The Mating System of Habropoda pallida Timberlake(Anthophorinae: Apidae)

John Alcock & Stephen Buchmann

Revised: 25 April 2011 /Accepted: 5 May 2011 /Published online: 3 June 2011# Springer Science+Business Media, LLC 2011

Abstract Males of Habropoda pallida searched for recently emerged females at alocation in central Arizona where many females had nested in the preceding year.Patrolling males exhibited a variety of mate locating tactics ranging from inspectingexisting emergence holes to patrolling flights around flowering creosote bush. Thesetactics appear to be under the control of a conditional strategy, given that malebehavior shifted during the day. Moreover, some marked males mounted deadfemales placed on the ground in the emergence area as well as mounting deadfemales pinned to flowers in the emergence area and at a creosote bush somedistance away. At least some males exhibited site fidelity in that numerous malesmarked within the nest site emergence area were recaptured there; others marked at acreosote bush were also seen again at that plant. The mating system of the beeinvolves scramble competition with individual males attempting to locate receptiveemerging and flower-visiting females before rival males. In keeping with thescramble competition hypothesis, males are considerably smaller on average thanfemales and are only aggressive when trying to push their way past rival malesalready mounted on a potential mate.

Keywords Alternative tactics . anthophorinae . conditional strategy .Habropoda .

mating system . native bee . scramble competition

J Insect Behav (2011) 24:348–362DOI 10.1007/s10905-011-9261-0

J. Alcock (*)School of Life Sciences, Arizona State University, Tempe, AZ 85287-4501, USAe-mail: j.alcock@asu.edu

S. BuchmannDepartment of Entomology, and Ecology and Evolutionary Biology Department, The University ofArizona, Tucson, AZ 85721, USA

Introduction

The study of the mating tactics of male bees has played a useful role in helpingexplain why animal mating systems are so varied. The pioneering work of Emlenand Oring (1977) established that differential mate-locating tactics employed bymales of different species have evolved in response to differences among species inthe distribution of receptive females available to males. In bees, as well as among thevertebrates considered by Emlen and Oring (1977), differences in female distributionare correlated with differences among species in male mating tactics (Alcock et al.1978). In some bees, for example, males search for emerging females at nesting/emergence sites where large numbers of virgin females can potentially be located(Ayasse et al. 2001; Eickwort and Ginsberg 1980); in many other species, malesdefend or patrol discrete patches of foodplant that attract females after they haveemerged from widely scattered emergence sites (Alcock et al. 1978; (Fraberger andAyasse 2007) or that retain their receptivity after mating (e.g., Rutowski and Alcock1980). Data of these sort provide support for Emlen and Oring’s argument thatvariation in female ecology in conjunction with sexual competition among males hasresulted in differences among species in their mate location and mating systems(Paxton 2005).

Moreover, variation within a bee species in the distribution of receptivefemales appears to promote the evolution of intraspecific variation in male matingtactics (e.g., (Alcock 1997; Leys 2000). This discovery is consistent with the claimthat the ecology of receptive female distribution provides the key to understandingwhy males employ particular mate location and mating tactics. Moreover,information on intraspecific variation in male mating tactics in bees has helpedmake researchers aware that complex alternative mating behaviors occur in insectsas well as birds and mammals (Eickwort and Ginsberg 1980; Thornhill andAlcock 1983).

Here we present an account of male behavior of the anthophorine beeHabropoda pallida with emphasis on the mating system of the species,especially with respect to the variety of mating tactics employed by males.The bee has been the subject of previous research conducted in western Arizonaand California (Bohart et al. 1972; Saul-Gershenz 2010; Saul-Gershenz andMillar 2006). Prior work has established that H. pallida is a univoltine specieswhose females build nests in a variety of soil types. Females can provision theirnests with pollen and nectar from more than one species of foodplant but theyare particularly likely to use pollen from creosote bush (Larrea tridentata).Matings have been observed on the surface of the ground after patrolling maleshave encountered emerging virgin females (Bohart et al. 1972; Saul-Gerschenz2010). Males at the Kelso Dunes in California also are known to fly nearflowering L. tridentata and Astragalus lentiginosus var. borreganus in search ofmates (Saul-Gershenz 2010). Our study of a population of the bee in centralArizona provides data for a comparison with findings made on other populationsat other locations as well as with other members of the genus (Barthell and Daly1995). Our results indicate that the mating system of H. pallida involvesscramble competition among males for access to a variety of spatially distinctpools of receptive virgin females.

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Materials and Methods

The bee H. pallida was studied from March 18 to May 3, 2010 in an open sandyarea (Fig. 1) in the old floodplain of the Salt River near the Blue Point Bridge northof Mesa, Arizona (N 33° 33.151 by W 111° 34.321). Early in this period, malesheavily patrolled a triangular area approximately 23×20×20 m in size that had beenutilized as a nesting area by females the preceding spring. The soil was a clay-richsand that supported some scattered Esteve’s pincushion plants (Chaenactisstevioides), a small annual aster. Other plants at the site included isolated individualsof the Sahara mustard (Brassica tournefortii) as well as a few small patches of exoticred brome grass (Bromus rubens), both introduced species. Surrounding thegenerally open emergence/nesting area were native mesquites and paloverdes(Prosopis velutina and Parkinsonia florida) as well as creosote bush (L. tridentata),ringed by dense stands of Sahara mustard and other non-native plants.

The Blue Point Bridge site was visited on 21 days between March 18 to May 3,generally between 1 to 3 h per day during the morning to early afternoon, although thestudy also included late afternoon visits on 4 days between April 11 and April 27. Onthese visits, males were captured in an insect net or picked off by hand from the back ofdead females that had been frozen, then thawed, before placed in various locations withinthe emergence area and at a nearby creosote bush. These “target” females usually hadbeen collected on previous days, placed in chilled cooler, taken to a refrigerator andfrozen prior to being returned to the study site for use in experiments designed todetermine whether males flying over the emergence area and around creosote bushwouldapproach and mount these females in the same manner as males searching for mates.

Captured males had their head-widths measured using a pair of Helios dialcalipers; head-width is highly correlated with body weight in other bee species (e.g.,(Alcock 1996; Stubblefield and Seger 1994).

In order to determine whether male body size was correlated with the mate-searching tactic employed by males, samples of males were collected by sweepingup patrolling males flying low over the emergence area on March 28 and April 3 andby capturing males attracted to target females in this area as well as at a creosotebush nearby that was patrolled by males as well.

Fig. 1 The open emergence/nesting area in the old flood-plain of the Salt River near theBlue Point Bridge

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After the head-widths of captured males were measured, males were given adistinctive paint mark using extra fine point DecoColor paint pens. Whenevermarked males were observed or recaptured on subsequent days, a record was madeof the identity of the individuals.

As the season progressed and the number of nesting females increased, patrollingmales appeared to focus their searching efforts on inflorescences of C. stevioides ratherthan searching for females on the ground, perhaps because these individuals were morelikely to be unreceptive nesting females rather than recently emerged virgins. To testwhether males did have searching preferences, on April 6 (when the number of activenests exceeded 90), we took one target female and placed her on the ground by aflowering C. stevioides and then on the flowerhead itself, or vice versa, alternating theorder of presentations on each double trial (n=10). We noted whether the target femalewas approached, touched or mounted by a patrolling male during a 60 s period. Thedata permit a comparison of the attractiveness of a potential mate in the two locations.

Results

Activity During the Flight Season

On 18 March, a handful of small circular emergence holes were found in the soil inwhat had been a nesting area of H. pallida during the previous spring. The holeswere made by bees as they dug their way up to the surface after having eclosed asadults within their underground natal cells. By late March, when there were manymore emergence holes, males were observed in small numbers flying low (usually5–20 cm over the ground) in locations where these holes occurred. On March 21, 26,and 27, the first male patrollers were not seen until after 0930 M.S.T. The firstnesting female was observed on March 22; the number of such females hadincreased slowly to nine by March 27, by which date dozens of male patrollers wereactive in this clearly protandrous species.

The site was not monitored again until April 3, at which time 76 nests were countedin a circuit of the emergence/nesting area. The count increased to 90 nests by April 4.The total number of nesting females continued to grow so that by mid-April the numberof nests was estimated to be at least 200. Nesting continued through May 3.

At the Blue Point site, females relied heavily on creosote bush pollen and nectarwhen provisioning their nests, and indeed nesting appears to have been synchronizedwith the phenology of creosote bush flowering. Although on March 27, only one of12 creosote bushes located within a few hundred meters of the emergence/nestingarea had open flowers, by April 3, eleven of 12 creosotes were in flower to at leastsome degree. These bushes became covered with flowers soon thereafter and heavyflowering continued before tailing off in late April and early May.

Alternative Mate-Searching Tactics of Males

Male Tactic 1: Males flew slowly in circuitous routes within a few centimeters of theground. When in this search mode, males sometimes flew to and hovered by orlanded next to burrow openings made by emerging bees (Fig. 2), usually stopping

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only for a second or two before continuing on, often to land by or hover over anothernearby emergence tunnel for a moment before flying further. Early in the flightseason, repeated inspection of the same set of emergence holes occurred often. Forexample, on March 25, a set of four emergence holes was visited in total 49 times bya number of males during 20 min of observation between 1200 and 1300. As theflight season progressed, the inspection of old emergence holes stopped by mid-morning (Fig. 3) as the males switched to tactic 2 (see below).

Rarely, a male would crawl into the old emergence hole and remain inside brieflyafter entering before exiting (Fig. 4a). On another occasion, a male was seen mountedon a female (Fig. 4b). On other occasions, males appeared to dig briefly at an existingemergence hole. On March 25, after a male scrabbled at an emergence hole at midday,another male came out of the tunnel, followed by a female, which immediatelyattracted a ball of three males, one of whom presumably inseminated the female. Theclusters of males that formed around a female on the ground lasted only a short time;in 4 cases, the duration of the multi-male cluster ranged from less than 15 s to 63 s.After the group disbanded, one male remained mounted on the female for a shortperiod before flying off. Copulation was difficult to observe because of the frenziedbehavior of the males surrounding a female (Fig. 5) and the apparent rapidity withwhich mating occurred (averaging 3 s in 3 timed recorded cases).

Fig. 2 Males of H. pallidahovering by emergence holes inthe emergence/nesting area at theBlue Point Bridge site

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Fig. 3 The number of timesmales of H. pallida landed atthe edge of six emergence holesduring 20 min observation peri-ods, which began on the half-hour as early as 0930 M.S.T. onthe days of April 3–5

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Males were also seen digging briefly at two emergence holes from which fellowmales exited; two balls composed entirely of males were seen on the ground,suggesting that emerging males could trigger sexual responses in patrolling males.These observations suggest the function of tactic 1, which appeared to enable males

Fig. 4 a A male that had beencaptured and marked previouslyon the thorax was later observedentering and leaving a emer-gence tunnel, presumably insearch of an unmated femalewithin the tunnel. b A male ofH. pallida mounted on a femalewithin the exit of an emergencetunnel

Fig. 5 A group of males com-peting with one another for afemale on the ground whileanother male hovers near thecluster prior to diving into themelee

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to locate receptive virgin females that were using existing emergence tunnels toreach the surface.

Male Tactic 2a: A second mate-searching tactic involved apparently continuousflight low over the ground. Males in this mode (rapid patrolling) flew swiftly lowover the emergence area without stopping at emergence holes. Counts made of beesflying straight and fast over a 40 cm long line in the emergence area increased frombetween 11 and 14 per min (at around 0930 on April 4 to 6) to from between 24 and41 per min (at around 1030 on these days). The increase in rapid patrollers duringthe morning coincided with a decrease in the frequency with which emergence holeswere visited by slow patrollers (see Fig. 3).

Rapid patrollers were responsive to freshly emerged individuals discovered byother males on the surface of the soil. Patrolling males quickly formed clusters ofcompetitors around apparently recently emerged individuals. Six mating ballscontaining a female and four or five males were observed on the ground in theemergence area between March 26 and March 28. Many other males (up to about adozen) were attracted to some of these groups.

In addition, three recently mated females were captured, frozen overnight, andthen returned to the bee site to be placed on the ground in the emergence area on themornings of March 27 and 28 as well as on April 4. These presentations of thawedfemales (n=8) quickly attracted the attention of patrolling males, at least one ofwhich mounted the target female within 40 s in every case. In five of thepresentations, several males reached the female nearly simultaneously and allattempted to grasp her at the same time, leading to the formation of a group of malesclustered around the female.

Male Tactic 2b: Rapid patrollers also inspected scattered flowering plants as theyflew over the emergence/nesting area. These bees ascended some 10 to 20 cm asthey approached a flowering C. stevioides or desert chicory (Rafinesquia neo-mexicana). As they swerved up from their flight path, the males would pass within afew cm of the flowerhead, sometimes even touching the flowers, or slowingmomentarily in flight near the inflorescence before descending to cruise off low overthe soil surface once again. The frequency with which these flowerhead approachesoccurred also increased over the course of the morning (Fig. 6) in conjunction with adecrease in the frequency of emergence hole inspections.

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Fig. 6 The number of times apatrolling male H. pallida altersits flight path to closely ap-proach an inflorescence of anisolated Chaenactis stevioides inthe emergence/nesting area dur-ing one-min samples at differenttimes of the day on March 27–28and April 3–6

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Although a few males landed on an unoccupied flowerhead and spent a short timethere, apparently foraging for nectar, these events were very rare. Instead thefunction of flowerhead inspections appeared to be to locate mates as was partlyrevealed by observations of patrolling male H. pallida striking and immediatelyreleasing honey bees (Apis mellifera) and conspecific males as they perched on C.stevioides (n=3). These apparent mistaken pre-mating contacts demonstrated thesexual motivation of the males as did experiments in which dead females collectedand frozen on previous days were placed on or pinned to an inflorescence of C.stevioides within the emergence area. In the late morning on April 4, 5, and 6, fivedifferent target females were placed in sequence on five different inflorescences ofC. stevioides for a total of 25 presentations. In 23 cases, a male H. pallida mountedthe target female (Fig. 7a) in less than a minute (18.0 s on average) and attempted tomate with her. In some cases, two or even three males landed on the female and eachother nearly simultaneously (Fig. 7b). In contrast, dead, frozen and thawed male beeswere never mounted during 15 presentations of three different target males, althoughon 11 trials the target bee was briefly touched by a flying male, which immediatelyresumed its patrol route.

Over the course of the study, males mounted dead females on flowering C.stevioides from as early as 0910 to as late as 1750 M.S.T.

Male Tactic 3: In addition to the mate-searching tactics exhibited in theemergence area, males also flew rapidly around flowering creosote bushes locatednear the emergence/nesting site. Between April 5 and April 14, a total of 33unmarked males were captured and marked at one creosote bush growing 35 m fromthe emergence area. Between 11 April and 14 April, dead females pinned to flowersabout 1.5 m high in the shrub were approached and mounted 37 times (Fig. 8).Males continued to patrol at least one creosote bush as late as May 3 when twomounts by two different males were recorded in a 20 min sample period.

Identification of Potential Mates by Patrolling Males

Early in the flight season (late March), males appeared to be searching primarily forrecently emerged females, which they located either as these exited from establishedemergence tunnels or by rushing to females on the ground that had just been foundand mounted by other males. Their response to nesting females, which presumablyhad been mated before beginning to dig a burrow, was very different. On March 21,when one of the very few nests under construction then was observed, we noted thatmales often altered their low patrolling flight to approach the nest entrance and thelow mound of fresh dirt excavated from the burrow. These approaches occurred atotal of 118 times during three 10-min observation periods distributed between 1025and 1325. The inspecting males flew upwind toward the nest entrance, sometimescircling back toward the entry to the burrow, occasionally hovering for a momentthere, even very briefly dropping down to touch the soil at the entrance beforecontinuing. In so doing, they at times encountered the female as she pushed soilfrom a burrow that was being constructed. Although males sometimes hovered a fewcm behind a digging female, they never struck or mounted her. This pattern persistedthroughout the study: females pushing dirt from a burrow entrance (Fig. 9) werenever touched by patrolling males.

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It is curious that males did not attempt to grasp nesting females given that whenfemales were frozen after having been captured incidentally during sweeps of theemergence area, these dead females, which were assumed to have been mated and tohave been nesting when captured, often were highly attractive (when thawed andplaced in the nesting area) to mate-searching males. For example, on April 6, when

Fig. 7 a A male attempting tocopulate with a dead, frozen andthawed, female placed on aflowerhead of Chaenactis ste-vioides. b A second male arrivedsoon after the first male foundand mounted the target female,creating a stack of three bees

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creosote bushes were flowering profusely and many females were nesting, a female thathad been collected during a sweep of the nesting area was thawed and placed alternatelyon the ground near a flowering C. stevioides, or on the flowerhead of the plant itself inalternating sequence (10 paired trials at different locations within the emergence area).Every presentation of the female on an inflorescence generated a mounting within 60 swith a mean time to attempted copulation of 22.8±13.9 s (n=10). In contrast, onlyfour of the 10 presentations of the same dead females placed on the ground elicited amounting (Fisher’s exact probability=0.01), although during three other such trials amale struck the female (that is, he made contact with the female but flew offimmediately).

Fig. 8 A marked male of H.pallida that has just landed onthe back of a dead, frozen andthawed female pinned to aflower of creosote bush(L. tridentata)

Fig. 9 A nest-constructing fe-male in the midst of pushingexcavated dirt away from herburrow. This behavior exposedthe female to patrolling malespassing nearby, but althoughthey often approached femalesof this sort, they did not attemptto copulate with nest-buildingindividuals

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Thus, males seemed less responsive to females placed on the ground whilefinding females pinned to flowers more sexually attractive. Over the next severaldays, females pinned to C. stevioides continued to be approached and mounted bylow-flying males in the emergence area. In a 20 min period from 1630 to 1650 M.S.T. on April 11, one thawed nesting female that had presumably been mated wasmounted by ten different males (and struck eight times as well).

During the first two weeks of April, as the local creosote bush produced more andmore mature flowers and the number of nesting females peaked, dead females usedas targets for patrolling males also elicited copulatory attempts when pinned to theflowers of L. tridentata (these females had also been collected from the nestingarea). A female of this type pinned to creosote bush flowers on the afternoon ofApril 11 generated 14 mounts (copulatory attempts) and two strikes. On thisafternoon, the same female when pinned to a pincushion inflorescence elicited 10mounts and 8 strikes.

By mid-April, males had ceased to patrol C. stevioides in the emergence/nestingarea and shortly thereafter, mate-searching activity at creosote bush also declined toa very low level (Fig. 10). Between April 15 and May 3, when females pinned on alarge flowering creosote bush elicited no more than two mounts per 20 min trial,many females were digging their burrows and provisioning brood cells in the nestingarea. In one approximately 5 m square section of the emergence/nesting area,between 4 and 24 females were seen entering their burrows daily during 20 minobservation periods on 7 days between April 15 and April 27. From 4 to 14 of thesefemales clearly had pollen loads, and so were provisioning nests at this time. Thus,nesting extends past the intense mate-searching phase of the flight season.

Site Fidelity of Mate-Searching Males

Some males captured and marked in both the emergence area and at the nearbycreosote bush were recaptured or seen again on another day or days during the study.Of 100 males marked at the emergence area between 25 March and 12 April, 44were recaptured, 16 of which were taken on 3 or more days. Indeed, four individualswere found within the emergence site on at least 4 days during the study. One ofthese frequently resighted males was marked with a blue dot, and this male appeared

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Fig. 10 The number of males ofH. pallida captured during twoalternating 20 min blocks in theperiod from 11 April to 18 April.The males were captured as theymounted dead pinned females atinflorescences of C. stevioides inthe emergence area (dotted line)or at flowers of L. tridentata(solid line)

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over and over again within a roughly 5 m square section of the emergence area onfour consecutive days starting on March 25. Blue dot repeatedly inspected aparticular set of emergence holes within his habitual patrol route. He was recorded aspresent from 8 to 11 times per day over periods of 2 h or more beginning as early as0952 and ending as late as 1302.

Among the recaptured males taken in the emergence site were some individuals thatapproached or mounted females pinned to C. stevioides flowers on several differentdays. So, for example, of the 14 males captured as they approached or tried to copulatewith a female on a pincushion flower in the emergence area on April 12, eight hadbeen captured previously in this area as they engaged in the flower-visiting tactic.

Likewise, certain males (13 of 32) were recaptured or resighted at the creosotebush where they had been originally netted. Five of these were recorded as presenton at least three days during the study with a maximum interval between first andlast encounter of 8 days.

Six marked males mounted pinned dead females at both the emergence area andthe creosote bush, demonstrating that at least some individuals could search forreceptive females in these two different locations.

Discussion

The Mating System of H. pallida

Males of H. pallida, like males of many other bees whose females nest in relativelydense aggregations (Alcock et al. 1978), can and do search for receptive virginfemales emerging from the nesting area of the previous flight season. This tacticmakes intuitive sense considering that many potential mates will emerge from withina relatively small area. But unlike some members of this group of solitary bees,males of H. pallida exhibit very little territorial aggression toward conspecific malesbut instead appear devote their efforts almost exclusively toward being the first maleto reach a potential mate. All observers of this species have seen groups of males(“mating balls”) clustered around a presumptive virgin female on the ground (Bohartet al. 1972; Saul-Gershenz 2010), which probably form when a recently emergedfemale is discovered by one male just before other males join the pair. Althoughaggressive competition surely occurs in these tumbling balls of males, these groupsdisperse quickly, apparently disbanding shortly after the located female hascopulated, an event that takes only a few seconds in H. pallida, as also noted byBohart et al. (1972) and Saul-Gershenz (2010).

In contrast, males of another ground-nesting bee (Centris pallida) found in theBlue Point area regularly fight for several minutes over small sites from which virginfemales are about to emerge (Alcock et al. 1977). In this species, males that are ableto prevent others from reaching an emerging females either before she has emerged,or by taking her away from a ball of competing males, can complete withoutinterference a post-insemination interaction of several minutes, which usually takesplace in a tree or shrub to which the male flies carrying his partner (Alcock andBuchmann 1985). Females of this species that do not receive the post-copulatorycourtship (Eberhard 2009) remain sexually receptive.

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The extremely rapid copulations of H. pallida and the apparent absence of a post-insemination courtship signal phase are indicative of a rapid loss of receptivity byfemales once they have mated. In monandrous species (and most solitary bees arethought to fall in this category (Paxton 2005)), male searching efficiency andpatrolling stamina should be at a premium, which selects against large body size andaggression, particularly in areas where many other males are engaged in a race tofind receptive females. Indeed, the evolution of scramble competition polygyny isassociated with a sexual dimorphism in body size in which males are smaller thanfemales (documented for H. pallida by Saul-Gerschenz 2010 and for the Arizonanpopulation as well; unpubl. data). In addition, scramble competition polygyny islinked to either a dispersed distribution of potential mates (e.g., Seidelmann (1999))or such high densities of competing males as to make aggressive territorial defenseextremely costly (Thornhill and Alcock 1983).

Alternative Mate-Searching Behaviors of Male Habropoda pallida

Although the mating system of H. pallida can be labeled scramble competitionpolygyny, conspecifics males compete for mates using quite different tactics, aconclusion also reached by others (Bohart et al. 1972; Saul-Gerschenz 2010). Withinthe emergence/nesting area, males often patrolled slowly, interrupting their flight toinspect existing emergence holes from which fresh adult females might emerge, atactic known to occur in other anthophorine bees (Barthell and Daly 1995; Alcock1997). Alternatively, males of H. pallida sometimes engaged in rapid, low,uninterrupted flight, presumably in part as an effort to reach females on the groundthat had been discovered by other males. Rapid patrollers also frequently flew upshort distances to inspect the flowers of annuals in the emergence area and werequick to mount dead females pinned on these plants. The same was true for malesthat circled around the perimeter of flowering creosote bush plants.

Although only a few complete matings were directly observed during this study,those that occurred on the ground almost certainly involved freshly emerged females.Matings of this sort and the formation of frenzied groups of males around females on theground have been reported by others who have studied the bee in western Arizona andCalifornia (Bohart et al. 1972; Saul-Gershenz 2010). The same pattern has beenrecorded for other members of the genus Habropoda (reviewed by Barthell and Daly(1995)). In addition, Saul-Gershenz and Millar (2006) and Saul-Gershenz (2010) haveseen males attempting matings with females visiting flowering A. lentiginosus var.borreganus while also observing mate-searching males at flowering creosote bush.

The variety of mating tactics exhibited by males of this species suggests thatreceptive females can be found in several different locations, each one of whichrequires a somewhat different mate-searching tactic. Freshly emerged virgin femalescertainly provide a major pool of potential mates. The fact that males also obviouslysearch for females later in the flight season after many (if not all) females haveemerged and have begun nesting has been taken to mean that mated females mayretain or regain their receptivity at some point (Saul-Gershenz 2010). Indeed, Bohartet al. (1972) reported that males pounce upon all females encountered, which wouldsuggest that mated females may at least occasionally receive sperm from more thanone male. In addition, the fact that males at the Blue Point site responded sexually to

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dead females originally captured in the nesting area, where they almost certainly hadbeen mated before beginning to nest, is further evidence that females other thanvirgins attract mate-searching males.

On the other hand, we, unlike Bohart et al. (1972), never observed malesmounting (or even striking) living females active on the ground at the nesting site, afinding that Saul-Gershenz (personal communication) confirms for the populationthat she studied. If some nesting females were truly receptive, one would expectmales to attempt to mate with females in this behavioral category. Moreover, onewould also predict that the male searching season and the female nesting seasonwould overlap more or less completely, but this species is protandrous as are othermembers of the genus (Barthell and Daly 1995). Moreover, although it is true that afew males continued to respond to dead females pinned in flowering creosote bushas late as May 3, male mate-searching activity in the emergence/nesting area endedsome weeks before the end of the nesting season. It seems likely that virgin femalesare the primary category of potential mates for males of H. pallida.

It remains puzzling, however, that dead pinned females known or suspected ofhaving been nesting (and, thus, of having been already mated) remain attractive topatrolling males of H. pallida as they search for mates at flowers within and outsidethe emergence area. Do living females actively produce and release a repellentpheromone that dead females cannot offer? Or are males responding to behavioralcues (such as those provided by living females that are digging or foraging) to avoidalready mated females, the better to concentrate on finding receptive (virgin?) females.

In any event, males of H. pallida provide another example of a bee species withhighly specific alternative mating tactics (Alcock 1997; Alcock et al. 1977; Barrows1983; Barthell and Baird 2004; Simmons et al. 2000). In most previously studiedcases, researchers have concluded that the various mating tactics are under thecontrol of a conditional strategy (Gross 1996), which enables individuals to adjusttheir mate-searching behavior in response to variation in environmental conditions,including their social environment. Males of H. pallida make these adjustments asindividuals switch from inspecting fresh emergence holes to visiting floweringannuals over the course of a morning, perhaps as emerging females become lesslikely to be discovered by males examining old emergence tunnels. More evidencefor conditional mate locating comes from the discovery of a few males that patrolledboth the emergence area as well as creosote bushes. Although the mating system ofthe bee can be given a single label, scramble competition polygyny, the manner inwhich males attempt to outrace competitors to potential mates varies over the courseof a day and over the flight season as a whole.

Acknowledgements We received generous assistance from Leslie Saul-Gerschanz who shared herknowledge of Habropoda pallida with us and who commented on the manuscript.

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