for use in a variety of contexts, and it has a variety of functions. These functions need not be mutually exclusive.
Male urine marks: Male urine marks advertise information about the male (e.g. his testosterone levels, which vary a great deal between males), and urine marking increases when males can smell females in heat nearby (Manzo et al. 2002). Doty (1974) hypothesizes that the female uses male urine to select her mate from among the advertisers.
Female's response to male urine marks: Intact females display great interest in male urine by sniffing and licking it (McIntosh et al. 1979) and marking over it (Brown 1977). Intact females prefer the urine of males with high testosterone levels (Brown 1977, Taylor et al. 1982, but see Birke and Sadler 1983). In addition, females prefer to interact with sexually experienced males (Gilman and Westbrook 1978), who have heavier testes and higher levels of testosterone than sexually naive adult males (Kamel et al. 1975). Ovariectomized females show no preference for male odor (Brown 1977, 1978). Physiologically, male urine influences the length of the estrus cycle of the female (Aron and Chateau 1972, Cooper et al. 1972).
Thus, male urine functions as a sexual advertisement aimed at females, and intact females use may male urine to help them select a mate from among the advertisers -- females prefer males with high levels of testosterone. High levels of testosterone correlate with spermatogenesis (DeJong et al. 1977), maturation of the sperm in the epididymis (Moore and Bedford 1979), successful copulatory behaviors (Malmus 1977), the capacitation of of sperm in the female (Overstreet and Bedford 1974), and fertilization of embryos (Ewing et al. 1979).
Female urine marks: Females urine mark their environment the night before they ovulate in order to attract males to come and mate with them. She is advertising availability and receptivity via her urine marks, and marks more in the presence of preferred male urine (Taylor et al. 1982).
Male's response to female urine marks: Urinary odors of females in heat are highly attractive to intact male rats (Brown 1977, Sachs 1997, Pfaff et al. 1973). Males prefer the urine of estrus females to that of non-estrus females (Carr and Caul, 1962, Carr et al. 1966, Stern 1970, LeMangen 1952).
Castrated males show no preference for female odor (Brown 1977, 1978) or for receptive vs. non-receptive female odors (Carr et al. 1966). This lack of differentiation in castrates may be due to a decrease in motivation, rather than an inability to discriminate, because castrated rats can be trained to tell the odors apart (Carr and Caul 1962). To put it another way, castrates can still tell the odors of receptive and non-receptive females apart but this difference is not meaningful to them.
Therefore, female urine produced during proestrus -- the day before she ovulates -- serves as a sexual advertisement that attracts males. Such urine marks may help to bring males to the female at a time when she is most likely to conceive.
Rats may be "labeling" their habitat with urine marks. There are a number of hypotheses about the function of habitat labeling: urine marking (1) may create and maintain an optimum odor field, (2) may be a response to novelty that wanes with time, (3) may constitute an index of spatial knowledge, and (4) may increase the confidence of resident rats while decreasing that of intruders. These hypotheses need not be mutually exclusive.
(1) Optimum odor field theory: The marking of novel and unscented objects (Hopp and Timberlake 1983), the increase of urine marking in the presence of odors of other rats (Birke and Sadler 1984, Hopp and Timberlake 1983), and the marking of unscented areas (Stevens and Köster 1972) may serve to create and maintain an optimum odor field -- an optimum level of the rat's own odor -- in its environment (Hopp and Timberlake 1983, Eisenberg and Kleiman 1972).
The optimum odor field may be a self-feedback process that increases the home rat's familiarity with its environment (Eisenberg and Kleiman 1972). If the rat encounters a strange odor, this disrupts its odor field and the rat increases its marking to reinstate the optimum odor field.
(2) Response to novelty: Rats urine marking may also be a response to novelty (Bronson 1976, Maruniak et al. 1974), especially in a familiar environment. Hopp and Timberlake (1983) found that rats urine marking increases when rats smell a novel odor -- urine from a strange rat, a gerbil, or a chemical (amyl acetate), but as the rat became familiar with these odors its urine marking decreased. This result supports the novelty hypothesis of urine marking instead of the optimum odor field hypothesis.
(3) Index of spatial knowledge: Rats re-mark objects that have been moved (Harley 2001), and rats with damage to the hippocampus -- an area of the brain involved in spatial memory -- urine mark their environment more than rats without damage (Harley 1999). Urine marking may therefore be used as an index of spatial knowledge.
(4) Navigation system: rats can follow odor trails (not just urine) left by themselves and by other rats. They may therefore use such trails to navigate through the environment (Wallace et al. 2002). [Note: the rat's ability to track itself and other rats using odor may present a problem in the interpretation of maze studies on spatial navigation.]
(5) Increase confidence of resident: Marking one's own habitat may also increase the home rat's confidence while decreasing the confidence of intruders. In this latter sense, urine marking would be part of the repertoire of agonistic behaviors (Adams 1976).
Note, however, that a rat who is well-established in an area has had a lot of time to mark it, may therefore be more invested in its defense. So urine marking may correlate with increased confidence, without causing it. One way to test this would be to examine aggression against an intruder in a marked home cage, a cleaned home cage, a novel cage with the rat's own urine placed in it, and a novel cage with no urine.
Predictions: If urine tends to cause aggression in the resident rat, then aggression should be greatest in the home cage and in the urine-imbued novel cage. If resident aggression is enhanced by a combination of factors including the familiar environment and his own odor, then the strongest aggression should occur in the uncleaned home cage, followed by the cleaned home cage and the urine-imbued novel cage, and the least aggression should occur in the novel clean cage.
Urine marking in mammals is often called "territorial," and is assumed to play a role in territorial defense: the animal is supposed to urinate at the perimeter of its territory and thus deter other animals of the same species from entering that space. However, many of the claims of territorial urine marking have little evidence to support them: many of the observations of urine marking are anecdotal or are interpreted with preconceived notions of territoriality in mind (Johnson 1973).
The evidence on whether rat urine marking is territorial is mixed:
Evidence that supports a territorial function for urine marking: Gawienowski et al. (1976) found that male urine has a deterrence effect on other males, and Stevens and Köster (1972) found that rats prefer to mark clean places and avoid areas marked by predecessors. Richards and Stevens (1974) found that male rats prefer the urine of isolated males to socially housed males, which may indicate that socially housed male urine has a deterrence effect.
Evidence against a territorial function for urine marking: On the other hand, other studies have found that male rat urine is attractive to other male rats, and not a deterrent (Krames and Shaw, 1973, Schultz and Tapp 1973, Brown 1973). Richards and Stevens (1974) found that male rats prefer the urine of socially housed males to a plain odorless substrate, indicating that urine in this context does not elicit avoidance.
Therefore, it is unclear whether urine marking has a territorial function or not. It is also important to bear in mind that wild male Norway rats have a territorial social system, in which one rat defends a territory against intruders, only at low population densities. At high population densities (e.g. 0.2 rats per square meter, or one rat per 5 square meters), male Norway rats do not defend territories any more, because there are too many intruders to make territory defense worthwhile. At high densities male rats switch to a social heirarchy, called a despotism, in which one male rat is socially dominant over others regardless of physical location. Most pet and lab rats are kept at high densities, hence, domestic male rats tend to be socially despotic rather than territorial.
Rats deposit attractive cues on and around foods that they like. Young rats find these marks attractive, and prefer to feed at sites marked by other rats. This is one of the ways in which young rats acquire food preferences through cultural transmission (Galef and Beck, 1985, Laland and Plotkin 1991, 1993). Rats do not, howeve, appear to deposit aversive urine marks around poisoned food (Galef and Beck 1985).
Conspecific marking (urine-marking another rat) occurs when one rat crawls over another and deposits "a drop or two of urine, leaving a wet patch on the fur of the other rat" (Grant 1963). This may be a form of social communication, but its function is unknown.
One hypothesis is that such marking identifies other rats or maintains colony odor (Barnett 1975), but this has not yet been examined. Another hypothesis is that conspecific urine marking is no different from marking objects in the environment: other rats are marked just like inanimate objects are.
The function of conspecific marking may vary with the sex, age and hormone levels of the marker and the recipient.
Adult male-female marking
Taylor et al. (1984) found that males mark females at high rates, more than females mark males. Males mark females the same whether the females are in heat or not. Female urine marking of males varies with her ovarian cycle: females who were not in heat marked males more than females who were in heat.
Aggressive and non-aggressive males mark females at similar rates. However, females could tell the difference between aggressive and non-aggressive males, and marked the aggressive ones more (Taylor et al. 1984).
In a third experiment, females were paired with castrated males who had received either a low or a high injection of testosterone. The high-testosterone males marked females more than the low-testosterone males. Females can differentiate between the males with different testosterone levels, and prefered to urine mark the high-testosterone males (Taylor et al. 1984).
In conclusion, the female rat appears to be marking males with different amounts of urine to identify and select males she prefers. She marks males with preferred traits, such as higher levels of testosterone and aggression, more copiously than those with unpreferred traits.
Interestingly, females mark males more when the females aren't in heat. It is possible that her urine marks will help her choose and stimulate a high quality mate when she comes into estrus again a few days later (Taylor et al. 1984).
Adult male-male marking
Males readily mark other male rats. There appears to be no prefered body part to mark; urine is distributed over the back. On any given day, less than 25% of the back is marked (Taylor et al. 1987).
Testosterone: Conspecific marking is correlated with testosterone. Males who were castrated mark other males about half as much as they did before castration. However, testosterone replacement does not reinstate conspecific marking. Therefore, scent marking of other rats may be less dependent on testosterone than environmental scent marking, which increases with testosterone injections (Taylor et al. 1987).
Dominance: Socially dominant males mark subordinates more than vice versa. Dominants crawl over subordinates nearly three times as often as the reverse. On each crawl over, dominants and subordinates deposit similar amounts of urine (about 6.5 marks per crawl-over). The end result is that dominant rats deposit three times as much urine on subordinates as subordinates do on them. This discrepancy may be because subordinates don't have much opportunity to crawl over dominant males (Taylor et al. 1988).
Subordinate rats mark dominants and other subordinates differently: subordinates walked over dominants only half as often as over other subordinates, but deposited more urine on dominant rats per crawl-over (they deposit 6.6 marks when crawling over a dominant rat, but 3.3 marks over a subordinate) (Taylor et al. 1988).
In the end, subordinates mark dominants and subordinates with the same amount of urine, but deposit their urine on dominants in half as many passes. (Taylor et al. 1988).
It is possible that aggressive males are simply less discriminating, and deposit lots of urine everywhere, while females and subordinate males are more selective. Dominant males deposit more urine in the environment and on other rats than anyone else, but in spite of this, the chemical composition of the urine, and the pattern in which it is deposited, may be more important than the quanity.
Adult-juvenile females
When an adult and juvenile females are paired together, starting when the juvenile is 30 days old and ending when she is 50 days old, each marks the other at similar rates over time.
Adult-juvenile males
When an adult and juvenile male are paired together (from juvenile age 30-50 days), both mark each other at very high rates early on (from age 30-39 days). However, as the juvenile ages he marks the adult male less and less, even though his own testosterone levels are rising with puberty. The adult male continues to mark the juvenile at high rates. One reason the juvenile may mark the male less is that a young male approaching puberty is less likely to crawl over an adult male, so he doesn't have as much opportunity to mark him (Taylor et al. 1987).
Therefore, even very young juvenile males urine mark adult male rats, and they do so before their surge of testosterone at puberty. In contrast, very young juvenile males typically do not mark their environment at all.
Conclusion
The two types of marking -- environmental and conspecific -- share many features. Both are sensitive to hormone levels, both are sexually dimorphic (males mark more than females), and both are correlated (animals that mark the environment s lot also mark other rats a lot). However, there are differences too: conspecific urine marking may be less influenced by hormones than environmental marking, the two types of marking have different developmental trajectories. Therefore, conspecific marking may not simply be an extension of environmental marking, but may be a different behavior with its own different function.
