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Female Foraging and Intranest Behavior of a Communal Bee,Perdita portalis (Hymenoptera: Andrenidae)

BRYAN N. DANFORTH1

Snow Entomological Museum, Department of Entomology,University of Kansas, Lawrence, Kansas 66045

Ann. Entomol. Soc. Am. 84(5): 537-548 (1991)ABSTRACT Female Perdita portalis Timberlake are ground-nesting, partially bivoltine,communal bees that inhabit the deserts and arid grasslands of Arizona, New Mexico, andnorthern Mexico. From 2 to 29 adult females may share a single nest. Nests are commonlyreused from year to year and may become very large, with >200 overwintering prepupae,although some new nests are started each year. By constructing artificial, below-groundobservation nests, it was possible to observe the details of cell provisioning and of female(and male) nestmate interactions within the nest. The details of cell construction, pollencollection, pollen ball formation, and oviposition are described. There was no evidence ofcooperation among female nestmates or reproductive division of labor, nor was there anyindication of intraspecific cleptoparasitism. The behavior of female P. portalis is comparedwith the behavior of females in other species of Perdita and with what is known of theintranest behavior of other bees.

KEY WORDS Insecta, Perdita portalis, nesting behavior, sociality

THE GENUS Perdita contains >600 species of smallto minute bees which are most common in the aridsouthwestern United States and northern Mexico.All species studied to date excavate nests in theground, which consist of tunnels leading to cellswhere pollen and nectar are stored for larval de-velopment. Most species are narrowly oligolectic,usually restricting pollen collection to a small groupof closely related plants. Rozen (1967) and Dan-forth (1989) review the published information onPerdita nesting behavior.

Although in many species of Perdita each nestcontains just one female (e.g., P. octomaculata (Say)[Eickwort 1977]), several species are communal,with >30 adult females per nest: e.g., P. texanaCresson (Neff & Danforth 1991); P. opuntiae Cock-erell (Bennett & Breed 1985, Custer 1928); P. mel-lea Timberlake (J. G. Rozen, Jr., personal com-munication); P. latior Cockerell (J. G. Rozen, Jr.,personal communication); P. coreopsidis Cockerell(Danforth 1989); P. lingualis Cockerell (Michener1963); and P. portalis. Communal nesting by fe-male Perdita raises a number of questions abouthow females interact behaviorally within nests. Dofemales cooperate in any aspect of nest construc-tion, maintenance, defense, or foraging? Is therereproductive division of labor? In communal nests,females have access to the fruits of each others'labor (the pollen and nectar needed for larval de-velopment). Does cell robbing or cleptoparasitismoccur under such circumstances? And finally, do

1 Current address: Department of Entomology, National Mu-seum of Natural History, Smithsonian Institution, Washington,D.C. 20560.

the intranest interactions among nestmates shedlight on theories of social evolution (Lin & Mich-ener 1972, Eickwort 1981)? To answer these ques-tions, one must observe females under seminaturalconditions within nests. This paper outlines the ba-sic natural history of P. portalis and presents thefirst observations on intranest behavior of a com-munal andrenid bee.

Although the behavior and morphology of fe-male P. portalis are similar to those of many of itsclose relatives, the males of this species are highlyunusual in having two discrete morphs differing inboth structure and behavior. One morph is capableof flight, is relatively small-headed, and is foundregularly on Sphaeralcea St.-Hilaire (Malvaceae)flowers, where they mate with foraging females.First discovered by Rozen (1970), the other (de-rived) morph is strikingly modified, as judged bycomparison with related bees, possessing a greatlyenlarged head, enlarged facial foveae, reducedcompound eyes, elongate pointed mandibles, athree-pronged clypeus, and reduced thoracic mus-culature which renders them flightless and restrict-ed to a life within the natal nest. Unlike most ofits close relatives, which vary continuously in headsize, albeit with strong positive allometry (e.g., P.texana), the males of P. portalis are truly dimor-phic. A detailed description of male intranest be-havior and comparison of the two male morphs ispresented elsewhere (Danforth 1991).

Materials and Methods

Perdita portalis has been collected from north-central Arizona east to the southwestern corner of

0013-8746/91 /0537-0548$02.00/0 © 1991 Entomological Society of America

538 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 84, no. 5

New Mexico (Hidalgo, Grant, and Luna counties)and south to Zacatecas state, Mexico (Timberlake1954, 1968). Adult foraging is restricted to speciesof Sphaeralcea.

This study was conducted at a locality 2 km northof Rodeo, Hidalgo County, where ~10 nests in1987, 24 nests in 1988, and 33 nests in 1989 werelocated. Nests were also found at other localities:30 km north of Hachita, Grant County (1988) and9.2 km east of Animas, Hidalgo County (1989). Alllocalities were mixed Chihuahuan desert-grasslandhabitat with scattered Sphaeralcea plants, the solesource of pollen and nectar for this species. Sphaer-alcea subhastata Coulter predominates at the Ro-deo locality and S. angustifolia (Cavanilles) at theAnimas locality. All nests were found in patches offine claylike soil devoid of vegetation.

Nests 2 km north of Rodeo were mapped in 1988and 1989 to determine the frequency of nest reuseand new nest founding from year to year. As atthe other localities, nests were located only in areasof exposed soil devoid of vegetation. Five suchareas were found on the west side of a dirt roadthat extended northeast from Highway 80 to a cattletank and a wind-operated water pump. The fivepatches together stretched «110 m. To map nestsaccurately, a metal stake was placed roughly at thecenter of each of the five areas and all nests weremapped with respect to the central stakes. Themetal stakes were then mapped with respect toeach other. Mapping was done using a hand-heldcompass and a 50-m measuring tape.

Nests were excavated by blowing a fine mist oftalcum powder down the tunnels and carefully dig-ging away the soil with a penknife. Care was takento excavate nests early or late in the day or oncloudy days to ensure that all resident bees wouldbe present. Larvae and pupae were placed in 96-well tissue culture dishes for rearing in a laboratoryincubator at 30°C and 100% RH.

The body weights of adult bees and pollen ballswere measured after they had been dried for atleast 2 d at 55°C (dry weight). Prepupae (postdefe-cating, last instars) were weighed live. Weights weremeasured to the nearest 0.01 mg.

Observation nests, similar to those used to studyintranest behavior in Lasioglossum zephyrum(Halictidae) (Michener & Brothers 1971), wereconstructed in the following way. Each observationnest consisted of a thin layer of soil sandwichedbetween two transparent red Plexiglas plates, witha soil thickness equal to the diameter of tunnelsand cells in natural nests (2.2-2.5 mm in diameter).A length of 16-gauge electrical wire with plastichousing was glued to the surface of a rectangularpiece of Plexiglas (20.3 by 40.6 cm) with clearsilicone glue to form an enclosure (Fig. 1A). Ap-proximately 1 cm was left between the wire gasketand the edge of the Plexiglas all the way around,and a gap of «0.5 cm was left between the endsof the wire at the top of the Plexiglas plate. Siftedsoil from the Rodeo locality, moistened slightly,

was gently packed into the wire enclosure on thePlexiglas plate with a rolling pin. When the soilwas packed tightly enough that tunnels could becut into the soil with a razor blade, no more soilwas added. A simple system of tunnels and cells,with one main tunnel leading to the opening at thetop of the plate connected to laterals leading tocells, was cut into the packed soil surface (Fig. IB).Pupae were then placed into the artificial cells withtheir heads facing toward the main tunnel. From2 to 10 female pupae were placed in each obser-vation nest and, in some nests, 1-6 male pupae.Finally, another rectangular piece of red Plexiglasof the same size was placed on top and clampedinto place with 5.1-cm (2 in.) paper binder clips(Fig. 1C). It was important to clean the surface ofthe wire gasket before attaching the top plate toensure a tight seal between plate and gasket. Nestswere kept upright in an incubator at 30°C for 1-2 d before they were placed in the field.

In this study, unlike previous studies of halictinebees in which observation nests were placed inindoor flight rooms (Batra 1964, 1968, 1970; Stock-hammer 1966; Kukuk & Schwarz 1987,1988), nestswere placed in the field so that bees could forageunder natural conditions (Fig. ID). To do this, ahole (1.5 m deep, 1.5 m wide, 2 m long) was dugat the Rodeo locality and covered with a 1.9-cm(% in.) plywood top fitted with a trap door (Fig. 2).Four slots (1.0 by 20.3 cm) were cut along one edgeof the plywood top into which the uppermost edgesof the observation nests could be fitted. The nestswere supported from beneath by a wooden shelf.The entire plywood lid (except the trap door) wascovered with a thin layer of soil.

When adult bees eclosed in such nests, they fol-lowed the artificial main tunnel and then dug theremaining 3-4 cm of soil to the surface. In 1988,seven nests were constructed and three were even-tually accepted by at least one female and onemacrocephalic male. In 1989, six nests were con-structed and three were accepted by at least onefemale. Large-headed males were deliberately ex-cluded from the 1989 nests to observe female be-havior in their absence: a situation like that in new-ly initiated nests before the emergence of the firstmacrocephalic males. Observation nests containedat most six adult females and four adult macro-cephalic males. Fifty-six cells were completed inthe six successful observation nests. In one nest, asingle cell was completed by the solitary femaleresident; whereas, in another nest, 24 cells werecompleted by six female residents.

During the periods of observation, usually from0900 to 1500 hours (PST), the behavior of all fe-males and males in observation nests was recorded.For females, I recorded the times of departuresfrom the nest, returns with and without pollen, cellconstruction, pollen ball formation, egg laying, andmating within the nest. For males, I continuouslyrecorded their behavior and location within thenest (either at the nest entrance, in the main tunnel,

September 1991 DANFORTH: FEMALE FORAGING AND BEHAVIOR OF Perdita portalis 539

k.

Fig. 1. Observation nest construction. (A) Two pieces of Plexiglas; lower piece with gasket glued to surface.(B) Soil rolled into lower Plexiglas plate and artificial nest tunnels and cells constructed. (C) Upper plate clampedinto place. (D) Observation hole surrounded by barbed wire fence at Rodeo locality.

in lateral tunnels leading to open cells, or in cells),and when mating and male-male fighting oc-curred. In addition to this continuous record, I re-corded the position and activity of each bee in the

nest at 10-min intervals throughout the observationperiod (scan sampling of Altmann [1974]). Eventswere recorded to the nearest second with a hand-held tape recorder. A total of 69 h of observations

Fig. 2. Below-ground observation nest box at the Rodeo locality showing four active observation nests.

540

Table

Nest

87-188-188-388-488-588-1289-1189-1589-1789-5089-51Total

ANNALS OF

1. Nest excavation

Dateexcavated

31 Aug.3 Aug.

18 Aug.18 Aug.27 Aug.3 Sept.

14 Aug.21 Aug.26 Aug.6 Sept.8 Sept.

Eggs &feedinglarvae

2322

30

6430

025311524

—

data

THE ENTOMOLOGICAL

Cell contents"

Pre-pupae

11105

137

415792

>11281

187

—

Pupae

06

18085

746400

—

Total

3413334

711392

166>143

4316

211

—

99

511——1032

2129105

—

SOCIETY

Adultsb

Large-headed

66

112——

632

26001

—

OF AMERICA

Small-headed

66

01

——

0003000

—

99

—1413—

54

331410

75

Vol. 84,

Broodc

Large-headed

66

—66

—30

211500

42

Small-headed

66

—30

—52

148600

38

no. 5

——————11

1———

12

a Contents of cells at time nest was excavated.b Number of adults collected in the nest at the time the nest was excavated.c Sex and morph of brood collected at time of excavation and those later reared to pupal or adult stage in the laboratory.^ Number of males for which morph type was not determined.

was recorded (1988, 45.5 h; 1989, 23.5 h), plusunrecorded time spent studying nest constructionand larval development.

Voucher specimens have been deposited in theSnow Entomological Museum, University of Kan-sas, Lawrence.

Results

Nest Occupancy and Structure Based on Ex-cavations. P. portalis is a communal bee with from2 to 29 adult females and up to 26 adult macro-cephalic males per nest (n = 9 active nests exca-

30

20

10

0 •

88-I

/ * 8 9 - l l * e 9 . 5 l A

' 1- H

• 8 9 1 5 / /

88-5

8 9 - 5 ° 89-,7*1 1 1 ^

10 15 20

NO. FEMALES/NEST25

Fig. 3. Relationship between number of macroce-phalic males and number of females per nest in nestsexcavated in 1987-1989 (n = 9 nests fully excavated).Solid line indicates equal numbers of males and females.Old, persistent nests are shown with closed circles; newlyinitiated nests are shown with triangles.

vated) (Table 1). Small-headed males were foundin two nests, but they were probably recentlyemerged bees which had not yet left the nest. Nosmall-headed males remained in observation nests.

There is evidence that the number of macro-cephalic males per nest is correlated with the num-ber of adult females per nest (Fig. 3). If we excludenests 89-17 and 89-50 (because, from the smallnumber of prepupae, they appear to be newly ini-tiated), in the remaining seven nests the numbersof males and females per nest are significantly cor-related (p = 0.977, P < 0.01; Spearman's rankcorrelation coefficient) and appear roughly equal.

Fig. 4 shows three typical nests of P. portalis.All nests were quite shallow, extending no deeperthan «15 cm, but some nests were complex, with>200 cells occupying an area 20 cm in diameter(Table 1). Main tunnels usually extended straightdown and were not filled with loose soil. Cells werecoated with a waterproof lining, as in some otherpanurgine bees (Rozen 1967), but pollen balls lackedthe shiny hydrophobic coating present in some spe-cies of Perdita (Danforth 1989). All nests lackedtumuli, and entrances remained open throughoutthe nesting period. Based on nest excavations, itappeared that in the largest nests, each female oc-cupied her own lateral burrow because each lateralended in a group of recently constructed cells anda single adult female.

Nest Persistence from Year to Year. All evi-dence indicates that nests of P. portalis are reusedfor several generations and persist for extendedperiods of time. The number of completed cells innests can be quite large, in excess of 200 in somenests (Table 1). Bees overwinter as prepupae, andmost cells in larger nests contain prepupae (e.g.,

Fig. 4. Nests of P. portalis. Letters refer to cell contents: e, egg; s, small larva; m, medium-sized larva; 1, largelarva. Unlabelled cells contained defecated prepupae, and cells connected to open lateral tunnels were partially


Nest 89-50 Nest 87-1

provisioned. These three nests show the presumed ontogenetic development of nests: 89-50 represents a newlyinitiated nest before the emergence of macrocephalic males; 87-1 represents a newly founded nest at the end ofthe first season (five adult females were collected returning to the nest with pollen loads; note five partially provisionedcells); 89-51 represents an old, persistent nest which contained primarily diapausing prepupae.


nest 89-51). Evidence from excavations of neststhroughout the season and the rearing of larvaeand pupae in the laboratory suggest that all over-wintering prepupae do not eclose in the same year.For example, nest 89-11, which was excavated atthe start of the 1989 nesting season, contained afew adults and many pupae and overwintered pre-pupae. Only 12 of the 92 prepupae pupated in thelaboratory during that summer; the remainder per-sisted as viable diapausing prepupae at least throughMarch 1991. This suggests that only a fraction (per-haps half) of the overwintering prepupae pupatein any year, and most do so early in the season. Asnests were dug later and later in the season in 1989,the number of pupae found dropped to zero (e.g.,nests 89-50 and 89-51, both excavated in early Sep-tember). Other nests with large numbers of over-wintering prepupae (e.g., 88-1 and 89-15) show thesame pattern: only small proportions of them eclosein any given year.

Because nests are large, as judged by the numberof cells, and because some prepupae may remainin diapause for >1 yr, nests persist in the samelocation from year to year. Based on nest mappingdata from 1988 and 1989 at the Rodeo locality,nest reuse is common. Seventeen of the 33 nestsfound in 1989 were within 10 cm of nests locatedin 1988 (Fig. 5). Nest 89-7, for example, was ex-tremely close to the location of nest 88-25. Fourteenof the 24 nests found in 1988 reappeared as activenests in 1989. In some cases, the number of nestsfound at one site in 1989 exceeded the numberfound at that site in 1988, possibly indicating nestfission due to the establishment of more than onemain tunnel (e.g., nests 88-20 and 88-17 appear tohave given rise to nests 89-28, 89-29, and 89-30 inarea 2). The fact that one commonly finds old, filledcells during nest excavation supports the idea thatnest reuse is common.

Using the nest maps from 1988, it was possibleto locate a number of newly initiated nests in 1989.One such nest, 89-17, was excavated (Table 1). Thelack of adult macrocephalic males and the smallnumber of prepupae both suggest that the nest wasnewly initiated. In contrast, consider nests 89-11and 89-15, both of which had been active in 1988.In both cases, the numbers of macrocephalic malesand females were equal and both nests containedlarge numbers of diapausing prepupae. It remainsto be seen how up to 29 adult females, as seen innest 89-17, come together during new nest initia-tion.

Sex and Morph Ratio. The gender and morphtype could be determined only for offspring whichwere collected as pupae or raised to the pupal stagein the laboratory. The sex ratio of 167 offspringreared from nests excavated in 1988 and 1989 was55% male, 45% female (Table 1) (not significantlydifferent from a 1:1 sex ratio; x2 = 1-73, P < 0.5).Of the 80 males reared and identified to morph,52.5% were macrocephalic males and 47.5% weresmall-headed males (not significantly different froma 1:1 morph ratio; x2 = 0.20, P < 0.9).

Female Cell Construction Behavior Based onObservation Nests. Cell construction began in theearly evening, usually by 1900 hours, and contin-ued at least until 0100 hours the following morning.Each female in a communal nest constructed onecell per evening, and there was no evidence ofcooperative cell construction. However, when twoor more females shared a common lateral, theyappeared to contribute equally to the general main-tenance of that tunnel. All females participated inkeeping the main and lateral burrows open bypacking soil into the side walls of these burrows.

When excavating new tunnels or cells, femalesfirst loosened the soil with their mandibles and,using their legs, pushed the soil behind them intothe open lateral tunnel. Females eventually clearedthe laterals of loose soil by walking backward andpushing the soil with their legs and metasoma intothe main tunnel or a nearby lateral.

During cell construction, females shaped the cellwall by repeatedly packing it with the pygidialplate and adding soil when necessary. When thesoil had been packed and smoothed sufficiently,the hydrophobic cell lining was added. Only onefemale was observed during this phase of cell con-struction. The female brushed the walls of the cellwith her glossa and paired, brushlike paraglossae,beginning at the junction of the cell with the lateraland ending with the distal-most portion of the cell.During this process she faced away from the lateral.Each stroke lasted roughly 4 s, and the femalebrushed continuously for at least 10 min. At onepoint, she turned around and made packing orsweeping motions with her metasoma as if applyingDufour's gland secretions, then returned to theoriginal position, facing away from the lateral, andcontinued her brushing motions over the areatouched by the tip of her metasoma. This processresembled the cell-lining behavior described byTorchio et al. (1988) for Colletes kincaidii (Col-letidae).

Female Cell Provisioning Behavior Based onObservation Nests. The daily pattern of femalebehavior involved cell construction, provisioning,oviposition, and cell closure (Fig. 6, Table 2). For-aging began as early as 0945 hours, and all cellprovisioning was completed by 1500 hours (Fig.7). Cells were completely provisioned with be-tween four and eight foraging trips (Fig. 8). Allcells were completely provisioned in 1 d, and nofemales provisioned more than one cell per day.Females did not cooperate in cell provisioning, andno obvious agonistic behaviors were observed amongfemales in the same nest. Guarding behavior wasnot observed, even by females who were not pro-visioning cells.

The mean duration of foraging trips and stopsin the nest between trips are given in Table 2.Females returning from foraging trips entered theircells head first, and then turned around so that theyfaced into the open lateral. The pollen loads wereremoved by rubbing the two hind legs togetherand remained as discrete clumps in the cell. Fe-

September 1991 DANFORTH: FEMALE FORAGING AND BEHAVIOR O F Perdita portalis 543

\+ ''

CD =103 CD

>

/

\

\

Fig. 5. Map of the Rodeo locality showing five groups of nests located in areas devoid of vegetation (crossesindicate location of metal stakes for each nest area), and nest areas 1 and 2 showing locations of nests relative tocentral stakes. Nests found in 1988 shown in open circles and nests found in 1989 shown in closed circles.


Table 2. Summary of female behavior based on data from observation nests

Behavior

Foraging behaviorForaging tripsStop between tripsFeeding trip

Behaviors within the nestPollen ball formationBeginning of pollen ball formation until first departure from cellDeparture from cellMatingEgg layingCell closure

Duration, i ± SE

27.07 ± 1.36 min67.7 ± 14.8 s34.69 ± 14.57 min

19.93 ± 1.09 min9.46 ± 0.93 min2.68 ± 0.20 min1.96 ± 0.13 min

18.31 ± 3.03 s12.52 ± 1.70 min

n

8688

3

19162216"1317

" One to three matings per pollen ball.

males did not form the pollen into a ball after eachtrip, as in some panurgines (Rozen 1967).

Pollen loads collected from females returning tonatural nests weighed 0.89 ± 0.04 mg (n = 10),which represents 68 ± 5.4% (n = 8) of female dry-body weight (mean dry body weight, 1.44 ± 0.05mg [n = 17]). Nectar loads of females collectedreturning to nests measured 0-39 fi\ of nectar (n= 16). On the last daily foraging trip, the beessometimes carried only small pollen loads (4 of 19cells) or no pollen at all (4 of 19 cells). Nectar forpollen ball formation is probably carried on thefinal trip.

Following the last daily foraging trip, femaleswith full or partial pollen loads deposited the pollenas described above, and then left the cell for 40.4± 5.37 s (n = 12), during which time groomingoccurred in the lateral burrow leading to the pro-visioned cell. After grooming, they returned to thecell and began shaping the loose pile of pollen intoa spherical ball. Females returning with no pollenbriefly groomed for 12-31 s (n = 2) in the lateralburrow before entering the cell to begin pollen ballformation.

When forming the pollen ball, females suspend-ed themselves above the pollen mass by pressingagainst the walls of the cell with the basitibial platesof their hind legs. While the pollen ball was rotatedwith the mid- and forelegs, the mandibles kneadedthe pollen, and nectar was regurgitated. The av-erage time required to completely form the pollenball was 20 min (Table 2).

Approximately 9 min from the initiation of pol-len ball formation, females always left their cellsand entered the lateral tunnel, or occasionally themain tunnel. If a macrocephalic male was present,mating always took place during this departurefrom the cell (9 of 9 times). In nests that lackedmales, females simply groomed during this periodand then returned to the cell (10 of 10 times) andcontinued pollen ball formation. In nests with mac-rocephalic males, one to two more copulations oc-curred before the egg was laid, but, unlike the firstones, the subsequent matings were initiated whenthe male entered the cell and pulled the femaleout into the lateral with his mandibles. These later,

male-initiated matings were recorded in eight ofthe nine cells I observed completely provisioned.No mating was observed within nests at any othertime except during pollen ball formation, and forevery cell observed completely provisioned, fe-males mated at least once with a resident macro-cephalic male, when present, before egg laying.

Immediately after egg laying, the cell was closedby the female. She simply walked into the lateral,remaining facing away from the cell, and beganto make packing motions with the apex of hermetasoma. Females were never observed to usetheir mandibles or legs when closing a cell. Cellclosure took «13 min (Table 2). Females then in-variably left the nest and, in the three cases ob-served, returned approximately 35 min later (Table2) without any pollen visible externally. This lasttrip of the day is, I believe, a feeding trip, as insome other panurgine bees: Perdita (Danforth1989), Calliopsis (Hypomacrotera) callops (Cock-erell) (Danforth 1990).

The mean durations of the behaviors listed inTable 2 are based on observations of females innests with and without macrocephalic males. Whenthe data for each of these behaviors are analyzedseparately, there are only slight differences be-tween females in nests with and without macro-cephalic males. The mean time for pollen ball for-mation is only slightly, although significantly, longerfor females in nests with macrocephalic males (x= 22.32 ± 1.77 min, n = 9) than for females innests without macrocephalic males (x = 17.78 ±0.97 min, n = 10, P = 0.044). This is probably aresult of repeated matings before oviposition innests with macrocephalic males. Macrocephalicmales appear not to alter any other recorded as-pects of the provisioning behavior of females.

In four cases, completed cells were only partiallyprovisioned because of the death or disappearanceof a female resident. These cells were generallyfilled with dirt by the remaining residents within3 d. No females adopted the empty or partiallyprovisioned cells of their absent nest mates.

Larval Development Based on ObservationNests. Although most offspring produced in obser-vation nests entered diapause, some larvae contin-


FEMALE BEHAVIOR

Intra-nest mating (1-3 times)Feeding trip (35 min.)

Cell closure (13 min.)

t Egg laying (18 sec.)

^_ Pollen ball formation (20 min.)

Cell provisioning

New cell construction/sleep (4-8 trips/cell, 27 min./trip)

1

1

1

1

1

1

1

2

i

i

3

1 i

i i

4 5i

6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24

TIME »

Fig. 6. Summary of female behavior throughout the day (see Table 3 for detailed data).

ued development and emerged as second-genera-tion adults the same year (partial bivoltinism, Seger1983). This is probably true of most bees in naturalnests, as judged by the nest excavation and labo-ratory rearing results (see above).

In observation nests at 25-30°C, larvae com-pleted feeding and defecated in 6-9 d (x = 7.8 ±0.2 d, n = 25). From 3 to 7 d thereafter, theypupated (x = 3.9 ± 0.4 d; n — 11), and in as fewas 9 d thereafter they eclosed to adults. The shortestobserved period from egg to adult was 21 d. Thered Plexiglas made it difficult to determine theexact stage of development reached in some cells,so these data may be subject to error.

During development, larvae initially feed on topof the pollen ball, facing toward the back of thecell. Larvae in the later stages of development,when the pollen ball had been nearly consumed,rest on their backs with the remaining pollen cra-dled on their venter. After all the pollen is con-sumed, but before defecation, larvae begin to rotatearound the transverse axis of the cell head first,maintaining contact between their dorsal tuberclesand the wall of the cell as they do so. Up to eightfull rotations by one larva were observed in 4 h.The period between the completion of feeding anddefecation was 1-5 d (x = 3.4 ± 0.5; n = 8). Larvaeglue their feces to the posterior part of the cell,and diapausing larvae rest on their backs, facingtoward the cell entrance. As in other panurgines(Rozen 1989), no cocoon is spun.

The weights of 157 live prepupae ranged from3.5 to 10.5 mg (x = 7.55 ± 0.12) and were normallydistributed. The dry weights of 32 pollen ballsranged from 3.4 to 6.0 mg (x = 4.81 ± 0.11) andwere also normally distributed. Dividing pollen balldry weight by adult dry body weight gives an es-timate of the efficiency with which pollen mass isconverted into bee biomass. For an average drybody weight of both males and females, I used asample of 10 small-headed males, 10 large-headedmales, and 20 females because these are roughly

the proportions of the three types based on broodsreared from nests (Table 1). Based on this estimate,average adult body dry weight equals 1.25 ± 0.05mg (n = 40). Conversion efficiency equals 1.25 mg/4.81 mg or 26.0%.

Parasites and Predators. Although two femalePseudomethoca spp. (Mutillidae) were found whileexcavating nests (one Pseudomethoca toumeyi(Fox) and one undescribed) no mutillid larvae werefound in natural nests, nor were any other parasitesfound. However, in observation nests, two parasitesand one predator were discovered. On August 31,an adult female Pseudomethoca sp. near scaevo-lella (Cockerell & Casad) was found in observationnest PPO#11, which contained seven completed,fully provisioned cells. She was resting in a filledlateral, approximately 9 cm from the junction ofthe main tunnel. Although a single female P. por-talis had been seen in the nest the day before, therewere no adult Perdita in the nest the day the mu-tillid was found. The mutillid remained in the nestfor the next 4 d and was observed entering one cell(F) on 2 September. On 3 September, the mutillidleft the observation nest and was collected. Thisnest remained in place until 14 September, andmutillid larvae were eventually detected in cellsB, C, and E. The larvae in cells C and E spuncocoons and pupated by 14 September, whereasthe larva in cell B died 7 September. Only one ofthe seven Perdita larvae survived to reach the pre-pupal stage (cell A). Apparently only cells withdefecated pupae could be parasitized. The pupa incell F, although entered 2 September, had not yetdefecated and was not parasitized. However, larvaein cells E and C, the two larvae successfully par-asitized, had both defecated by the time they wereattacked.

In another nest (PPO#12), a small meloid beetlelarva was seen feeding on top of a 3-d-old Perditalarva. The nest had one adult female resident atthat time. Over the next 9 d, the beetle consumedfive Perdita larvae within the nest by burrowing


a. 40 •

35 ••

•- 30 ••Oi 2 5 -

a. 20

1 5 •

1 0 •

UJa. 5 •

8-

6-

4-

2-

^ «/> ^ j? ^ 4 5 6 7 8TIME No. foraging trips/cell

Fig. 7. Histogram showing the percentage of returns from pollen collecting trips occurring per hour throughoutthe day (n = 57 returns with pollen observed). Data based on observation nests.

Fig. 8. Histogram of the number of foraging trips made per pollen ball by females in observation nests. Nineteencells were observed for the complete provisioning cycle.

from cell to cell. On 10 September, the nest wasbrought to the laboratory and the beetle was fedan additional two P. portalis larvae. Unfortunately,the beetle died before reaching the pupal stage.

Finally, one observation nest containing larvaeand pupae (but no adults) was attacked by ants(Solenopsis molesta (Say)), which killed several pu-pae.

Discussion

All the behavioral observations of females withinthe nest indicate that this species is communal. Noagonistic or cooperative behavior was observed,and each female oviposited in the cell which shehad provisioned. There was no evidence of within-nest cleptoparasitism or robbing in P. portalis. Fe-males were never observed opening cells and tend-ing larvae or removing feces, a subsocial behaviorobserved in some Ceratina Latreille (Sakagami &Maeta 1987) and Lasioglossum (Evylaeus) Rob-ertson species (Knerer & Plateaux-Quenu 1966).

Communality appears to be a well-establishedtrait in this species. Unlike all other communalPerdita studied, there were no solitary nests found.The origin and maintenance of communality hasbeen attributed to the advantages of nest defensein bees (Michener 1974, Abrams & Eickwort 1981)and sphecid wasps (Evans & Hook 1982). However,because females were never observed spending ex-tended periods of time at the nest entrance or de-fending the nest against intruders, improved de-fense does not seem to be associated with communalnesting in this species.

A more likely hypothesis for the maintenance ofcommunality is that the costs, in both time andenergy, of solitary nest construction may be great.

Although nests are shallow, burrows penetratethrough a hard-packed clay layer located 3-5 cmbelow the surface. The brief season of peak Sphaer-alcea bloom («4-5 wk) may also impose a repro-ductive cost on delayed reproduction for new nestconstruction. Interestingly, in the two newly ini-tiated nests excavated, there were 10 and 29 adultfemale residents, suggesting that when new nestsare founded, many females participate. A female'sbest reproductive option may be to remain in hermother's nest, making use of the main tunnel andlaterals constructed by previous generations.

Because of the apparently high frequency ofnatal nest reuse, nestmates may be significantlymore closely related to each other than to a randomsample of the overall population. The degree ofwithin-nest relatedness would depend, first, on thenumber and genetic relatedness of the original nestfoundresses and, second, on the number of matri-lines that persist through time. The presence offlightless, macrocephalic males that mate with fe-male nestmates no doubt raises the coefficient ofrelatedness among nestmates, but at this time it isimpossible to say by how much.

The biology of P. portalis is similar to that of aclosely related species, P. texana (Neff and Dan-forth 1991). Both species are communal, althoughthe nests of P. portalis contain many more femalesper nest. In both species, females provision one cellper day, and intranest mating almost certainly takesplace in P. texana as in P. portalis, although malesof P. texana are not dimorphic. Unlike P. portalis,however, P. texana nests do not appear to be reusedover many generations.

Although the information now available on in-tranest behavior of nonapid bees is primarily basedon observations of only a few distantly related spe-


Table 3. Previous studies of bee behavior within nests(excluding studies of the family Apidae)

Family and species Reference

Colletidae

Colletes kincaidii Cockerell"

HalictidaeLasioglossum (Chilalictus)

erythrurum (Cockerell)''

Lasioglossum (Dialictus)zephyrum (Smith)d

L. (D.) versatum Robertson"*L. (D.) imitatum (Smith)d

L. (Ecylaeus) spp.d

Halictus rubicundus(Christ)*

Neocorynura fumipennis(Friese)"

Augochlora pura (Say)"Nomia melanderi Cockerell"

Andrenidae

Perdita portalis Timberlakeb

MegachilidaeOsmia lignaria propinqua

Cresson"O. califomica Cresson"O. montana Cresson0

Anthophoridae (Xylocopinae)Xylocopa pubescens Spinolac

X. sulcatipes Maac

Ceratina japonica Cockerellc

C. flaoipes Smith0

C. Okinawa Matsumura &Uchidac

Braunsapis sauteriella (Cock-erell)c

Torchio et al. 1988

Knerer & Schwarz 1976;Kukuk & Schwarz 1987,1988

Batra 1964

Batra 1968Batra 1968Knerer & Plateaux-Quenu

1966Batra 1968

Batra 1968

Stockhammer 1966Batra 1970

This paper

Torchio 1989

Torchio 1989Torchio 1989

Cooperative behaviors such as oral trophallaxishave been reported for a number of species listedin Table 3 (e.g., L. erythrurum (Cockerell), Cer-atina species, and Xylocopa species). No oral troph-allaxis was observed either among females or amongfemales and males in P. portalis nests. However,macrocephalic males were observed entering par-tially provisioned cells and manipulating the loosepollen stored there by females, but whether malesare ingesting pollen or nectar or both is not known.

Among the species listed in Table 3, L. erythru-rum, although distantly related to P. portalis, showsthe most similar type of intraspecific interactionsobserved in P. portalis. As many as 10 L. erythru-rum females share a nest, and there are no agonisticinteractions among nestmates (or non-nestmates),nor is there any obvious cooperation within a nest.Unlike P. portalis, however, nestmates of L. eryth-rurum share food via oral trophallaxis, both amongfemales and with the flightless macrocephalic malespresent in the nest (Kukuk and Crozier, 1990).

Acknowledgment

Gerling et al. 1981, 1983Gerling et al. 1983, Stark et

al. 1990Sakagami & Maeta 1985,

1987Sakagami & Maeta 1987Sakagami & Maeta 1982

Maeta et al. 1985

" Solitary species.b Communal species.c Facultatively eusocial species.^ Species in which eusociality is a

togeny.

cies (Table 3), it is worthwhile to compare thebehaviors observed in P. portalis with some of thebehaviors described for other species. Most of thespecies listed in Table 3 show agonistic relation-ships among nonnestmates and even nestmates. Forexample, Xylocopa sulcatipes Maa and X. pubes-cens Spinola females actively defend their nestsand fight with intruding conspecifics (Velthuis1987). Other species show aggressive behavioramong nestmates; for example, most eusocial hal-ictids, in which physical interactions determine, inpart, dominance hierarchies (Michener 1988). Fur-thermore, oophagy, a form of indirect aggression,was observed in Lasioglossum (Dialictus) species,Ceratina flavipes Smith, C. japonica Cockerell,and Xylocopa sulcatipes (Stark et al. 1990). Noneof these forms of conflict was observed in P. portalisnests; females passed each other in tunnels with nosign of aggression, and females were never ob-served destroying eggs or larvae.

I am grateful to C. D. Michener (University of Kansas)and J. G. Rozen, Jr. (American Museum of Natural His-tory) for their advice and help during this study. WithoutDr. Rozen's generous help in the field, this project wouldnever have been started. I thank the Resident Directorsof the American Museum of Natural History's South-western Research Station; Wade Sherbrooke; Pam Lim-berger; Kristina Schwartz; and volunteers Emily Dick-inson, James A. Davidson, David Domingo, and ErnieLuikart for their help in collecting data. I am gratefulto Karl V. Krombein (Smithsonian Institution) for iden-tifying the mutillid. George C. Eickwort (Cornell Uni-versity), John Alcock (Arizona State University), JaneBrockmann (University of Florida), Penelope Kukuk, C.D. Michener, and J. G. Rozen, Jr. commented on earlier

normal stage in colony on- versions of this paper. This study was supported by twoTheodore Roosevelt Memorial grants from the AmericanMuseum of Natural History and a pre-doctoral fellow-ship from the Smithsonian Institution. This is contribu-tion 3045 from the Department of Entomology and theSnow Entomological Museum, University of Kansas,Lawrence.

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Received for publication 4 September 1990; accepted2 April 1991.

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