When Butterflies Meet

by Ronald L. Rutowski

Intent on seeing where she lays her egg, I am diligently following a Little Yellow female as she flies low to the ground along a railbed in south-central Florida. Suddenly a fast-flying male zips into view and dives toward the female. He flies rapidly around her as she continues deliberately along. After a few seconds, and with the male still in pursuit, she begins a slow upward flight that takes the pair ten to twenty feet off the ground. I almost lose them against the bright summer sky but then the male suddenly breaks off his chase and drops straight toward the ground before turning to dart away. The female descends a moment later and by a less precipitous route, but once near the ground she continues her search for a plant on which to lay her eggs, which I learned was a legume, the partridge pea (see articles about cassias).

Three may be a crowd but butterfly relationships not infrequently become a menage a trois. Here a female Falcate Orangetip (without the orange tips) is wooed by two males. April 28, 1993. Assunpink WMA, Monmouth Co., New Jersey (photo by Jeffrey Glassberg)

   My scientific life has been spent describing the interactions that occur when butterflies meet and trying to understand what is going on and why. In spite of the difficulties of studying behavioral interactions of these fast-flying aerial animals -- even determining the sex of the participants can be a problem -- I persist in following butterflies with stopwatch and notepad. In this article I hope to give you a sense of what I and others have discovered about the sexual encounters between butterflies, which you might put to use the next time you are butterflying.

Males are from Mars and females are from Venus?
Adults are the sexually active stage of the butterfly life cycle and so reproducing is the goal behind all of their behavior. However, male and female butterflies are very different creatures, who use different tactics to attain this goal.

   The activities of males are primarily those of finding, courting and mating with females, but various species (and sometimes males of one species, at different times and places) use different means to find females. Some males are patrollers, with sexually driven individuals flying through their environment looking for females here and there, while others are perchers, selecting a suitable site to sit and wait for females to appear. Classic examples of patrollers include the male whites and sulphurs. In this group, no male stays long in one place as he courses about searching for females. Among the best known of the perchers in North America are Painted Ladies and Red Admirals. In these species, males perch in the afternoon and patiently wait for females to appear on hilltops or along paths and walkways.

The wonderful wing-bar display of the Barred Sulphur. Hey, if you've got it, flaunt it. Lake Placid, Florida (photo by Ronald L. Rutowski)

   Females are another story. Usually they are found by a male very soon after emerging from the chrysalis. Or, they themselves fly to the areas where the males have set up territories. In either case they usually welcome a male's advances. But after this initial mating they typically become unreceptive to male courtship attempts and focus their time and energies on egg-laying. However, after laying eggs for a few days they may become receptive again; if they succeed in mating, they will then no longer accept a partner for another period before (perhaps) becoming receptive once more.

Prospecting for mates
Most butterfly interactions begin when a male, eager to court and mate, rushes toward any other butterfly that even vaguely resembles a female. Males are surprisingly indiscriminate [well, maybe its not such a big surprise -- ed.]. Little Yellow males will approach almost any yellow object of the appropriate size, including bits of surveyor's tape, cast off candy bar wrappers, and dead leaves. Males of the Empress Leilia in Arizona enthusiastically fly toward other kinds of insects passing nearby, even birds on occasion.

   When an approaching male draws near its target, what happens next depends upon the target's identity. First, the male may quickly veer off and continue on his way, as happens when the approached individual is a fellow male or a member of some other species. But, particularly when two males belong to the same species, they may chase one another back and forth for a bit before parting company to go their separate ways.

Courtship with unwilling females
Alternatively, a male may begin flying rapidly and persistently around the flying butterfly for longer than a few seconds. This behavior is a good indication the male has located a female but what happens next depends on whether she is receptive or not. If, as happens in most cases, she is not, then she may signal to the pursuing male that he is out of luck by beginning an ascending flight like that described at the beginning of this article. Invariably the male gets the message and gives up his chase usually after 10 or 15 seconds of the slow, upward flight.

   Another option is for the female to land and assume a posture that makes it exceedingly difficult for the male to copulate. The best known of these maneuvers is the "mate-refusal posture" of white and sulphur butterflies in which the female spreads her wings and points her abdomen skyward (see photo, below). Males cannot make genital contact with a female in this stance and so they usually give up after a frustrating 10 or 15 seconds of trying. Yet another option is for the perched female to persistently and rapidly open and close her wings while the male is trying to contact her abdomen tip with his own, an action that buffets her harasser and eventually sends him on his way.

First photos (I think) of the courtship dance of Arctic Skippers. Starting from the upper left, this sequence shows the synchronous wing flapping that the male and female engage in as they run along stems and leaves. Then the male curls his abdomen around to the tip of the females abdomen and they mate. June 28, 1996. McNair, Lake Co., Minnesota (photos by Jeffrey Glassberg)

Courtship with willing females
The behavior of a sexually receptive female is much more congenial from the male's perspective. A willing female slows her forward flight and finds a place to land when a suitable partner comes close. With little obvious courtship, he will land a little behind the female, scramble up beside her, and begin probing the rear margin of her hindwings with his abdomen. Once the tip of the male's abdomen meets that of the female, the genitalia link and copulation begins, all in a few seconds time. Once coupled, the pair sits quietly for a period that depends on the species but is typically 30 minutes to an hour.

   Sexual behavior can be a bit more exciting in those species in which the female requires that males perform more elaborate courtship rituals. One of the best known butterfly courtships is that of the Queen, described by Lincoln Brower and his colleagues in the 1960's. The striking feature of this courtship is that while the female is still on the wing, the male moves in front of her and begins flying up and down facing away from the female but very close to her head. While doing this he everts a pair of brush-like, scent-disseminating structures on his abdomen, called hairpencils, bringing them close to or even in contact with the female's antennas. Hairpencils are found in most milkweed butterflies, but we rarely see them because they are everted only during or just prior to courtship, and then only briefly. After the male uses his hairpencils for a minute or so, a receptive female lands on the ground or vegetation and permits the male to couple with her.

   Here, I must mention a well-known relative of the Queen, the Monarch which engages in a sort of mating frenzy in the late winter just before and as their well-known winter aggregations in central Mexico and the West Coast of the United States are breaking up. In sharp contrast to the hairpencilling display of their close cousin, male Monarchs are more likely to grab flying females and carry them to the ground where they attempt to mate with them. This illustrates the rather striking differences that can evolve in the courtship rituals of even closely-related species.

   Another species with a visually impressive male courtship display is the Gulf Fritillary. The eager male lands alongside the female and begins clapping his wings together about 5 or 10 times per second. Our slow motion films of this display show that the female swings her antennas back so that the one on the side next to the male is inserted between his wings and is therefore embraced by them with each clap of the male wings. Because males have special fringed scales along certain veins on the dorsal (upper) surface of the forewing, this display probably delivers a chemical signal to the female that encourages her to remain still and permit the male to couple.

   In my experience, the most bizarre display is that of the Barred Yellow, which ranges from the southern United States into Central America. After the female lands, the following male lands alongside the female. While his other three wings remain closed over his back, he extends his forewing on the side next to the female so that it is directly in front of her. He then waves the wing up and down in front of her several times a second in such a way that on each up-stroke the female's antenna is rubbed against the trailing edge of his forewing. If properly stimulated by this display, the female keeps her wings closed and bends her abdomen ventrally so that it protrudes from under the hindwings, which makes it readily available to the male for coupling.

Eager males but choosy females
Most butterfly courtships probably involve chemical and visual signals, even in species without elaborate or complex displays. Why do males provide these signals and why do females require them? Not all virgin females agree to mate, even after vigorous courtship. Perhaps females are sizing up the male's attractiveness from his behavior and the quality and quantity of signals he is delivering.

   What useful information might females get from the male's displays? One possibility is that they learn whether or not the male belongs to their species. Most mating between individuals of different species are unproductive and such matings are a waste of time for both sexes. Bob Silberglied and Chip Taylor demonstrated that Orange Sulphur females distinguish males of their own species from those of Clouded Sulphur by using chemical signals produced by the male and by the ultraviolet light reflected by special scales on the male's upperside wing surface. Interestingly, the bright orange color of the male was found to play little role in their attractiveness to females.

   In another example, Western White females preferentially mated with males having naturally darker markings on the margin of the forewing above. Diane Wiernasz found that she could increase a male's chances of mating if she experimentally darkened the appropriate marks with a marking pen. She concluded that this preference helps females avoid mating with males of a closely related butterfly, Checkered White, which occurs in the same areas.

   In addition, females may also get information during courtship about the male's quality relative to other males of the same species. His behavior and signals could tell her about the quality of his genes and the quality of nutrients that he can pass to the female during mating, both of which could affect the survival chances or number of offspring the female may ultimately produce. Whether female butterflies gain such benefits from actively choosing among males within their species has only recently been an active area of investigation in laboratories around the world. The experiments and results to date do not unfortunately allow simple or broad conclusions and so are beyond the scope of this brief overview. Suffice it to say that, because most butterflies do not behave well in cages, the study of mate choice and its advantages under controlled conditions is proving to be a difficult nut to crack.

Sometimes males choose inappropriate partners. Opposite page: A male Sachem attempts to mate with a male Whirlabout while both are perched on an embarrassed butterflier! Oct. 27, 1996. Roma, Starr Co., Texas (photo by Jeffrey Glassberg)

   As a final note on sexual interactions, although the general pattern is that males approach females, on occasion females will be seen actively approaching and chasing males. These interactions have been interpreted as attempts by females to draw the attention of males and are therefore called courtship solicitation. In my lab we have studied this behavior in Checkered Whites and found that, not surprisingly, the females that do this are most likely to be either virgins or females who have not mated for some time. In both cases females may be anxious to mate to acquire or renew sperm supplies and get on with the business of producing eggs. My friend, Per-Olof Wickman, at Stockholm University in Sweden found a similar behavior in the Common Ringlet, a species that occurs in both Sweden and North America.

Territorial males
Not all complex and lengthy interactions in butterflies are between males and females. In many species in which males use a sit-and-wait or perching tactic to locate females the males defend the same perching location for day after day and do not tolerate other males perching anywhere nearby. In other words, they are territorial. Resident males approach intruders and chase them from the territory, but intruders may resist, leading to intensely competitive interactions between the resident and intruder.

A male approaches a female who clearly is not interested, and who sticks her abdomen into the air to prove it. July 26, 1993. Chappaqua, Westchester Co., New York (photo by Jeffrey Glassberg)

   In Arizona, male Pipevine Swallowtails occupy and defend hilltop territories where they wait for females. John Alcock, Mike Carey, and I have observed lengthy aerial interactions between persistent intruders and territorial males, which spiral around one another while rapidly gaining altitude. In appearance, these interactions are very much like the ascending flights between males and unreceptive females. However, these male-male ascending flights are actually fights that require endurance and maneuverability as the butterflies climb three hundred feet or more into the sky. After one or more of these flights the intruder, usually but not always, ends up leaving the area. Thus, when we see an ascending flight we cannot automatically conclude that it is a male interacting with an unreceptive female.

   In a recent and fascinating study with Black Swallowtails, Bob Lederhouse and Mark Scriber at Michigan State University demonstrated that coloration may play a role in determining the outcome of these fights. They altered the color of newly emerged males with marking pens to make them look like females. They then released altered and unaltered males into an area where males were defending mating territories and recorded the success of the released males in becoming territory residents. The clear result was that males made to look like females were less successful in acquiring a territory, which adds a new twist to our understanding of the role of coloration in interactions between butterflies.

   So from this quick review what general statements can be made about what happens when butterflies meet? Clearly, the form of the interactions we observe is determined by the sexual identity of the interactants as well as their mating histories, coloration, and a host of other variables, some of which we do not yet fully understand. As a result, we can often infer from the form of the interactions what is going on and why, but not with complete certainty. For events like ascending flights, the participants and function vary depending on the species and context. The relevant caveat is to interpret what we see with care. In any event, the interactions of butterflies can be complex and beautiful, give us a bit of a window into how they experience their world and mates, and perhaps cause us to reflect on the interactions we have with them and members of our own species.