PIPE AND BY AZdownloads.hindawi.com/journals/psyche/1991/049063.pdf · kmsouth ofAjo, Arizona where...

THE MATING BEHAVIOR OF DROSOPHILA MOJAVENSISON ORGAN PIPE AND AGRIA CACTUS

BY ROBERT A. KREBS and Karen L. Bean

Department of Zoology, Arizona State UniversityTempe, AZ 85287-1501

INTRODUCTION

Drosophila flies are prime examples of laboratory animals thathave been poorly studied in nature. This is true even for the cac-tophilic members of the genus, for which the. breeding habitat iswell known (Barker and Starmer, 1982; Barker et al., 1990;although see Markow, 1988). One of four cactophilic Drosophilaendemic to the Sonoran Desert, D. mojavensis, utilizes primarilynecrotic tissue of agria cactus, Stenocereus gummosus, on BajaCalifornia and organ pipe cactus, Stenocereus thurberi, in main-land Sonora, Mexico and southern Arizona (Fellows and Heed,1972; Heed, 1978).

Isolated populations of D. mojavensis show morphological,behavioral and genetic variation, (Mettler, 1963; Zouros, 1973;Etges, 1989 Krebs, 1990), features that have made this organismimportant for studying the evolution of reproductive behaviors andspeciation. Populations on the Baja peninsula and mainlandSonora, Mexico are separated by the Gulf of California, and labo-ratory experiments have shown partial sexual isolation betweenthem (Wasserman and Koepfer, 1977; Koepfer, 1987a, 1987b;Krebs and Markow, 1989).

Despite the great attention given this species for evolutionarystudies, knowledge of its behavior in nature is limited to prelimi-nary tests of dispersal (Johnston, 1974), rearing records fromnecrotic cacti returned to the laboratory (Heed and Mangan, 1986;Ruiz and Heed, 1988), and a brief mention of adult distribution onorgan pipe (Markow and Toolson, 1990). This deficiency led us tostudy the behavior of D. mojavensis on organ pipe and agria cactus

1Current address: Department of Animal Science, University of New England,Armidale, New South Wales 2351, AustraliaManuscript received by the editor December 4, 1990.

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102 Psyche [Vol. 98

to demonstrate that results obtained in the laboratory are applica-ble to populations in nature.

MATERIALS AND METHODS

Observations of D. mojavensis were performed on two popula-tions of the mainland Sonora race. One site was a population ca. 20km south of Ajo, Arizona where organ pipe cactus is plentiful onthe southern and eastern slopes of the St. John the Baptist Moun-tains (the St. John site). A second population was observed thatuses agria cactus in the Desemboque region of Sonora, Mexico,approximately 30 km north of Punta Chueca, across from TiburonIsland.

Drosophila mojavensis adults may be watched easily on theouter skin and within pockets of necrotic cactus arms (rots). Wefound that the number of flies on the necrotic arms varied, as rotsof typical appearance often contained no flies whereas apparentlyless promising rots had many. The number of necrotic arms at theDesemboque agria site was greater than at the organ pipe site, as istypical for these two cacti (Mangan, 1982). More flies were pre-sent at the agria site, but they were spread over many plants. Wefound most flies at a single rot at the organ pipe site.

Observations were recorded periodically through Oct., 1988 toMarch, 1989 (Table 1), during which we made continuous observa-tions on flies for three hours beginning at sunrise (ca. 7 AM) andagain for two hours before sunset (ca. 5:30 PM). Rots were alsoexamined for the presence or absence of flies and courtship behav-ior throughout the day.

Table 1. Number of matings and vertical distribution of copulating pairs ofDrosophila mojavensis along an upright columnar cactus arm.

Number of VerticalDate matings distribution (cm)

10/22/88 13 35

10/23/88 23 50

11/5/88 60 110

11/6/88 22 85

2/26/891 9 25

3/9/89 10

Observations made on agria cactus

1991 Krebs & Bean 103

RESULTS

Courtship behaviorCourtship and mating were common from shortly after sunrise

until 10:00 AM during Autumn to early Spring. On organ pipe, fewflies were observed at rots during the afternoon, and although afew males were observed on rots shortly before sunset (5:00little courtship and no copulations were observed.

Courtship components on the cactus were identical to thoseobserved previously in the laboratory (Markow, 1981). Malescourted females from the rear, while intermittently vibrating one orboth wings. During courtship, the male’s foretarsi drummed contin-uously upon the underside of the female’s abdomen. Successfulmales elicited a characteristic acceptance signal, wing spreadingby the female, that was followed by an immediate attempt tomount. The courtship durations measured in the field ranged froma few seconds to over a minute before female acceptance orrejection.

Female acceptance signals usually led to successful copulation.Of 30 attempted copulations observed, three males failed to copu-late. They fell off the female and dropped to the ground, unable toresume courtship with the same female. During copulation the fliesremained motionless unless greatly disturbed. If other malescourted the copulating pair, the female usually walked away withthe male in copula. We never observed D. mojavensis fly while incopula.

Physical conflict between males was never observed unless twoor more males courted the same female. A male that approached acourting pair would push between them from the side to gainaccess to the female’s ovipositor. The interrupting male initiatedcourtship immediately, ignoring the previous male, but no inter-rupted courtship led to successful copulation.

Mating SystemDrosophila mojavensis males on necrotic cactus arms generally

remain motionless unless disturbed by the arrival of a female.Some males were positioned just within or at the edge of breaks inthe cactus skin that allowed females access to necrotic tissue, butthe majority were distributed across the necrotic cactus arms, farfrom openings to oviposition sites. On agria cactus, we observed

104 Psyche [Vol. 98

some matings on non-necrotic arms, but all observed matings onorgan pipe were on the arm containing the necrotic tissue.A test for random male spacing was performed by overlaying

the positions of males across the cactus arm, determined by pho-tographs (e.g., Figure 1), on a grid. Randomness of male positionswas compared to that expected under a Poisson distribution. Thevariance in male distribution was only 60 percent that of the meanindicating a repulsed distribution. Males were spaced more evenlythan expected by chance.

Although D. mojavensis males present at high densities wereevenly dispersed across the cactus arm, at lower densities maleswere concentrated adjacent to openings to the necrotic tissue. Thevertical distance of an upright cactus arm over which males wereperched, their vertical distribution, was positively correlated withthe number of observed matings (Table 1, r=0.91, P<0.01). For thetwo days with the lowest number of observed matings and foradditional observations of rots with only few males and no mat-ings, most flies remained by the rot entrance. The total number offlies on rots, however, could not be measured because females, andpossibly males as well, continuously arrive and depart during mat-ing periods.

The horizontal distribution of flies was influenced by factorsdifferent from those affecting the vertical distribution. Males wereexpected to wait (1) on the leeward side to intercept landingfemales which presumable fly upwind to the necrotic cactus arm,following volatile cues (Fogleman, 1982) or (2) along the side ofthe cactus arm containing the opening to the rot to more easilyintercept females walking to oviposition sites.

During observations on an arm fully exposed to the sun(November 5th and 6th, beginning at sunrise, ca. 7 AM), half of theobserved matings in the first hour took place in direct sunlight (11of 21, excluding any that occurred within the rot pocket). After8:00, almost all males moved to the shaded side of the cactus and

Figure 1. The distribution of males of Drosophila mojavensis at relatively highdensities on part of an upright necrotic arm of organ pipe cactus (reproduced from aphotograph taken shortly after sunrise, Nov. 5, 1988). As the entire arm rots andturns brown, the spines and areoles may break off, providing possible access to thesoft necrotic tissue, indicated by the small solid black regions in the center. Largerand more accessible openings in the cactus were located on the opposite side.Densely speckled areas on the right represent slowly flowing exudate which is usedas feeding sites on the surface.

1991] Krebs & Bean 105

106 Psyche [Vol. 98

only of 59 observed matings occurred in direct sunlight (G-46.7,P<0.001). In contrast, where a rot was shaded by other arms of theplant (Oct. 22 and 23), all observed copulations (N 36) occurredwithin 5 cm left and right of the only entrance point through thecactus skin, although the vertical distribution of males was muchgreater (Table 1). Temperature and access to the rot were thereforemost important to the distribution of males.

DISCUSSION

Courtship structure of D. mojavensis is similar in the field andin the laboratory. Only the cost to males of failing to successfullymount receptive females is substantially different between the lab-oratory and the field. In the laboratory, failure to copulate afterfemale acceptance is observed for 18 percent of copulationattempts, but males reinitiate courtship and almost always mateeventually (Krebs and Markow, 1989).

Laboratory observations showing an absence of direct male-male aggression, expected where no male size advantage in matingis present (Krebs and Markow, 1989), were supported in the field.More than one male will attempt to court the same female, but con-tact between males appears incidental to gaining access to herovipositor. As observed on the cacti, a female courted by twomales in shell vials will rarely accept a male until one can courtwithout interruption by another male (unpublished data).

Laboratory results showing correlation between courtshiplatency and female locomoter activity (unpubl.) can be explainedby the stationary posture of males at mating sites. On cactus,receptive females are active while sexually ready males are not.

The mating system of D. mojavensis at relatively high densitiesis similar to that of D. nigrospiracula, which has been reported"lekking" on saguaro cactus (Markow, 1988). Drosophilanigrospiracula populations tend to be much larger than those of D.mojavensis, and most matings take place on non-necrotic portionsof the saguaro. Our observations of D. mojavensis, however, sug-gest that the mating system may be labile, and that a resourcedefense mating system based around oviposition sites providesmales with the greatest opportunity for mating when fly densitiesare low.

1991] Krebs & Bean 107

Determination of mating periods may be deceptive in the labo-ratory where mature virgin flies may mate at any time. The matingsites in the field are not occupied throughout the day. Also, obser-vations made during evenings in late spring while collecting flies(Markow, pers. comm.) suggested two daily mating peaks, andmultiple mating within a day are possible for D. mojavensis(Krebs, 1991). Both events, however, are unlikely during seasonsof short day length. Darkness and falling temperatures may reducemating opportunity before females again become receptive aftermating in the morning.

Our observations of D. mojavensis show the importance ofstudying animals within their natural environment even when theycan be easily maintained in the laboratory. Timing of behaviorsdiffers in nature, and behaviors such as number of mating peaks,mate choice, and locomoter activity, are more easily interpretedfollowing even a short field study.

SUMMARY

The courtship behavior of Drosophila mojavensis under fieldconditions was similar to that observed previously in the labora-tory. Males were uniformly spaced across necrotic arms of organpipe cactus when present at high densities, although aggregationswere centered around openings to oviposition sites. At low densi-ties, most males were adjacent to these openings. The two dailymating peaks observed in the laboratory were reduced in the fieldto one during the mornings when day lengths were short.

ACKNOWLEDGMENTS

Previous observations on the behavior of D. mojavensis havebeen made by a number of investigators, Therese Markow of Ari-zona State, Henar Pimentel and Bill Heed at the University of Ari-zona, William Etges at Arkansas, and Tom Starmer of Syracuse.All shared their field experiences which aided our completion ofthis study. This project was supported by a small grant from theArizona State Graduate Student Association.

108 Psyche [Vol. 98

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BARKER, J. S. F. & W. T. STARMER1982. Ecological Genetics and Evolution. The Cactus-Yeast-Drosophila-

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ETGES, W. J.1989. Evolution of developmental homeostasis in Drosophila mojavensis.

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FOGLEMAN, J. C.1982. Mating systems of cactophilic Drosophila, In: Ecological Genetics and

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