Avian Visual Cognition

Visual Control of Sexual Behavior

Chana K. Akins & Melissa Burns
Departments of Psychology, University of Kentucky & Texas Christian University

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This chapter is a review of the various visual cues and their mechanisms with regard to the sexual behavior of avian species. The first half of the chapter is devoted to describing various visual cues and their role in facilitating successful mating in the wild. From being able to predict the onset of the breeding season to attracting a mate, many visual cues help to direct the reproductive effort. Some cues may be predictive, such that they provide environmental information about the breeding season, and trigger neuroanatomical, neuroendocrine, and physiological changes in animals to ready them for the reproductive season. Other cues appear to be synchronizing in that they help synchronize the reproductive effort of potential mates, such as with elaborate courtship dances, and species-specific and/or sex specific visual features. The last half of this chapter explores the procedures, a description of the visual stimuli used in the laboratory setting, and the findings from various laboratory experiments. These experiments complement naturalistic observations in that they involve systematic manipulations to elucidate which visual stimuli control sexual behavior and how these visual stimuli control sexual behavior. In accordance with naturalistic studies, the findings from laboratory studies indicate that visual species-specific cues play a key role in the regulation of sexual behavior. Laboratory studies that manipulate experience indicate that animals learn about the visual features of potential sexual partners and about visual cues that signal a mating opportunity. Learning about visual cues that signal access to a mate or a potential mating opportunity has been shown to contribute to the reproductive fitness of organisms. Together, naturalistic observations and the findings from laboratory experiments have greatly enhanced our understanding of how visual stimuli control sexual behavior. This information is critical to our understanding of animal learning and cognition.

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Chapter Outline & Navigation

I.   Introduction

II. Visual Cues for Successful Mating

      Physiological Cues
      Predictive Cues
      Synchronizing Cues
      Ornamentation
      Courtship Behavior
      Courtship Structures

III. 
Visual Control of Sexual Behavior in the Laboratory
    
Laboratory Techniques for Isolating Visual Stimuli
      Species-specific Female Cues: Single-stimulus Tests of Social Proximity
     
Species-specific Female Cues: Single-stimulus vs. Choice Tests

IV.
Visual Control of Learned Sexual Behavior in the Laboratory
   
Pavlovian Conditioning of Visual Stimuli
     Species-specific Female Cues
     Local Cues
     Contextual Cues

V. Theoretical Implications:  The Behavior Systems Approach


VI. Conclusions

VII. References

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I. Introduction

Reproductive behavior is central to the ultimate fitness of organisms. Various sensory systems play a role in regulating reproductive behavior. The predominant system is typically highly-developed and species specific. For example, the olfactory system is highly developed in rats and serves as the primary sensory system involved in the reproductive behavior of rats. In contrast, the auditory system is highly developed in songbirds and it plays a critical role in social and courtship interactions. Just as the auditory system is highly developed in songbirds, the visual system is highly developed in some gallinaceous species of bird and serves as the primary sensory system involved in the reproductive behavior of birds. The purpose of this chapter is to review the literature on the various types of visual cues that affect sexual behavior and sexual learning and on how these cues influence reproductive behavior.

The first section of this chapter is a description of the predictive and synchronizing cues used by avian species in naturalistic settings that are associated with the visual system and that are critical for the performance of copulatory behaviors. Predictive cues are preparatory cues that serve to set up reproductive condition. They primarily serve to induce reproductive readiness and to activate the physiological mechanisms that regulate sexual behavior. Predictive cues include photostimulation, the hypothalamus-pituitary-gonadal axis, and sex hormones. In contrast, synchronizing cues serve to elicit reproductive behavior and may include sexually dimorphic plumage, ornaments, and courtship rituals. These cues serve to enhance sexual responding in females of many bird species.

The second part of this chapter is a review of the laboratory research that has been conducted to examine various types of visual cues. It includes a description of how these visual cues facilitate both unlearned and learned sexual behavior. Visual cues that have been found to enhance unlearned sexual behavior include species-specific female cues, while those that have been shown to facilitate learned sexual behavior include species-specific female cues, local or discrete cues, and environmental contextual cues.

Because we want to present an integrated account of both unlearned and learned sexual behavior, much of our discussion in the latter half of this chapter will include research that has been conducted with domesticated Japanese quail (Coturnix japonica). Domesticated quail are particularly well-suited for studying sexual behavior, in part, because Japanese quail they have a well-adapted visual system with which to gather information about the environment for potential mating opportunities. In addition, males and females are sexually dimorphic. Male quail have darker brown plumage, especially in the head and neck area, while female quail have a lighter shade with small black dots.  This sexual dimorphism may be related to their propensity to learn about various visual features involved in sexual behavior.

II. Visual Cues for Successful Mating

The survival of a species is dependent on the members of that species reproducing. For such an important function, however, reproduction is quite complex. To breed successfully, birds need to predict the onset of the breeding season, travel to a suitable breeding site, develop and maintain functional gonads, establish and defend a territory at the correct time, select and/or seduce a mate, coordinate sexual behavior with the mate, and switch from sexual to parental behavior when it is appropriate to do so. A large repertoire of diverse behaviors is required to navigate through each step of the reproductive process. The wrong behavior at the wrong time could prove to be detrimental to the reproductive effort. Fortunately, there are many cues that help to direct the reproductive effort along the correct path. Some cues come in the form of long-term changes throughout the environment, such as an increase in temperature and day length as spring draws near. Such omnipresent cues tend to cause relatively long-lasting internal changes in birds, such as an elevation of certain sex hormones that last throughout the breeding season. Ambient cues help birds to predict when the breeding season will begin and when it will end. Other external signs occur very quickly and in a limited area in the environment, such the appearance of a reproductively mature conspecific on oneís territory or the sound of a neighboring male singing to defend his territory. These types of discrete cues can elicit sudden changes in the birdís internal state, such as a brief surge in the release of sex hormones. Discrete cues often aid in the synchronization of mating behavior. Thus, it is important, even vital, that each reproducing member of the species be highly tuned to its external and internal environment in order to detect cues that signal when, where, and towards whom each specific behavior should occur.

Researchers have identified many environmental signals that serve as predictive or synchronizing cues for avian species. Many of these cues are of an auditory nature (e.g., vocalizations), some are somasthetic (e.g., humidity and temperature), but most of the cues used by avian species are visual. The present chapter, therefore, focuses on cues that are of a visual nature.

Physiological Cues

It is not a simple matter to turn a visual signal into reproductive activity. Rather, the conversion of external cues into sexual behavior is carried out by a series of neural and physiological events. In order for an environmental cue, such as the presence of a potential mate or the change in day length, to affect the reproductive physiology of a bird, the cue must be perceived by the nervous system, converted to meaningful information, and directed towards a target area in the body.

Photic energy from the environment enters the avian brain both through the eyes and by penetrating the skull to activate extra-retinal photoreceptors in the brain. Discrete visual cues in the environment, such as a brightly colored patch of feathers on a conspecific, enter the nervous system through the retina of the eyes. Ambient visual cues, such as daylight, activate photosensitive loci in the brain both indirectly, through the eyes, and directly, through the skull. The hypothalamus of the bird brain contains special cells that are sensitive to extremely low light levels, intensities comparable to the amount of light that can penetrate brain tissue. The hypothalamus also receives one-way afferent connections directly from the retina. These fibers terminate primarily in the suprachiasmatic nucleus, an area of the anterior hypothalamus that is essential in gonadotropic ("gonad changing") mechanisms in birds (doves - Cooper, Pickard, & Silver, 1983; ducks Ė Bons, 1976; jackdaw Ė Meier, 1973; Java sparrow Ė Ebihara & Kawamura, 1981; pigeon Ė Meier, 1973; Reperant, 1973; and house sparrow Ė Hartwig, 1974).

Many neurons in the avian hypothalamus are specialized for the synthesis and secretion of peptides into the bloodstream. Once in circulation, these peptides act as hormones on distant cells. Their effects are enduring and serve to control neuron excitability and synaptic effectiveness. Thus, peptides can enhance or suppress neuronal sensitivity to specific environmental stimuli. These long-lasting activities are thought to be important for a variety of behavioral functions, including mood, motivational state, and learning.

The hypothalamus also controls the endocrine system. Regulatory hormones produced by the hypothalamus are secreted into a blood vessel, the hypophyseal portal blood vessel, which drains into the anterior pituitary gland. The pituitary gland produces specialized hormones that act on target glands and tissues in other parts of the body by prompting the release or inhibition of certain hormones. Within the reproductive system, stimulation of the hypothalamus results in the secretion of gonadotropin-releasing hormone (GnRH) into the hypophyseal portal blood vessel. When activated by GnRH, the anterior pituitary secretes two gonadotropin hormones, follicle-stimulating hormone (FSH) and luteinizing hormone (LH). The gonads detect the presence of gonadotropins in the blood stream and respond by producing gametes and sex hormones. The sex hormones then bind to hormone receptors sites in specific loci in the brain (e.g., the pre-optic area, nucleus preopticus paraventricularis manocellularis, and nucleus hypothalami lateralis). Stimulation of these brain regions generates synaptic transmissions that ultimately create either changes in reproductive physiology, such as the development of song regions in the brain, or a specific motor activity, such as erecting and spreading oneís beautifully ornate tail feathers in the presence of a female.

Predictive Cues

The environmental cues most important for successful breeding are those that are most highly correlated with the breeding season. Because breeding activity occurs at approximately the same time each year, the diurnal photocycle, or varying light:dark ratio during the year, is an excellent indicator of when to prepare for the breeding season and when to terminate breeding. Testicular growth and hormone production are strongly correlated with day-length ("photoperiod"). Long days of the summer breeding season support large, productive testes while short days of winter instigate atrophy and general inactivity of the testes (Wingfield & Farner, 1993). In this respect, changes in the photoperiod provide predictive information (Wingfield, 1980) that induces gonadal maturation prior to the breeding season and causes degeneration of gonads at the end of the breeding season. Since the effects of day length on gonadal development were first reported by Rowan in 1925, the phenomenon has been demonstrated in about 70 species.

The development of a functional reproductive system requires several weeks, thus individuals must predict the ensuing reproductive period and begin maturation well in advance so that the gonads are functional when environmental conditions become favorable for breeding. This process has been well investigated in the males of many species (e.g., Mattocks, Farner, & Follet, 1976; Donham, 1979; Assenmacher & Jallegeas, 1980; Bluhm, Phillips, Burke, & Gupta, 1983;). As day length increases, photic stimulation of the hypothalamus results in the secretion of GnRH. When activated by GnRH, the anterior pituitary secretes two gonadotropin hormones, follicle-stimulating hormone Click here to view Figure 1 (FSH) and luteinizing hormone (LH). FSH acts on sperm-producing structures in the testes, while LH acts on interstitial cells of testes causing them to secrete the steroid hormone testosterone. The pituitary gland monitors the amount of testosterone in the blood, thus creating a negative feedback loop to maintain hormone levels within a set range. (See Figure 1) As testosterone level increases, the pituitary gland decreases secretion of LH. In contrast, a drop in testosterone stimulates the pituitary gland to produce and release more LH.

In general, wild avian species maintained on natural day lengths show a gradual increase in testes volume and plasma levels of sex hormones in the spring. These hormone levels remain high until midsummer and then decline. The testes also show a marked decrease in size as day-length decreases. In most species, the significant elevations of circulating sex hormones in the spring coincide not only with development of the testes and secondary sexual characteristics, but also with heightened aggression as territories are formed, and with periods of heightened sexual behavior (Mattocks, et al., 1976; Donham, 1979; Assenmacher & Jallegeas, 1980; Bluhm, et al., 1983; Stokkan & Sharp, 1980; Sharp & Moss, 1981; Scanes, 1974; Wilson & Follet, 1974).

The importance of the eyes relative to the extra-retinal photoreceptors in controlling photo-gonadal mechanisms is poorly understood. Studies have shown that when the eyes are removed, some bird species still show photoperiodically induced gonadal growth (Benoit, 1938; Beniot & Assenmacher, 1966; Menaker, Roberts, Elliot, & Underwood, 1970). For instance, White-crowned sparrows have light receptors in the ventromedial hypothalamus. Pinpoint illumination of these hypothalamic receptors by means of a single, thin light-conducting optical fiber induces both testicular growth and migratory behavior (Yokoyama & Farner, 1978). However, other species, such as domesticated quail fail to show gonadal responses to changes in photoperiod when blinded by bilateral enucleation (Bons, Jallageas, & Assenmacher, 1975). Thus it seems that the relative contribution of the retina versus extra-retinal photoreceptors to photoregulation in intact birds is diverse.

Synchronizing Cues

Other visual cues that are critical for successful breeding are those provided by potential mates or nest-related stimuli. These cues tend to be discrete rather than ambient cues in the environment. Although the details of the neural processing of discrete visual cues remain unclear, it is likely that the cues enter the nervous system through the retina of the eyes and follow the retinohypothalamic pathway to the hypothalamus. The hypothalamus then acts to indirectly increase or decrease sex hormone secretion. These hormones act on specific locations in the brain which, in turn, activate particular motor responses related to reproduction. For instance, many cues provided by potential mates are highly effective in stimulating LH release and they produce quick-acting changes in sexual behavior.

Unlike photic stimulation which causes slow and long-lasting changes to reproductive physiology, synchronizing cues may aid a bird in focusing its reproductive efforts on a potential mate, thereby releasing sexual behavior at the appropriate time during the breeding season. Discrete cues such as the presence of a nest box, nesting material, or a potential mate, are more closely related in space and time to reproductive activity than the light cycle. Due to their close spatial and temporal relationship, discrete cues can be powerful stimuli that engender specific reproductive behaviors to help synchronize the reproductive effort of the pair. In most species, initial predictive information, such as photoperiod, is necessary to bring a bird into reproductive condition in time for the breeding season. Specific stimuli then predominate to engage the readied bird in sexual behavior with an appropriate mate.

Synchronizing cues may be in the form of nesting material, as is the case of the cockatiel (Shields, Yamatoto, & Millam, 1989), or they may be in the form of species-typical and/or sex specific characteristics of a potential mate. For example, plumage and courtship dances are very common in birds. In fact, male birds are notorious for signaling sexual interest with visual displays. Other visual signals involve more subtle behaviors that occur in the course of reproductive activities. Many synchronizing signals are not obvious to human observers. For instance, it was long believed that female birds choose mates based on male characteristics that are visible to the human eye. Recent research has shown that this is not always the case. Rather, some species of birds make mate choices based on ultraviolet plumage coloration to which humans are blind (Bennett, Cuthill, Partridge, & Maier, 1996; Bennett, Cuthill, Partridge, Lunau, 1997). However, many sexual displays involve robust behaviors and brightly colored plumage and ornamentation that are easily discernible by the human eye. These the sexual displays have been well studied and provide wonderful examples of how birds can use visual cues to sexually stimulate members of the opposite sex.

Plumage is the most obvious indicator of species, sex, reproductive maturity, reproductive condition, dominance, and health. However, male birds also display elaborate ornamentation, engage in courtship behavior and build structures to attract females. The most effective form of visual stimuli in eliciting sexual behavior varies among species of birds.

Ornamentation

Elaborate ornamentation of males of some species serves as a strong sexual stimulus for females. Types of ornamentation include colorful or iridescent body feathers, crests, elongated or elaborate tails, and variable large areas of colorful skin exposed on the head, especially around the eyes. Often, the more exaggerated the trait, the more likely it will elicit copulation from the opposite sex. For instance, long-tailed widowbirds can have tails up to 0.5 meters long. This is a very attractive attribute since female long-tailed widowbirds typically prefer males that have the longest tails. When malesí tails were artificially enhanced or shortened by an experimenter, females were observed to prefer males with "super tails" that were 25 cm longer than natural (Andersson, 1982). Playing on the relationship between exaggerated secondary sex characteristics and sexual success, males often posture to emphasize ornamental feathers and color patches.

Peafowl ocellus

Bulwer's pheasant

Great argus pheasant

Great egret

Lyrebird

Peafowl offer an excellent example of a feature display. Colorful iridescent eyelike ocelli are located on the highly elongated tail coverts; about 100-175 such ocelli may be present on a single adult male. These male displays are mostly frontally oriented to exhibit the ocelli maximally. In an observational study, Rands, Ridley, and Lelliot (1984) found that male peafowl that were reproductively successful were of intermediate age, did not have longer tails or greater body mass than other males, but they spent more time displaying sexually. Furthermore, the males with the most  elaborate trains were typically most effective in attracting females (Petrie, Halliday, & Sander, 1991). Thus, the beautifully iridescent ocelli of the peacock tail acts as a sexual stimulus for peahen. The Bulwerís pheasant also signals females of sexual interest by displaying a fan of tail feathers. The stark white tail feathers contrast dramatically with the dark black feathers on the body. 

Much like peafowl, the male great argus pheasant signals his sexual interest in a female by fanning large, iridescent feathers.  However, the ornate feathers are located on his wings instead of his tail. Male great egrets also attract sexual partners by displaying special plumage. Their sexual signal involves the erection of long white filigree feathers located on the back and tail. The male lyrebird has a  greatly elaborated version of the great egret display. Lyrebirds have similar long white filigree feathers in the tail. When displaying, males emphasize their special plumage by throwing the tail feathers forward over the back and head.

Frigatebird

Kori bustard

Black sicklebill

Parotia brid of paradise

Wilson's bird of paradise

12-Wired bird of paradise

For female great frigate birds, the most powerful sexual stimulus comes in the form of an inflated red throat. Male frigate birds solicit females from a nest site by inflating a fleshy scarlet pouch beneath the throat. When a female is nearby, males accentuate their ballooning throats by spreading and vibrating their black wings. The kori bustard also inflates a throat pouch to attract females, however, the ballooning pouch is covered in long, wispy feathers rather than the brightly colored flesh of the frigate bird. 

For several species of New Guinea birds, sexual stimuli take the form of plumage displays that leave males looking less like birds and more like abstract works of art. (See the Black sicklebill, Wilsonís bird of paradise, Parotia bird of paradise, and 12-Wired bird of paradise). For each species of bird, only a specific shape, angle, color, or  movement that is associated with the malesí display sexually stimulates the female. The male of the species that is best able to match the femalesí prototype stimulus will be the most successful at mating.

Courtship Behavior

Buff-breasted sandpiper Prarie chicken Count Raggi's bird of paradise Raggiana bird of paradise Temmick's tragopan

Courtship dances are another type of visual signal used to induce sexual behavior in potential mates. For instance, the sexual display of the great snipe male involves vigorous activity rather than ornamentation. When a female approaches a male, a male will shift his activity from territorial defensive behaviors to intense flutter-leaping near the female. Females of lekking 

species are sexually stimulated by the sight of a gathering of males vigorously displaying their most  sexually stimulating attribute. The conservatively dressed male buff-breasted sandpipers gather in northern Canada to breed. When a female arrives at the lekking ground, the males will display their best attribute Ė a snow white armpit Ė by raising one wing. When under close scrutiny by a female, the male may become excited and expose both armpits. This display is very appealing to female buff-breasted sandpipers.

In the case of the Lesser Prairie Chicken, ornamentation and activity are combined to stimulate potential mates. About 14 sexually mature males gather on a common lekking ground to display. The males produce a yodeling vocalization, which exposes and expands brightly colored skin patches at each side of the neck, all the while fanning and closing the tail feathers. When a female approaches the lek, a new behavior is  performed at high intensity, the "nuptial-bow" posture, which is often followed by copulation (Johnsgard, 1994).

Count Raggiís bird of paradise is another lekking species with a spectacular sexual display. Males attract potential mates by bending forward and vigorously flapping their wings while fluffing out long colorful plumage on their backs. The male Raggiana bird of paradise also uses high-intensity activity to accentuate his beautiful plumage.

Temmickís Tragopans have a spectacular courtship display. Males of this colorful species drum their wings rhythmically while hiding behind a rock or fallen log. When a female approaches, the male springs to the top of the rock or log then erects a blue feather horn above each eye, fluffs his body feathers, and spreads his wing feathers in a downward position. He will hold the pose for several seconds, then run to the location from which the female observed his display. If she is still there, they will copulate. It is hypothesized that the display serves to mesmerize the female into temporary immobility (Johnsgard, 1994). Regardless of the effect on the female, it is evident that surprise is a vital part of the display. When captive males are not provided with a suitable location in which to hide and display, courtship may not take place at all (Johnsgard, 1994).

Courtship Structures

Building complex, highly decorated, colorful structures allows the visual display to exist independently of the male, freeing him from burdensome ornamentation and bright colors that increase risk of predation. This is the method of display employed by bower birds. Males of this Satin bower bird promiscuous species build bowers to attract females. A bower is a small structure consisting of two walls of twigs, separated by enough space to barely allow an adult bower bird to pass through, and variably decorated at one or both ends with colorful items. The color of the decorations varies between species. For instance, blue is the favorite color of the satin bower bird. Their bowers are commonly decorated with blue parrot feathers, blue, violet, or purple flowers and berries, blue human artifacts (glass, paper, plastic, aluminum foil) grayish fungus, brownish snail shells, and greenish flowers and fruits (Gillard, 1969). A particularly remarkable bower Vogelkop gardener bower bird is created by the male Vogelkop gardener bowerbird. For this species, a powerful sexual stimulus for females takes the form of large, elaborately decorated huts. Males sing from and posture at their bowers. When a female is seen by the displaying male, he vocalizes while posing with his tail elevated, bill pointed towards the ground, and body held on stiff legs. Sometimes, he will hold a feather or other bower object in his bill, with wings outstretched and tail raised before the watching female. If the female remains in the bower, the male will mount the female and copulate. The lure of an attractive bower appears to overpower the actions of the male. If the bower is particularly well decorated, the female may remain in the bower for some time, or even return to it repeatedly after the male has forcibly driven her from it with severe pecking and clawing movements (Cooper & Forshaw, 1979).

In some species of birds, the elaborate and colorful male displays will prompt a female into nest building activity or receptive squatting. In other species, the particularly enthusiastic hopping and bobbing by the male is sufficient to bond a female with that male for the remainder of the breeding season. Regardless of the form it takes, the result of an effective sexual displays is cooperative copulation between the pair.

In summary, the first section of the chapter has provided descriptions and examples of various visual stimuli and their role in eliciting and regulating courtship and sexual behavior in a naturalistic setting. Although naturalistic observations provide valuable and interesting information about courtship and sexual behavior, they do not provide information about the causes of these responses with regard to visual stimuli. Laboratory experiments allow for experimental manipulation and control of various stimuli to better ascertain what visual stimuli may be involved in the regulation of sexual responding. Such manipulations invariably involve introducing circumstances that are not likely to occur in the field. This research is both necessary and valuable because it can serve to identify sources of visual stimuli that control sexual behavior and the mechanisms that accompany them.

The next section of this chapter provides a review of some laboratory experiments that have been conducted to investigate visual control of unconditioned sexual behavior. The techniques used to investigate visual control of sexual behavior involve presenting taxidermic models that contain various visual features of a female quail. The effectiveness of visual features in eliciting sexual responding may then be assessed by monitoring sexual responding of male quail. Some of the experiments involve measuring a social proximity response while others involve monitoring more direct indices of sexual responding such as the frequency of grabs, mounts and cloacal contact movements.

III. Visual Control of Sexual Behavior in the Laboratory

Laboratory Techniques for Isolating Visual Stimuli

One laboratory technique that has been used to identify socially effective visual stimuli involves using a window test Click here to view Figure 2 apparatus. A window test apparatus has been used to investigate male social proximity in domesticated quail (see Domjan & Hall, 1986). The test apparatus consists of a window that can be closed by placing a piece of opaque duct tape over the opening. When the window is open, the male can see the female only by standing directly in front of the window. (See Figure 2).

The social proximity behavior of male quail is thought to share characteristics with mate guarding in other birds. Mate guarding is primarily controlled by the visual cues of a female conspecific (Lumpkin, Kessel, Zenone, & Erickson, 1982). Males of some avian species, such as magpies (Birkhead, 1979) and bank swallows (Beecher & Beecher, 1979) display social proximity by remaining near a female conspecific. The social proximity behavior of male domesticated quail is similar to the mate guarding behavior of other avian species, except that, it does not appear to be strongly influenced by the reproductive state of the female conspecific (Domjan & Hall, 1986). It does, however, appear to be controlled primarily by the visual cues of the female (Domjan & Hall, 1986; Domjan & Nash, 1988).

Another technique that has been useful in identifying the critical visual stimuli that control social and sexual behavior is the use of taxidermically-prepared models. Live stimulus animals present a complex of visual, auditory, olfactory, and behavioral stimuli, any of which could potentially elicit a sexual response by a conspecific. Use of taxidermic models is an effective technique for isolating visual stimulus features. Taxidermic models of females are effective in eliciting male copulatory behavior in various galliform birds, including quail (Domjan, Greene, & North, 1989), chickens (Fisher & Hale, 1957; Carbaugh, Schein, & Hale, 1962), and turkeys (Schein & Hale, 1957, 1965).

Using the window test apparatus and taxidermically-prepared models of male and female quail, Domjan and Nash (1988) evaluated whether the static visual features of a female model were sufficient to control male social proximity behavior in the absence of vocalization, olfactory cues and movement. They found that male quail that had visual access to a normal adult female spent more time near the opened window than when they had visual access to an empty side cage or one containing live male birds. More importantly, the social proximity behavior of the males presented with female models was similar to the social proximity behavior to a live female quail. Thus, the femaleís calls and movements were not necessary to stimulate social proximity behavior in males.

Species-specific Female Cues: Single-stimulus Tests of Social Proximity

Partial taxidermic models are useful in testing the effectiveness of various female conspecific body parts in eliciting male copulatory behavior. Domjan and Nash (1988) investigated the social proximity behavior of male quail to taxidermically-prepared models of male and female quail with various body parts.

Males were given single-stimulus tests with the following models in this order: a full-body female quail model, a full-body male quail model, a female quail head and neck, a male quail head and neck, a full-body female quail model whose head was covered with a brown cloth hood, a female quail head and neck suspended upside down, a full-body male quail model, and a full-body female quail model. The amount of time subjects spent near a window through which they could see a model was recorded. (See previous section on Common Techniques for Isolating Visual Stimuli for more detail.)

Click here to view Figure 3The results indicated that male quail showed the most social proximity behavior in the presence of the head and neck female model and the whole body female model (See Figure 3). Amazingly, the response to these two stimuli was the same. Not only were the static visual features of the female model sufficient to elicit male social proximity behavior but the features of the head and neck were as effective in eliciting social proximity Taxedermic Head Models behavior as the entire body of the female. The importance of the head and neck as visual stimuli may be related to the high degree of sexual dimorphism evident in the head and neck feathers of domesticated quail. The relationship between the stimulus control of sexual behavior and the degree of sexually dimorphic visual cues is also evident in other avian species, including domesticated turkeys (Schein & Hale, 1965), and red jungle fowl (Wilson, 1974).

Species-specific Female Cues: Single-stimulus vs. Choice Tests of Copulatory Behavior

Male turkeys respond best to models that contain a femaleís head and neck (Schein & Hale, 1957, 1965; Schoettle & Schein, 1959), but male chickens respond best to models that contain a femaleís body (Carbaugh et al., 1962). Schein and Hale (1965) speculated that the differential effectiveness of cues provided by the body of a female for male turkeys and chickens is related to the postures involved in their copulatory behavior. After mounting, a male turkey sees only the femaleís head and neck because he completely covers the rest of her body. In contrast, a male chicken maintains visual contact with the femaleís body during copulation. A male chicken grabs the henís neck or comb at the start of the copulatory sequence and maintains the grab during the mount and cloacal contact movements, ensuring visual orientation to the henís body.

The copulatory behavior of male domesticated quail is similar to that of chickens. A male quail first grabs the feathers of the Click here to see video of this behavior femaleís neck in his beak, steps onto her back, spreads his wings, and arches his back, lowering his cloaca with that of the female. Click here to see a video of this sexual behavior.  He then displays a rapid "shivering" movement which ends in a few moments of immobility, still with the wings spread and in the arched position. Schein and Haleís analysis (1965) suggests that because male quail presumably maintain visual contact with the henís body, cues provided by a henís body should be sufficient to elicit copulation. Crawford and Akins (1993) tested this prediction inHead model a study using stimulus  models with varying proportions of a female quail and artificial parts made of terrycloth. A whole-body model was a completely  natural female model positioned in a sexually receptive squat position. A head model contained a femaleís head and neck positioned in front of an artificial body. A body model consisted of a femaleís body positioned behind a vertical terrycloth cylinder similar in size to a femaleís head and neck. The artificial model was composed entirely of terrycloth.

Click here to view Table 1Male quail were given single model tests and choice tests in the following sequence: (See Table 1). The frequency of grabs and cloacal contacts were recorded, as well as grab latency (sec). For the single model tests, both whole and head models were effective in eliciting male copulatory behavior while the body andCopulatory behavior with head model artificial models stimulated little copulatory responding. Males had slower grab latencies with body and artificial models than with whole and head models. Although males grabbed the whole model  more often than any other model, they also made more cloacal contacts with both whole and head models than with body and artificial models.

The choice tests supported different conclusions about the relative contribution of various body parts in controlling male copulatory behavior (See Figure 4). More copulatory responses were directed toward the whole  model than toward the head model. In addition, more copulatory responses were directed toward Click here to view Figure 4 the body model than the artificial one. Surprisingly, however, male quail responded comparably to the body model and the head model. This is contrary to what the findings of the single model tests indicate. Single model test results support previous findings that the plumage of a henís head and neck might be sufficient for eliciting copulatory behavior. In contrast, the choice test results indicated that femaleís hind body plumage is also important in eliciting copulatory responding.

Itís unclear why the choice tests were more effective in revealing control of copulatory behavior by the femaleís body, rather than by her head and neck features. One possibility is that choice tests are more effective in revealing control by weak stimuli. Perhaps the cues provided by a female quailís body are relatively weak compared to her head and neck cues, but when two models are presented, body cues still influence sexual responding.

In summary, the findings of the laboratory experiments that have been conducted to investigate the stimulus control of visual features on male sexual responding indicate that the species-specific cues of the female, specifically the head and neck features, elicit more social proximity behavior and more copulatory responding than other visual features. (The exception to this appears to be when animals are given a choice between copulating with a model that contains head and neck cues versus a model that contains body cues.) That species-specific cues facilitate sexual responding may not be coincidental. As previously discussed (see introduction), male and female quail are sexually dimorphic and the head and neck features are the most sexually dimorphic plumage traits of Japanese quail. These visual stimuli appear to be the most important visual stimuli in eliciting sexual responding. The findings of these laboratory studies are in accordance with naturalistic observations in which species-specific cues and sex-specific stimuli are important in synchronizing a mating event.

Given that sexual behavior is subject to the influence of prior experience, it is necessary to investigate aspects of sexual behavior that result specifically from prior experience with visual stimuli. The experiments in the previous section did not involve manipulating experience of the subjects to visual stimuli. Therefore, the next section will review several laboratory experiments in which the acquisition of sexual responding to various visual stimuli is investigated. Species-specific female cues, local cues, and contextual cues will be used as visual stimuli.

IV. Visual Control of Learned Sexual Behavior in the Laboratory

Pavlovian Conditioning of Visual Stimuli

The Pavlovian Conditioning Paradigm

Pavlovian conditioning was discovered by Edwin B. Twitmyer. In an experiment in which he tested the knee-jerk reflex of college students by sounding a bell 0.5 seconds before hitting their patellar tendon, Twitmyer found that after several trials, the bell was sufficient to elicit the reflex in some of the students (Twitmyer, 1974). After Twitmyerís discovery, Ivan Pavlov, a Russian physiologist, conducted systematic studies of Pavlovian conditioning as an extension of his research on the process of digestion, using a salivary conditioning preparation. Pavlovís basic procedure for the study of conditioned salivation in dogs involved two stimuli. One of these was a tone or a bell. On its first presentation, this stimulus might have elicited an orienting response, but not salivation. The other stimulus was meat powder placed in the mouth. At first the dogs only salivated to the presentation of the meat powder but after several trials of having the tone paired with, or presented slightly before, the meat powder, the dogs also came to salivate when the tone was sounded. The meat powder that elicits the response of interest without prior training is called an unconditioned stimulus or US. Salivation elicited by the meat powder is an example of an unconditioned response or UR. The tone is an example of a conditioned stimulus or CS, and the salivation that develops from the tone is called the conditioned response or CR.

For more on this topic, see Control Procedures.

In an attempt to identify the species-specific cues of females, investigators have conducted experiments with sexually experienced subjects. Less experienced subjects do not respond as reliably as sexually experienced ones (e.g., Fisher & Hale, 1957). Sexual experience can enhance various aspects of reproductive behavior. For example, sexually experienced ring doves (Lehrman & Wortis, 1960) and domestic chickens (Fisher & Hale, 1957) are more successful in their reproductive behavior than are sexually inexperienced birds. These results suggest that subjects may learn something over the course of sexual experience. Learning may occur in the form of Pavlovian conditioning.

In some of the first Pavlovian conditioning experiments, Wolfsohn in 1897 in Pavlovís laboratory, investigated the salivary response of dogs to the visual cues of materials such as sand (see Domjan, 1993). Initially, the visual cues of the sand were ineffective in eliciting salivation; only the tactile cues of sand in the mouth worked. However, with repeated experience with sand in the mouth, the previously ineffective visual cues of the sand (conditioned stimuli) became associated with the biologically significant tactile cues of the sand (unconditioned stimuli).

Similarly, in sexual behavior, only some of the visual features of a potential sexual partner or mate may be effective in eliciting sexual behavior initially. With repeated sexual experience, initially ineffective features of a sexual partner may become associated with the biologically significant event, copulation, and thereby come to elicit sexually relevant responses. This suggests that animals may learn about the visual features of potential sexual partners and that what they learn may determine the effectiveness of visual cues in eliciting future social behavior.

Species-specific Female Cues

Just as in naturalistic observations, visual stimuli that are particularly effective in eliciting learned sexual behavior often involve stimuli that contain species-specific cues. Studies with domesticated quail have indicated that the sexual response of male quail to female conspecifics is, at least, in part due to what males learn about the species-specific cues of the female quail. Cusato and Domjan (1998) recently elucidated on the significance of species-specific female cues in sexual learning. In their experiment, two CSs were used; a taxidermically-prepared female head and partial Click here to view Figure 5 neck model and a terrycloth model (See Figure 5). The head and neck model did not elicit approach or copulatory responding when it was first presented. However, subjects came to approach and copulate with the model after repeated nonreinforced exposure to the model. In contrast, the terrycloth model that lacked the female head and neck features did not elicit responding as a result of previous nonreinforced exposures and it elicited little copulatory responding. Thus, although male quail have a predisposition to respond to female species-specific head and neck cues, repeated exposure to these cues may facilitate the acquisition of sexual responding.

Local Cues

Evidence from several studies indicates that arbitrary local visual cues may also come to control sexual responding. In a previous experiment (Hollis, Cadieux, & Colbert, 1989) with male blue gourami fish (Trichogaster trichopterus), male and female gouramis were presented with a 10 sec red light CS followed by a 15 sec exposure to each other (the US). Both male and females immediately approached the CS and engaged in a frontal display involving the erection of all fins. In addition, classically conditioned males significantly attenuated their territorial aggression and began courtship activities almost immediately. Thus, reproductive benefits might result from the Pavlovian conditioning of local visual cues with copulatory opportunity.

In a similar experiment (Domjan, Lyons, North, & Bruell, 1986) with birds, male quail were presented with a 10 sec red light, the CS, followed by the opening of an opaque door that separated the maleís test cage with that of a femaleís cage. Male quail were allowed five min to copulate with the female bird in the side cage. A control group was given copulatory access to a female bird 3-5 hours after the red light was presented. The amount of time subjects spent near the red light was measured on successive trials for 25 trials. Evidence for Pavlovian sexual conditioning was Click here to view Figure 6 inferred from the development of differential responding between the two groups (See Figure 6). The experimental group that received the red light followed by copulation with a live female rapidly increased the amount of time they spent near the red light across trials, whereas the control group showed no systematic acquisition of approach behavior. In contrast, during the 30 sec before the introduction of the red light (the pre-CS period), the approach behavior of the experimental and control groups did not differ across trials. These results suggest that approach behavior can come under the control of an arbitrary local visual stimulus that serves as a reliable predictor for sexual reinforcement. This approach behavior is similar to the approach behavior displayed by males toward the species-specific visual cues of the female.

Similar results have been reported with a more complex visual stimulus, a stuffed toy dog (Domjan, OíVary, & Greene, 1988). The toy measured about 14 cm from the tail to the tip of its nose. It had a bright yellow terry cloth surface, a thin black collar, black nose button, and white eyes with small black pupils. Male quail in the experimental group were presented with the toy for 30 sec followed by copulatory opportunity with a female quail. Quail in the control group were presented with the toy for 30 sec, 90 min after copulatory opportunity with a female quail. Two Click here to view Figure 7 types of trials were conducted, toy-absent trials and toy-present trials. (See Figure 7) Subjects in the control group showed little approach behavior on either type of trial. However, subjects in the experimental group increased their approach behavior across trials, specifically on the toy-present trials. Itís clear that the conditioned approach behavior displayed by subjects in the experimental group was controlled by the visual cues of the toy dog and the association of these cues with copulatory opportunity.

Contextual Cues

The most complex visual stimuli involved in conditioning are contextual cues or spatial cues. Not only do they include a wide variety of visual stimuli, but they may also contain local and/or species-specific visual cues. When contextual cues contain local and species-specific visual cues, they serve to modulate sexual responding.

Context modulation of local visual cues has been examined in studies with domesticated quail. In one study (Domjan, Akins, & Vandergriff, 1992), male quail were exposed to two distinct contexts that both contained a square holding box (the local CS). One context had a sand floor, white side and back walls, a wire mesh front wall, and contained dried tree branches. The other context contained a wire-mesh floor, natural wood-grain side walls, clear plastic front wall, and contained no tree branches. Subjects were housed in each context on alternate days, so that they spent an equal amount of time in both places. Exposure to the two contexts differed only in that a female bird was released from the holding box in one context (the sexual context) but not in the other context (the nonsexual context). Male quail in the sexual context, therefore, were allowed to copulate with the female quail that were released from the holding box in the sexual context. 

Results indicated that subjects increased the amount of time they spent near the holding box across trials in the sexual Click here to view Figure 8 context but not in the nonsexual context (See Figure 8). Subjects also continued to spend time near the holding box in the sexual context in the absence of the female bird. Thus, context may have served as a modulator that provided information about when the holding box would release a female bird. Alternatively, the conditioned excitatory properties of the context may have summated with conditioned excitatory properties of the female holding box, resulting in greater responding to the holding box in the sexual context than in the nonsexual context.

In addition to modulating approach responses to local visual stimuli, context modulates approach behavior to the species-specific cues of female quail. In the same experiment described above (Domjan et al., 1992), after male quail were given 20 trials in the sexual context and 20 trials in the nonsexual context, they were tested for their response to a female quail in each context.  Figure 9 shows that the presence of the female bird stimulated significantly more approach behavior to the Click here to view Figure 9 window if the female bird was visible in the context in which the subjects had copulatory opportunity (the sexual context) than if the female bird was visible in the nonsexual context. Although subjects spent a substantial amount of time near the window to the female's side cage even in the nonsexual context, they were more attracted to the female quail in the sexual context than in the non-sexual context. Thus, the effectiveness of the female species-specific cues in eliciting approach behavior was enhanced by the presence of contextual cues that came to be associated with previous copulatory opportunity.

Contextual cues may also form a direct association with a sexual US. The difficulty in testing for direct context-US relationships in sexual learning is that the sexually conditioned response is usually directed toward an object in the context. The object, thereby, becomes the CS and context presumably modulates responding toward it.

A recent experiment (Akins, 1998) was conducted to investigate the direct association of context with a sexual US by using a place preference procedure. An initial preference test was conducted to determine which of two distinct contexts male quail preferred. One context had green walls and a wiremesh floor while the other context had orange walls and a sand floor. Subsequently, the quail were given several trials in which they received copulatory opportunity with a female in their nonpreferClick here to view Figure 10red context. As a result, males shifted their preference to the context in which they received copulatory opportunity with a female bird (See Figure 10, top panel). In addition, paired males showed increased locomotor activity across trials during the five minutes before a female was introduced into the chamber whereas an unpaired control group did not (See Figure 10, bottom panel). This increased locomotor activity may been the result of the development of an "anticipatory response". An unpaired control group did not demonstrate a shift in place preference. Thus, the shift in place preference was due to the direct association that developed between the contextual cues and copulatory opportunity.

V. Theoretical Implications: The Behavior Systems Approach

A Behavior Systems Analysis

The behavior systems approach is a relatively new and comprehensive model of learning (for reviews, see Timberlake & Lucas, 1989; Timberlake, 1993, 1994). According to the model, presentations of a US in a conditioning procedure activates the behavior system relevant to that US. There are various behavior systems that might be activated, such as the feeding system, defensive system, or sexual behavior system. Each behavior system consists of response modes that are arranged on a temporal and spatial continuum from appetitive general search behavior to focal and consummatory acts at the other end. For example, a feeding sequence may begin in a general search mode characterized by a search for food-related cues. When cues predicting the presence of food are encountered, the animal may enter into a focal search mode. When food becomes available, the animal enters into a consummatory/handling mode. As the certainty of food declines, after ingestion, the animal may re-enter the focal search mode, looking for food nearby, and if the animal remains unsuccessful, it may re-enter the general search mode. A conditioned stimulus that becomes associated with an unconditioned stimulus may come to elicit certain modes depending on the point at which it becomes integrated into the temporal and spatial organization of the system.

The control of the sexually conditioned response by visual cues fits nicely with a behavior systems approach (see Timberlake, 1994 for review). According to this perspective, behavior systems consist of coordinated sets of responses that are required to accomplish a biologically important task. In a species with a well-developed visual system, such as the domesticated quail, the response the bird makes may depend on the presence or absence of certain visual cues, as well as their temporal and spatial relationships. For example, the absence of a female quail may elicit increased locomotor activity or general search behavior for a potential sexual partner. When local visual cues signal that a potential partner is nearby, approach behavior or focal search behavior is elicited. When the male sees the head and neck of the female, he may approach and then copulate with the female. Thus, the behavior systems approach can be used to predict the nature of the conditioned response with respect to the type of visual stimuli used to elicit the response.

Click here to view Figure 11Domjan (1994) formulated a behavior system for Pavlovian sexual conditioning (See Figure 11) that contains response and stimulus dimensions. The response dimension consists of three categories: general search behavior, focal search, and copulatory behavior. The stimulus dimension likewise consists of three categories: species-specific cues, local cues, and contextual cues. According to Domjanís model, species-specific cues and local cues elicit conditioned focal search behavior (e.g., Nash, Domjan, & Askins, 1989; Domjan & Hall, 1986, respectively), while contextual cues serve to modulate species-specific and local cues to elicit conditioned focal search and copulatory behaviors (e.g., Domjan, et al., 1992; Domjan et al., 1986). Domjanís model can be updated by including more recent evidence for the effectiveness of female species-specific cues eliciting conditioned copulatory behavior (Cusato & Domjan, 1998), and the effectiveness of context to directly elicit focal search behavior (Akins, 1998).

VI. Conclusions

Successful reproductive behavior requires the presence of both predictive and synchronizing cues. Environmental cues such as daylength or photoperiod serve as predictive cues that are often correlated with the physiological mechanisms, such as gonadal maturation and hormone production, that further regulate reproductive behavior. Although, the role of the visual system in controlling photo-gonadal mechanisms is not completely understood, there is some evidence for the influence of visual stimuli on the hypothalamus.

In contrast to predictive environmental and physiological cues, other visual stimuli may serve as synchronizing cues that influence reproductive behavior more immediately. Synchronizing cues that release sexual behavior include decorative ornaments, elaborate courtship rituals, the building of intricate structures, or a combination of these cues. Naturalistic observations have provided a plethora of examples that implicate the importance of the visual system in regulating courtship but they do not provide causal information.

Laboratory studies allow for the manipulation and control of stimulus presentation. The findings of laboratory studies conducted to investigate which visual features of the female are important for eliciting sexual behavior indicate that the species-specific cues of the female are most important. In male domesticated quail, head and neck female features stimulate as much social proximity behavior as the full body of a female bird. The head and neck cues of the birds may be effective visual stimuli in eliciting male sexual responding because of their high degree of sexual dimorphism. In contrast, when given a choice, males direct as much copulatory responding to a model that contains no head and neck cues as they do to a model with head and neck cues. Thus, there may be circumstances in which male quail use other visual features of the female during sexual responding.

Learned sexual responses are similar in form to unlearned sexual responses except that the nature of learned sexual response may be even more tightly controlled by the type of visual stimuli that elicit them (see Domjan, 1994 for review). Typically, female species-specific cues come to elicit conditioned approach and conditioned copulatory responses whereas arbitrary local cues come to elicit conditioned approach but rarely conditioned copulation. Sexually conditioned contextual cues serve to modulate species-specific and local cues. They enhance conditioned copulatory responding toward species-specific cues and they modulate conditioned approach behavior toward local cues by providing discriminatory cues that signal when copulatory opportunity will become available.

From a functional perspective, conditioning to visual stimuli has been shown to contribute to the reproductive fitness of organisms. For example, not only does signaling the accessibility of a female blue gourami fish enable classically conditioned male blue gouramiís to attenuate their initial aggressive response toward arriving females, but more importantly, classically conditioned males were able to spawn with females sooner, clasp females more often, and produce more young than males that did not have the benefit of a signal (Hollis, Pharr, Dumas, Britton, & Field, 1997). Similarly, Domjan, Blebois, & Williams (1998) found that after several pairings of a distinct environment with copulatory opportunity, a stimulus that contained some female head and neck features presented in the environment resulted in the release of greater semen volumes and greater numbers of spermatozoa in male quail. The findings of these experiments and others suggest that understanding the role of function is critical to our understanding of animal learning and cognition (see Hollis, 1997 for review).


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Links Added by the Authors

For a good example of  feather display, see this movie about Peafowl.

A species in trouble: the Lesser Prairie Chicken.

Viewing of the Lesser Prairie Chicken.

Information about Temmick's Tragopan Pheasants.

Click here for information about Bower Birds.

Click Here for a list of photographers who's work has been added to this chapter.

 Acknowledgements  

We gratefully acknowledge Michael Domjan and Robert Cook for their helpful suggestions on this chapter. Preparation of this chapter and much of the quail research described were supported by Grants MH39940 and IBN-9728756 from the National Institutes of Health (M.D.) and National Science Foundation (C.A.), respectively.