Ethological Study of African Carpenter Bees of the Genus Xylocopa (Hymenoptera, Anthophoridae)

2. Tierpsychol., 44, 337-374 (1977) @ 1977 Verlag Paul Parey, Berlin und Hamburg ISSN 0044-3573 / ASTM-Coden: ZETIAG

Zoologisches Institut der Universitat Miinchen, Research Group Renner, and the Max-Planck-lnstitut f u r Verhaltensphysiologie, Seewiesen

Ethological Study of African Carpenter Bees of the Genus Xylocopa (Hymenoptera, Anthophoridae)')

By GUSTL ANZENBERGER

W i t h 18 figures

Received: Apri l 19, 1976

Accepted: February 25, 1977

Abstract

Over 200 bccs of 4 African Xylocopa species were observed for 3 months on the island of Rubondo (L. Victoria, Tanzania). Some 40 burrows wcrc investigated, 100 bees marked. Building techniques are minutcly reported; burrow construction simplifies defence and allows re-use by succccding generations. Food plants, collecting, provisioning and all aspects of ontogencsis arc trcatcd, insight given into pupal leg mobility and the much-debated emergence order after cclosion: the first-hatched bee, in the rcarmost cell, prepares the way for siblings. Copulation and the copulatory hold are studied using tethered 29, and illustrated. A few colonization experiments arc described and a spectrogram of begging sounds given. Mceting of the generations, feeding of the young and nest-defence by young siblings throw light on the evolution of primitively eusocial communities. The known liternture is reviewed in each chapter.

Introduction

Interest of the biological sciences in the Apoidea (Hymenoptera) has long centred on one species, the honey bee (Apis mellifica), distinguished for its social structure, a unique system of communication, and other physiological properties. Ever since K. v. FRISCH initiated a line of research into these various aspects, the bee has proved a most rewarding object. With interest i n the evolution of colony-forming Hymenoptera, increased attention was given their closest relatives. 4 of the 9 families of Apoidea (MICHENEK 1974), the Colletidae, Oxaeidae, Mellitidae and Fideliidae, consist exclusively of solitary species. Although some representatives of the Andrenidae, Halictidae, Mega- chilidae and Anthophoridae live in parasociai colonies, others have already developed primitive eusocial communities. The latter are the tribi Halictini and Augochlorini, within the Halictidae, and the tribus Ceratini within the Anthophorini. The Ceratini, with their primitive eusocial communities, form a link with the Apid colonies (WILSON 1971). My work focused on represent-

1) In homage to Prof. Karl V O N FRiScti on the occasion of his 90th birthday.

2. Tierpsychol., Bd. 4 4 , Heft 4 22

338 GUSTL ANZENBERGER

Tota l No. Species

X. imitator 90 X. nigrita LD X. torrida 60 X. flavorufa 30

atives of the Xylocopini, closely related to the Ceratini, and with them forming the sub-family Xylocopinae.

REAUMUR (1742) was the first to describe bees constructing nesting burrows in dry wood, and they are accordingly still called: les abeilles perce-bois, carpenteiros, carpenter bees, Holzbienen. Later accounts were given by F R l E s E (1 909, 1923), BRAUNS (1 91 3) and BISCHOFF (1 927). MALYSHEV gave the earliest comprehensive reports of Xylocopa valga (1931) and X . ins-cyanescens (1947). In the former work (“Life of the Carpenter Bees”) he included a summary from the literature of more or less complete data on some 40 species. But IdUKD and MOURE (1963) could still write of the Xylocopinae: “There is a critical need of comparative ethological studies.”

Individually Breeding recognizable ab ovo L a r v a Pupa

48 3 2 7 28 2 L 5 12 2 13 2 2

Material and Methods

Four African Xylocopa species were examined, ascribed by HURD and MOURE (1963) to three different sub-Kenera:

Sub-genus Koptortosoma Gribondo

Sub-genus Afroxylocopa H u r d and Moure

Sub-genus Mesotrichia Westwood

Xylocopa (Koptortosoma) imitator Smith

Xylocopa (Afroxylocopa) nigrita (Fabricius)

Xylocopa (Mesotrichia) torrida Westwood Xylocopa (Mesotricbia) flauortrfa (DeGeer)

The animals were a t first marked with standard bee-numbers applied with an instant glue, but these hardly withstood the intensive grooming of the 99 longer than 24 h. O n 8 8 they lasted a maximum of 3 days. I therefore resorted for identification to cropping portions of body hairs, and cutting marks in the wings inasfar as these were not already distinctively patterned by wear and tear.

Field protocols were made with a Grundig E N 3 dictaphone and processed in the laboratory. Photographs were taken with a Yashika TL Electro X-reflex camera, using the lenses Yashinon-DX 1 : 1.7, Hanimax Tele-auto 1 : 3.5 and Medical Nikkor Auto 1 : 5.6. For the tape recordings I used an Uher microphone (M 517) and an Uher (4200-report) stereo recorder. The sound spectrograms were prepared with a Sonagraph 6061 of K a y Electrics.

Observations, Experiments and Results

I. Occurrence and Biotope

The investigation, lasting 3 months, was carried out on Rubondo (900 m above sea level, 2’ 10‘ lat. south), an island in SW Lake Victoria (East Africa), where the four species occur sympatrically. Additional observations were made on Xylocopa flavorufa in the Serengeti National Park, Tanzania.

The main area of observation (Fig. 1) was an approx. 500 m X 800 m stretch of grass wit‘h scattered bush and several larger tree groups. The tract

Ethological Study of African Carpenter Bees of the Genus Xjilocopa 339

was bounded on the NW, SW and SE by gallery forest, but was open on the YE to Lake Victoria and merged directly into the sandy littoral. The food plants also grew within this area.

Fig. 1: Plan of burrows and food plant locations in the main investigation area on Rubondo. i = X.imitator; F = X.flrzvorufa; T = X.torrida; N = X.nigrita; 1-6 = Cassia

abbreviata bushes

X . imitator occurred cxclusively in the open grassland, 6 out of 7 burrows were found i n the thin branches of Annona chrysophylla Boj. (Annona- ccae), which here comprises 84 o/o of bush cover.

X . torrida and X . f lavorufu construct burrows in dry branches or trunks on the fringe of woodland or larger tree groups. I found nests of X . flauorufa in dry steins of Sesbania sesbun (L.) Merrill (Papilionaceae) in the Screngeti, but hcre too bordering gallery forest or Iropjes, not in open country.

X . nigrita shows a preference for constructing burrows in dead trees (un- identified) near the shore. Their bases were with one exception at least somc- tiiiies covered by water.

11. Nest-building Behaviour

1) General Preface

Many solitary Apids (particularly Megachilids) construct nests in dry timber, although usually in naturally-hollowed stems. The actual breeding cells are built of plant material by Osmia, Megachile, Anthidiurn, and of clay by Heriades and Chelostoma.

340 GUSTL ANZENDERGER

FRIESE (1923) describes only a single instance of a nesting burrow - of Anthophora f ~ r c a t a - found in Denmark and closely resembling a carpenter bee construction. In Germany only burrows in the ground are so far known for this species.

According to HURD and MOURE (1963), during the evolution of the Xylocopinae a comparable change has occurred in nest substrate choice. MALYSHEV (1913) presupposes a Xy- locopid primitive form nesting in the ground in wide-ramified constructions. H e considers the great problem to have been the damp, threatening breeding succes~, as carpenter bees neither finish off the breeding cells with a coating of saliva nor spin larval cocoons. Xylocopa (Proxylocopa) ol iv ier i , occurring principally in SW Russia, still constructs nests in the ground. These were first described by GUTDIER (1914). Xylocopa sicheli (BRAUNS 1913) and X . uesti ians (DOVER 1924) nest in the green petals of the aloe. Probably in adaptation to this soft, juicy substrate the mandibles of this species have become spoon-shaped, and are distinctly different from those of other species. HURD and MOURE (1963) therefore proposed for them the new sub-genus Gnathoxylocopa. These bees survive the dry season in thin stems. I mention as a curiosity a species of the genus Platynopoda, which sometimes tunnel nests in lead-covered overland cables (LADELL 1931; SCOTT 1932). All other carpenter bees conform in building in dry wood and in separating the breeding cells by sawdust partitions.

2) O w n Observations

a ) The Construction of a New Nest Newly adult 99 having parted from the mother and/or siblings, construct

a living and nesting burrow of their own. As all the ?? I ever saw thus occupied had perfect, undamaged wings, I am sure that they begin building their own nests within a few days of leaving the maternal burrow. At those seasons when newly-emerged animals are to be found in all burrows I saw very many young 99 flying and crawling over all sorts of dry wood, as if seeking. Un- fortunately I cannot give any basis for their choice; i t sometimes seems as if a bee tests timber suitability by a few “trial incisions”, in any case I found several attempted bores only a few mm deep.

A t first at the place selected an entrance hole is cut a t rightangles to the grain of the wood. This is circular in cross-section and has a sharp outer rim (in X . imitator, X . torrida and X . f lavorufa) or (in X . nigrita) i t is an upright oval, one to a few cm deep. The short atrium leads in a bend into the ascending bore, but there is a clearly-defined ridge where it leads into a descending bore. In all cases I observed, the ascending bore was tunneled first; in single- bore burrows this invariably ascended from the entrance hole. Table 2 sum- marizes nesting-burrow measurements for the 4 observed species. Fig. 2 shows the preferred orientation of the entrance holes.

Having started, the bee works a t a structure almost all day long, with only a short feeding pause in the late afternoon; the first night is spent in the new burrow, which has reached a depth of some 4 cm.

0 The daily stint was measured with a probe, and directly beneath the entrance hole all sawdust was caught in a small plastic bag. The bees were not in the last disturbed by these manipulations, and flew in without hesitation on returning from foraging. Work on the bur-

N

W

Fig..?: Orientation of entrance holes for the 4 species. Rings show numbers ob-

S served

Ethological Study of African Carpenter Bees of the Genus Xylocopa 341

Bore 6 in rnrn

1L 1L 13 1L 13 1L 1L I L 1.4 1L 15 I L 14 IS 1L 16 1L I5

Table 2: Burrow dimensions. Survey of entrance and bore diameters, and bore lengths measured from entrances, for X . imitator, X . flaworufa, X . torrida and X . nigrita

1LO 20 - 45 L5 - 80 65 - 15 - 70 - L5 -

70 - 100 95 -

100 100 70 65 -

100 - 90 - 80 - 80 - 55 - 70 - 90 - 100 -

Entrance I Q in rnrn Burrow Number

1L,1

17 17 18 18 17 19 18 17 18 I8 17 17.6

I 1 1 2 1 3 I L I 5 1 6 I 7 1 8 I 9 I 10 I 1 1 I 12 1 1 3 * I 1L* I 15 I 16 I 17 I 18,

78 65 70 150 - 60 - 80 -

100 - 100 - 85 - 60 - 120 - 56 - 90 - 70 - 88 -

12 1 1 12 1 1 12 12 1 1 1 1 12 12 12 12 12 10 12 1 1 12 12

T I T 2 T 3' T L

Mean: X. imitator

F 1 ' F 2* F 3* F L * F 5 F 6 F 7' F 8* F 9' F 10' F l l *

Mean: X. flavorufa

15 I L 1L 16

1 1,6

14 13 1L 1L 13 13 13 1L I L 14 I L

13,6 19 18 17

80 - - 70 -

70 - - 55 - 90 - - 1 5 5 -

Mean: X. torrida I 1L,2

18

N I N 2 N 3 N L

70 50 - 30 -

N 5 N 6

Mean: X. nigrita

17 x 21 16 x 20 17 x 21 17 x 19

I6,8 x 19.6

17 x 19 17 x 20

Ascending bores : lenqth in rnrn

Descending bores : length in rnrn

LO - 60 25 - 30 LO - 15 - 65 30 -

55 so - - -

LO LO 50 65 - 50 - 60 70 - 60 - 80 -

70 - 80 -

55 4 3 50 100 - 55 - 50 - 90 - 70 - 55 - 70 -

110 - 2L - 90 -

110 - 75 -

19 19 I8 19

19 18

1 Only ascending bores ILO 70 100, 60, 110, 110, 90, 260, 200, 150, 70

LO, 50, ILO LO, 70, ILO, 120 60

2L0, 200, 240, 100, 80, 80, 120, 80, LO, LO,

18,6

') = timber dimensions restrict bore number.


row continued after sunset, but I cannot say whether it continued all night with long pauses, or whether it stopped some h after sunset and/or was resumed before dawn. But i n the mornings the plastic bags always held their quota of “night-shift” sawdust, although this was considerably less than the day’s production. As soon as the ascending bore is finished, the bee either constructs breeding cells in it immediately, or else commences a descending bore.

Construction of a descending bore means that the sawdust does not fall out, but must be carried. Up to about a cm in depth the bee ejects the gnawed- off wood crumbs between its legs, using its head as a shovel. As the bore progresses the bee works at first head-downwards, dipping the head into the debris and pressing this by head movements against the thorax. Suddenly the animal somersaults with the abdomen angled, and now stands head-up in the bore; abdomen and back legs form a “basket” which now contains the debris; using mid and forelegs the bee climbs to the entrance, and the debris is brushed out by leg movements. This procedure is repeated until all the rasped wood is disposed of, then tunneling begins again. All wood waste is removed in this way; in the case of parallel bores, then, the sawdust must fall into any lower ones already completed, or is pushed there, and is onIy then transported to the entrance.

Nest structure - whether a bore ascends or descends or there are both types, or a system of several practically parallel bores develops - depends on the constitution of the wood (diameter, knots). Another factor is whether the branch o r stem already harbours burrows of ocher 99, so that a certain direction is prescribed for the latecomer.

The burrow system of one Q (Fig. 3) never communicates with that of another; we do not yet know how the animals assess the thickness of walls when gnawing at them, and avoid breaking into the neighbouring burrow. Once a young X . imitator P was observed trying to construct a new burrow

in its birth-timber, which already held the systems of 5 other 99. Only 1.5 cm was left for the young bee, whether up or down, and finally, having completed this modest burrow, it stayed in it for a day, then wandered off. Several days later I discovered this bee elsewhere, in a new burrow.

In X . imitator, X . torrida and X . flavorufa there is always only one adult Q in a burrow. In contrast, several adult 99 of X . nigrita live together in an extensive system, which however certainly originated with the work of a single 0 , and was enlarged by succeeding generations. There is invariably only one entrance to such

Fig. 3: X . imitaior burrow in natural position, entrance hole below, right. Bulge (middle) in the right-hand tunnel shows

commencement of a further parallel bore


a system, which rules out a chance or intentional fusion of two or more origin ally separate burrows.

One nest of X . nigrita was found when opened up to have 9 bores, their total length being 147 cm; in another the total length of the 13 bores was 181 cin (see Table 2). It is remarkable that all these bores led upwards, branch- ed off more or less irregularly, and ran parallel. In the first system there were 4 adult 99, and in the second 6. I cannot say whether the animals of a community were related, but in a later chapter I shall show that in all probability they were either mothers and daughters or else sisters. Here it seems that each 9 constructs her own bore with breeding cells, but this assumption is admitted- ly based on indirect observation: in the opened row of each bore, the conterminous larvae showed the same steps in development as in the other 3 species, where in each case only a single 9 provisions them. If several X. nigrita 99 provisioned a cell simultaneously, we could expect such rapid progress that larvae in conterminous cells would show practically no difference i n dc- velopmen t.

In all 4 species, bore diameter is not constant throughout the length; a t intervals coincident with the later breeding cells i t is reduced a few mm. These ringlike protrusions form the abutments for the partitions, to be erected later, which separate the individual cells.

Tunneling is the work of the mandibles only. I think it very unlikely that the bee’s leg sculpture is suitable for rasping wood (BISCHOFF 1927). SCHREMMER (1972a) considered that “the protruberances on the external surface of the hind tibia, and the outward-pointing spikes or jags on the distal end of the tibia of all 3 pairs of legs, could serve the bee in supporting itself in its cylindrical nesting-burrow, usually in timber”. According to my observations the outer sculpture of the legs is used exclusively for locomotion in the burrow. I would like to describe this general behaviour pattern.

b) Locomotion in the Burrow A bee moving undisturbed in its burrow holds itself by bracing the legs

sideways, only the outer sides of the tibiae and metatarsi contacting the walls. The other tarsi are curved in slightly towards the body, while the claws are never used for locomotion in the burrow. A t rest the forelegs are laid flush with the body, only the mid and hind legs being used as props (Fig. 4). On all 6 legs of both d 8 and 99 a distinct thorn projects outwards from the distal end of the tibia, not particularly strongly marked on fore and hind legs, but sharp and well-defined on the mid legs. When the legs are flush with the body the thorns of the mid-tibiae protrude to right and left a t rightangles to the longitudinal body axis, and their points, given purchase, form a pivot exactly in the lateral body axis. O n this the animal rolls itself head first to alter its direction. In the narrow tunnel crawling backwards is a difficult operation due to the hairy coat with its backward grain, and is seldom observed. It is known that the carpenter bee’s nearest relatives, the Ceratini, can run equally well backwards and forwards in their self-gnawed wooden bores (FRIESE 1923); but these are hairless bees.

c ) Observation of 8 d No d 8 of any of the observed species were seen constructing burrows or

even helping construct them in any way. They often used burrows abandoned by 99, or spent their nights in all sorts of holes and cavities. After leaving the maternal nest they will accept any lodging (whether of wood or not) as long as it affords some kind of shelter.


Ftg 4 : X. nigrita- 8 climbing inside an opened burrow. The forelegs are held close to the body and only mid and hind legs

used (photo slightly touhed up)

3) Review of Literature and Discussion

WAGNER (1958), JANZEN (1964, 1966), SAGE (1968), KAPIL and DHALIWAL (1 968, 1969) mention nest-building briefly in their work. More detailed descriptions have ;’ been given as yet only by HURD (1958) und HURD and MOURE

i (1960). Consistency in choice of dwelling timber is found mainly in species nesting in plant stems (HURD

{ and MOURE 1960). Structural timber is especially attractive to X . californica, X . tabaniformis, X . virginica

. , i (HURD 1958). X. orpifex prefers - * 1 felled but sound sequoia and pine-

wood, and NININGER (1916) writes: “This, I think, is a wise choice, for one of its dangerous foes is found abundantly, tunneling through decaying redwood”. It takes X . orpifex 7 days, however, to gnaw out ,I bore 2.5 cm long - the slowest rate of construction known for carpenter bees. Not only do all other species construct much longer bores within this time, they also complete and provision 2-3 cells.

Few species, then, exhibit a preference in choosing timber for their burrows, and i t seems that the condition of a plant rather than its type is the main factor.

Only NININGER (1916) describes the method and manner of building: “While digging the bee slowly turns in the burrow, requiring from 30 min to 1 h to complete the cycle. Observation showed no regularity or uniformity either in rate or direction of turning”. These sentences seem inconsistent, the first implying a certain regular speed denied in the second; or he gives the angular velocity, which cannot be calculated without a regular turning direction. I made an hour’s protocol for each of 3 nest-building 99 (2 X . flavorufa, 1 X . imitator) recording every alteration of gnawing position. After 10 s to 710 s at one place the bee turned either right or left by the most divergent number of degrees. In spite of the irregularity of adopting gnawing positions, each tunnel section is gnawed for approximately the same period. Probably the mandibles rasp all wood within reach of the head pivot, so that a circular tunnel results.

None of the observed species showed any regularity in the number of bores constructed, but new bores are added in time if timber diameter permits. According to BRAUNS (1913), X. f favorufa constructs many parallel bores, whereas for this species I found (Table 2) only single-bore burrows. The findings of KApiL and DHALIWAL (1968) and SAGE (1968) agree with mine, that single-bore burrows always ascend.

1

Ethological S tudy of African Carpenter Bees of the Genus Xylocopa 345

No work so far has discussed how these close-settling bees avoid in- fringing on neighbouring burrows. In the whole literature only 2 nest burrows (of X . frontalis) each having 2 entrance holes are described (MICHENER and MOUKE in HURD 1958).

A mechanism checking fusion of burrow systems from the outset is the aggressive behaviour of the 99 towards nearby settlers, as described by MALY- SHEV (1931) for X. walga and JANZEN (1966) for X . fimbriata. JANZEN describes a fight between 2 ? O (“they hovered facing, then flew at each other”), where the defeated newcomer ceases building. The possible adaptive value of this behaviour is limitation: the more bores tunneled in an old branch or tree, the greater the risk of collapse. Furthermore, parasites will detect a colony sooner that scattered nests; and with the latter, timber collapse claims fewer victims i n the population (JANZEN 1966).

I observed that new tunnelers leave even empty systems intact, these form limits, and are not merely incorporated in the new construction. A neighbour need not actually be present in a burrow to effect this. Somehow, therefore, carpenter bees have cognition of wall thickness. This is most obvious where borers i n thin branches follow every bend faithfully, without once break i ti g t h rough .

I observed in X . nigrita that several adult ?? inhabited one burrow system. NININGEK (1916) found this in X. varipunctata: “In one case I found several individuals using a common surface entrance from which each constructed a separate tunnel for her brood nest.” According to WAGNEK (1958), X. fimbriata live similarly; but JANZEN (1966) rated just this species as extremely aggressive intraspecifically (see above). Here we have incompatible statements, perhaps a mistake in species identification. SAGE (1 968) sometimes discovered so many 8 d and 99 in the nests of X . gualanensis and X . sub- eirescens that these could not possibly have been the progeny of a single ?. Unfortunately he does not go into the age structure of the community.

To my observation that X . nigrita constructs only ascending bores, I would mention that I assume this to be a condition for the communal living of several ?? in one structure. If a new ascending bore is added, the sawdust falls out of the entrance; there is no risk that it will defile a descending bore if there are none, and disturb a 9 who may just be provisioning her breeding cells.

There are two reports in the literature on the building activities of d d . According to HORNE (1872), d 8 of X . chloroptera help seal the breeding cells - a unique behaviour in Hymenoptera. DOVER (1924) observed X . aestuans 8 8 participating in building bores. MALYSHEV (1931) writes of X . valga d 8 that “they are able to construct a shelter for themselves for the night or as a protection against bad weather.” But he cites only one 8 which, he says, dug a short tunnel in a clay wall and “returned there every night”. H e does not report any burrows of 8 8 made in timber.

In Gnathoxylocopa the mandibles of the ?? are spoon-shaped (see chap. 11,l). 8 8 do not have this special formation of the mouthparts (HURD and MOURE 1963), so that they cannot construct bores, a t least in the nest substrate typical for the species. HURD (1958) also found that male carpenter bees (of X. californica arizonensis) do not build, and that after leaving the maternal nest they will accept shelter varying in quality. JANZEN (1966) reports that a X . fimbriata-c3 dwelt for some time in a hole in a concrete post. OSTEN (pers. com.) found 4 X. violacea-6 8 together in a hollow concrete block.

346

Flower colour

yellow

yellow yellow yellow

yellow

GUSTL ANZENBERGER

X. i. X. n.

+ +

+ + +

+

111. Behaviour on Flowers

yellow

1) General Preface

Hitherto, interest in the Xylocopinae has centred mainly on their collecting activities a t flowers - not so much in the “normal” flower visiting (SCHREMMER 1960, 1972; KUCLER 1972) as in nectar robbing. A great many authors have dealt with this, from HEYDEN (1861) to SCHEDL (1967). SCHREMMER (1972a) reviewed the whole literature; he also succeeded in giving a n exact description of the process, by functional morphological investigations of the head capsule. He reports that the petals are not bitten through, as with bumble bees, bu t pierced.

I n discussions o n Apid phylogenesis, importance is ascribed to the method of trans- porting pollen. Should Xylocopa be assigned to the crop or leg collectors? SCHREMMER (1972a) threw light on this problem too, in that he recognized the comb on the stipes of the maxillae as a pollen collector, parts of a whole pollen-collecting apparatus. A survey of the various food plants is given for X. appendiculata by MIYAMOTO (1961), for X . virginica by BALDUP (1962), for X.orpi fex by CRUDEN (1966), for X. f imbr ia ta by JANZEN (1966), for X.uiolacea by SCHEDL (1967), for X . fimbriata, X . gualansis, X . subvirescens and X . muscaria by SAGE (1968) and for X . fenestrata and X . pubescens by K A P I L and DHALIWAL (1969).

2) O w n Observations

Within the observation area a variety of food plants grew, a t which ?? of all 4 species collected. While X . imitator and X . nigrita were only occasion- ally observed, collecting by X . torrida and X . flavorufa was in full swing.

+

Table 3: Review of food plants and visiting species in the observation area

Plant species / Family

Caesalpinaceae Cassia abbreviata

Papilionaceae Calpurnia subdecandra Sophora tomentosa Sophora inhambanensis

T i liaceae Triurnletta macrophylla

Bignoniaceae Markhamia spec.

x. t.

+

x. 1.

+

+ + +

+

+

The specialisation of X . torrida on Cassia abbreviata was remarkable. While this shrub was in bloom I saw the species collecting on no other; later I saw them in a few instances on some undefined Papilionaceae and on one Solanurn. On Cassia che bees practised a singular collecting technique, SO at- tuned to the flower morphology that I must describe this shortly:

The single blooms of Cassia grow a t rightangles to the vertical protruding inflorescence, and the opening formed by the 5 petals is approx. 18 mm diameter. If the petals are removed the pistil and 10 stamen are visible. In its natural position in the flower the pistil points towards the observer. 7 of the stamen have short filaments and are max. 7 m m long, the remaining 3 however are strikingly larger and of peculiar shape. 2 (some 15 mm long) are curved outwards like a pair of cow’s horns, their tips pointing upwards; the third (up t o 25 mm long) curves still further out, then back in until the t ip is about 10 mm over the pistil.

KIRCHNER (191 1) distinguishes in Cassia between holdfast, gustatory and pollinatory stamen. Unfortunately I had no facilities for the examination of pollen, so that I could not differentiate between the latter two. Possibly the stamen of Cassia abbreviata serve both functions. But the “holdfast” stamen are very distinct.

Approaching a Cassia flower, a bee extends the forelegs just before ar- rival and grips the 2 enormous “cow-horn” stamen, while the wings are folded

Ethological Study of African Carpenter Bees of the Genus X J ~ ~ O C O ~ U 347

flat over each other. The bee seeks with ics proboscis among the short stamen; suddenly there is a buzzing noise and the interfolded wing pairs vibrate, so that for a fraction of a second the calyx is “filled” with pollen, which sticks to the hairs fringing the back of the head, and to the thorax hairs (mainly dorsal), and is immediately cleaned off. Grooming inovements followed each other so rapidly i t was impossible to make a sequence analysis, and I can only state which legs groomed pollen from which parts of the body. The forelegs clean the head, being applied at the back and drawn down to the front, whereby head and leg hairs cross each other and the pollen is brushed into thc leg hairs. The thorax is groomed by the mid legs; to reach its upper parts, tibia and tarsus are turned upwards, the tibia seeming to be inverted, as in a mirror, over against its normal position on the femur. On the thorax too, cleaning is from back to front, against the hair grain. Pollen is first caught in the mid leg hairs, and is transferred to the hind legs. But this often occurs when the bee is already i n flight again, when similar movements may be observed to those of the pollen collecting honey bee. Finally the pollen is concentrated mainly in the hind leg hairs. I did not observe that the forelegs transferred pollen to thc inid legs.

This singular collecting technique a t Cassiu flowers was shown by 99 of X. torrida, X. flavorufa and X . nigrita. X . imitator-?? collected without wing vibration. These are only half as big as ?? of the other species, so that when visiting they are not squeezed in between the pistil and the overhanging stainen tip. Possibly the touch of this stamen on the bee’s back releases wing vibration in the larger species - a stimulus non-existant for the sinaller X. imitator.

Visiting other plants, 09 of all 4 species hang quietly on the flowers, dipping the head into the calyx. Here the wings are not folded in flat layers, bur held out sideways so that the abdomen is uncovered. Usually only 2-3 blooms are visited consecutively at one inflorescence, and then the next is approached. And sometinies bees return to blooms at which they have recently collected.

Thc collecting activity showed a circadian rhythm, given in Fig. 5 for S. torrida on Cassia abbreviata. A corresponding rhythm was observed for the other 3 species.


Based on his studies of flower biology VAN DER PrjL (1954) formed a separate category of Xylocopu flowers, for which he gave 9 criteria. KUCLEK (1972) is reserved about this classification, as 8 of the 9 criteria would equally

He thinks ecological flower classifications well gpply to Bombus flowers. should be made only when “there is a clear and denion- strable conformity between the construction of a flower and the behaviour of the pollinator group concerned, not however when flowers are visited and pollinated by a certain group of animals merely because other

F i g . 5: Circadian rhythm, occurrence of X . torrida on Cassia abbreviata. n = no. of animals; t = time of day

2

0

10

L :i 0 2

i L 8 9 10 11 12 13 1L IS 16 17 18Itl


equally efficient pollinators are not present in the biotope”. This is indeed the case here, for there are no bumble bees in Africa south of the Sahara, and the carpenter bees occupy their ecological niche. Furthermore it seems, at least for those species I examined, that the last remaining criterion for Xylocopa flowers, i. e. the “pale, unsaturated colours”, does not apply. All flowers of the staple food plants, without exception, had a saturated yellow colour. Apis and Bombus have spontaneous preference for saturated rather than unsaturated colours (KUGLER 3 970). No similar results exist for Xylocopa, but it may be assumed that their colour spectrum and colour vision are comparable. And JONES and BUCHMANN (1974) have shown that Xylocopa species react to ultra-violet flower patterns exactly as other Apids have long been known to do.

The observed methods of collecting on Cassia abbreviata were already described before me by WILLE (1963) for X.gualanensis on the same plant genus. MICHENER (1962) and SAGE (1968) report a similar “buzzing technique” for various Xylocopa species when collecting on the Solanum genus. But on flowers of this genus I observed only quietly-collecting Xylocopa.

I am of ScHREhmER’s (1972a) opinion that pollen brushed from the head with the forelegs is received by the mouthparts, swallowed and carried home in the crop. At any rate I could perceive no foreleg and midleg interactions during pollen removal. On the other hand my observation contradicts SCHREMMER’S, who saw pollen brushed from the mid legs transferred to the forelegs and swallowed: the complete collecting process therefore would begin with the removal by the mid legs of pollen attaching to the notum, which is then transferred to the mouthparts via the forelegs. Pollen on the sternum however would be removed by the hind legs and carried home in the metatarsal hairs. In the species I observed, mid and hind legs formed an opera- tional unit, whereas the forelegs operated in isolation.

For this process there are probably various behaviour routines in the various carpenter bee species, there may even be variations in one and the same species, depending on the flowers from which the bee is foraging. Only high frequency film exposures allowing analysis of the behaviour elements of collecting 99 can help us here. This would also settle the question of pollen transport on the hind legs, which has occupied many authors (BRAUE 1913, FRIESE 1923, BISCHOFF 1927, MALYSHEV 1931, SCHREMMER 1960), and which SCHREMMER (19724 could answer very plausibly. To this I have only one result to add. To find an answer for the observed species, I barred the entrance to the living-burrow of collecting 99 with mesh. Returning home, they alighted on the mesh and bit fiercely into the wire, but remained perched on it, so that they could be closely observed and photographed. The bees were seen to be carrying a considerable pollen load on the metatarsi of the h h d legs. But also the tibiae and the side abdominal hairs were fairly well loaded, while all other parts of the body were practically pollen-free.

IV. Reproductive Behaviour

1) Construction of the Breeding Cells

a) Own Observations There are two prerequisites for the construction of the breeding cells: the

tunnels must have reached a minimum length (40 mm, also for the smaller species X . imitator), and food plants must be blossoming in large numbers. If

Ethological Study of African Carpenter Bees of the Gcnus Xylocopu 349

both conditions are fulfilled, then construction of the cells begins, without the bores being further prepared. First the ascending bore is fitted out with several cells and then, if there is one, the descending bore. N o t once did I see a whole burrow system completed prior to the equipping of the cells; only when these have bcen completed i n one bore is the next bore gnawed out. The bee is busy practically all day, collecting pollen and nectar and fashioning the provisioning mass. But unlike BRAUNS (1913) I failed to observe of X. f l u ~ o r u f u that “ in mild summer nights they work far into the night.” Nor did the other species continuc flying after sunset.

Collecting flights lasted from 15-25 min, upon their return the bees spent max. 15 min in thc burrow before flying out again. They often returned with very varying loads (at least of surface pollen), and I assume it is not the load which triggers the homeward flight, but that the period of absence from the nest is the limiting factor. This is understandable, as pollen lying exposed in the nest will attract other insects, particularly ants. After every absence the bee’s first job is to chase a few unwelcome visitors from the burrow. Short- er periods of collccting mean more likelihood of being on hand when an intruder appears. The periodicity noted a t the food plants (Fig. 5) agrees well with obscrvations a t thc burrow. Between 8.30 h and 11.30 h, and between 16 h and 17 h the animals collect briskly, between 11.30 h and 16 h they arc normally to be seen a t the burrows. save for the few which start collecting from 14 h ; the small amounts of pollen clinging to these returning bees indicate that a t this time the food sources are not very bountiful. 1 could not de- tcrniine whether only pollen or only nectar was collected from any one plant, or both at once. Pollen is certainly the main haul from Cusriu. O n these bushes 1 caught especially many X. tovridu for marking. Under the anaesthetic the Z; d’ regularly regurgitated the croD contents (reaped from other plants, as 8 Z; nevcr collect on Cassia). The 99 did not regurgitate, although they werc caught while collecting. As the bees are unlikely to react sex-specifically to anaesthetic, it appears that the 99 do not collect nectar from Cusriu, or only i n i nor quan ti ties.

The grooming behaviour shown by the 4 Xylocopu species on their return from collecting is remarkable. In this way the pollen is unloaded in the burrow. If the bee is near the entrance, one can observe more or less the same motions described for flower visiting. Removing pollen from the hind legs, position is held i n the bore by the forelegs only. The main motions consist of rubbing the legs together whereby, always in alternation, one leg is braced firmly and the other brushes pollen from it. The metatarsal brush of one leg is applied to the other leg at about the transition point from tibia to tarsus and is moved downwards repeatedly, and one sees little rolls of pollen “run- ning out of thc praetarsi”. This is not the work of the hind legs alonc, however; thc mid legs intcract with them, in particular brushing pollen downwards from the outer metatarsus and the tibia of the hind legs. The abdominal sidc hair cover is groomed exclusively with the hind tarsal brushcs, the pollen bcing transferred to the hind legs with very strong, synchronized strokes. At times a short buzzing is heard, perhaps any remaining pollen grains arc thus shaken out of the hairs. The wings are always left unt i l last, being pushed between the hind legs and abdomen and cleaned by wiping and stroking. movements of the abdomen directed from the foremost edge of the front wings towards the back wings, whereby the legs merely provide rssist- ance and themselves do no cleaning. These grooming motions can also be observed in Z; d’.


A provisioning mass is formed from the pollen hoard, with just enough nectar for the pollen grains to adhere firmly, and the whole to the wall. This mass, similar in shape to a well-risen loaf of bread, is applied to the cell side and top (in an ascending bore) and to the bottom (in a descending bore). The completed X . imitator provisioning mass weighed 1.3 g, 1.2 g and 1.2 g; that of X. flavorufa 2.1 g and 2.0 g; and of X . nigrita 2.4 g and 2.5 g.

The bee lays her egg on the provisioning mass. I was unable to watch this, but could nevertheless follow the process by measuring bore length daily with a probe. A newly constructed breeding cell shortens bore length by approx. 2 cm. The height of these cells (in opened burrows) was 16 mm for X . imitator, and for the 3 larger species 18 mm. Terminal cells measured up to 2 mm more.

Apparently the bee has a conception of the necessary size of a provisioning mass; when the load of pollen was repeatedly removed, one animal continued to carry home supplies for 5 days, after which she did not return. When an almost completed provisioning mass was removed, one bee nevertheless laid an egg, while two others faced with the same situation continued collecting. It was technically impossible to make reverse experiments, so that I cannot say whether bees would have reacted promptly by laying eggs if they had suddenly been presented with a complete provisioning mass.

For the partitions the bee gnaws chips from the walls, mixes them to a putty with saliva and forms a flat spiral with 5-6 coils (Fig. 6). All 4 species adopt this method. This spiral forms the flooring of the closed cell, but is not at the same time the ceiling of the next cell, for which the bee provides a smooth additional “finish” composed of saliva and much finer wood particles, this surface curving down at the edges to meet the walls. The same smooth finish also coats the ceiling of the rear, or terminal, cell, i. e., a bee terminates a bore in this way before provisioning. All breeding cells therefore show the same textural contrast: sides and ceiling smooth, floor rough. For all 4 species the provisioning and closing of a cell takes from 1 ’ / 2 to 2 days. The number of chambers lined up in a bore was found to be very uniform: in ramified sys-

Fig. 6: X. ~ Z U ’ U O T U ~ U burrow; 2 intercell walls showing spiral construction


tenis I found no more than 3, mostly 2 chambers, in single-bore burrows there were at most 4 such chambers.

b) Review of Literature and Discussion A number of authors have dealt with breeding cell construction: NININ-

GER 1916, BODKIN 1917, FRERE 1927, MALYSHEV 1931, KAPIL and DHALIW~M, 1968b and 1969. MALYSHEV (1931) found in X . v a l g a and FRERE (1927) in S. amethystina a palpable intraspecific difference in cell size, and both at- tribute this to short “male” and longer “female” cells. MALYSHEV also found provisioning masses of different size, but no other authors report such observations. O n the contrary, BODKIN (1917) writes (of X . fimbriata) that all cells were provisioned with the same amounts; this accords with my results for the 4 species observed. Both MALYSHEV and BODKIN report, however, that X . valga and X. fimbriata coat the insides of their breeding cells with saliva (which is even watertight in X . valga), bu t this has been reported for no other X?/~OCOPU species.

Data on provisioning mass size is very vague, e. g. “as big as a bee’s own body”, or “piled up half as high as the cell”. Only BODKIN (1917) gives the X . fimbriata provisioning mass as 2.5 g. MALYSHEV (1931) however gives exact details of its form and deposition. WAGNER (1958) tells us that in X . tabaniformis it is fastened to the cell ceiling by a stalk. FLORENTIN (1904) notes the chemical components of the mass as: Glucose 55.9 %, Sacharose 3.0 % and insoluble remnants (pollen) 41.1 % (for X . violacea).

According to KAPIL and DHALIWAL (1969), a X . fenestrata 0 undertakes 20.5 flights during 75.4 h to collect material for 1 provisioning mass. It would be interesting to learn from such investigations how much pollen is carried per flight; for this might reveal what i t is that prompts the bee’s return to the nest.

If, as I surmise, a certain predator pressure compels the bee’s periodic return , flight periods will be regular, and independent of the pollen load, which will vary greatly according to what is offered by the food plants. SCHREMMEK (1960) reported for X . valga that flowers once visited were not approached again unt i l 1-2 h later, the bee probably leaving a signal for itself and conspecifics about the recent spoliation, thus obviating wasted visits. But I failed tc make such an observation with the 4 species observed.

SKAIFE (1952) describes for X . caffra and KAPIL and DHALIWAL (1968 a) for X. fenestrata a particular behaviour pattern of the PP. Apparently they impregnate burrow entrances with a rectal gland secretion which repels ants for a time. In this case the 99 can safely allow themselves longer absences, returning home only when they have collected a certain pollen quota.

All authors agree on the spiral construction of the partitions. but there is less unity about where the material is taken from. REAUMUR (1742) says that the bee gathers ejected sawdust lying on the ground and carries it back in. And WAGNER (1958) once observed a X . fimbriata 9 carrying in a little roll of wood for partitioning. Experimenting with coloured sawdust MALYSHEV (193 1) could finally show that the material is taken from the inside of the bore; and 1 observed that this occurs directly beside the “abutments” left for the partitions. 1 consider this observation endorsed by the fact that oft-used bores ac- quire the appearance of a string of beads.

2) Behaviourof 8 8 I n X . torrida, X . flavorufa and X . nigrita I could study the behavinur of

d 8 closely, especially that leading to the encounter of the sexes.


HAAS (1960) gave very clear descriptions of the flight courses observable

I. Simple swarming courses, which show no relationship as yet to the feeding locality

2. Feeding locality courses, in which feeding localities and swarming areas are largely congruent

3. Swarming courses correlated to feeding localities, in which although feeding locality and swarming area are separate, the 8 8 uphold a constant connection.

On the whole the observed species showed flight courses comparable with the feeding locality course; yet they were so dissimilar that I would like to describe them separately.

Xyfocopa torridna: Save in the midday hours, 88 could be observed throughout the day on Cassia abbreviata, but without collecting from these flowers. They flew at least 1 m above ground, circling the bushes at a distance of 1-6 m. Flight elevation seems limited by bush height, for I seldom saw cTd swarming above the bushes. Having commenced circling, 88 fly without change of direction, but centre upon first one, then another bush. A regularity of circling was discernible, especially for 2 8 8 whose flight path lay in full view in an area with 3 bushes (nos. 2, 3 and 4 in Fig. 1). The other 8 8 too, although they were out of sight a t times, returned periodically to certain points. Not once did I observe 8 8 alighting on a bush, or behaviour in any way resembling scent-marking of the bushes. The 8 8 were observed to be tolerant of each other, that is, any one 8 was not chased more frequently or specifically than were sometimes butterflies, dragon-flies or even swallows.

6 6 fly to the feeding locations earlier than the 99, remain there longer towards midday and return earlier after the midday pause (Fig 5). Only in the late afternoon hours are 99 alone here, but these are old 99 (with badly damaged wings) which have spent the day guarding their brood (see chap. V. I) . It is conceivable that the longer period of activity of the 8 8 ensures that all young 99 ready for copulation will be mated.

Xyfocopa ffavoruja: These 8 8 too circle the food plants. As 99 arc not so strictly committed to one plant species as in X . torrida, the 8 8 too fre- quented various plants, principally Papilionaceae in the shore region. A B takes possession of a swarming territory round a bush, from which cvery intruder (intra and interspecific) is chased. Chasing off an intruder is a short operation, I never lost sight of the territorial bee in the process, and circling is resumed immediately. The flight courses and manner of flying of X . {lnvo- iufa 8 8 are remarkable: a horizontal 8 is executed in the top third of the bushes in a series of jerks, whereby the abdomen points inwards towards the bush and the eyes are directed outward a t the environment. 8 8 can be seen on the same bush for up to 6 weeks. Not all X . flavorufa 8 8 own and defend such a narrowly circumscribed territory, sometimes there were several together on Cassia. Strangely enough they then showed the same behaviour ns X . torrida 8 8 , that is, they were intra and interspecificall’y much more tolcr- ant than their conspecifics having individual territories, nor did they fly the “8” course. I saw no scent-marking in this species either, but X. jlavorrrfn does collect from bushes in the territories. Flying periods agree largely with those of X . torrida, but X . ffavorufa is generally active until shortly before sunset, and so has the longest period of activity of all 4 species.

for the various Apids, and distinguished the following 3 basic types:

.


Xylocopa nigrita: The 6 d circled bushes not in bloom; out of 5 observed cases, 4 of these were Jasminum dichitomum (Oleaceae) and 1 was Erythrina uhyssinica (Papilionaceae). The bushes were of different height, circumference and foliage profusion. In this species too the height of a bush seems to limit flight elevation. The bushes in which d d hold their individual territories are circled many times without change of speed or direction. The noise of their Ilying can be heard by the human ear for about 100 i n . Sometimes the animals alighted on leaves or twigs, presumably to rest, bu t here too I could see 110-

thing indicating scent-marking. Sometimes in a territory a fight between 2 8 8 occurs, always progressing similarly: a 6 invades the territory of another, and a t first both circle, either in the same or opposite directions. Suddenly they hover confronting each other, circle each other a t a distance of 10-SO cm, then rush together, so that their bodies can be heard to clash. This may be rc- peatcd several times, until the intruder quits the territory without being ihased any further by the territory owner.

3) Copulatory Behaviour

In the abundant literature (see following discussion) on the swarming behaviour of Xylocopa, copulatory behaviour is rarely mentioned. Either no meeting of d d with 99 could be observed (JANZEN 1966), or there were no copulations (VELTHUIS and CAMARGO 1975). CRUDEN (1966) describes a few single observations in detail, but then says merely “6 8 and 99 were observed to fall onto the ground, where copulation probably occurred”, and “copulation probably occurred during the 30 to 90 s on the ground”. FKIESE (1923) writes of X . viofacea that d 8 enter all manner of holes searching for the OQ. In order to copulate the 6 6 seize the 99 on the tips of twigs, where they sit waiting. Copulation time is 3-5 min. W. LINSENMAIER (pers. com.) confirms this. My own descriptions of the copulatory behaviour of X . torrida, X . f favorufa and X . nigrita follow.

Xylocopa torrida: The mid legs of the 6 6 are curiously fashioned (Fig. 7). The basal end of the femur is considerably widened and drawn to a

I I Fig. 7: Left mid leg of a X . torrida- 8, outside view. Note the femur spike,

the elongated metatarsus and hair-covered praetarsus

23 2. Tierpsychol., Bd. 44, Heft 4

354 GUSTL ANZENBERCER

point at one side. The tibia has a normal form compared with those of thc other leg pairs, but not so the metatarsus, which is nearly as long as the ti,bia (although this is not unusual in bees) and extremely flattened. Both its sides are closely covered with hairs approx. 3 mm long, which seem to be “trimmcd” in a certain shape. The next 3 tarsi show no aberrant form, but the praetarsus is hair-covered like the metatarsus. As this peculiar leg form occurs only in 8 8 , I assume it is for holding the ?? during copulation.

To find out, I fastened X. torrida 90 between abdomen and thorax on a thread some 2 m long, and let them fly beside a Cassia bush circled by 5 5. The 8 8 actually seized 90 so presented and held fast, even when 1 drew thc pair down to eye level to see exactly what was happening. Fig. 8 shows thc copulation position. The 8 rides the ? and thrusts in the extruded point of the femur behind the 0’s wing base, the mid legs are stretched forward, bring- ing the long-haired metatarsi to lie over the eyes of the ?, while the praetarsi hold the bottom of the head. The forelegs lie practically upon the body, and do not clutch the 0 . The hind legs lift the 9’s abdomen slightly, whereupon tlic 6 is firmly anchored with his enormous copulatory apparatus in the 0 .

I. I _ _ . _ -. /.r . _

Fig . 8: Copulatory hold of X. torrida, 8 (dotted) astride the 0 (cross-hatched). Mid leg of 6 is black; point of wing attachment in 9 is a black circle, white margin, the heavy white line through this symbolises wing position. Further explanation

in text

The copulation of undisturbed pairs also occurs in flight, at a height of about 5 m, and lasts some 20 s . The wings of the ? are held out sideways horizontally, immovable, and the ? glides. Normally only the 6 makes forward flight motions, and only if this is the case can one observe a more or lcss straight flight of the pair. If the 9 makes wing motions of her own they rnpid- ly lose height, but recover about 1 m from the ground, i. e., the ? resumes thc gliding position and the 6’s flight motions lift the pair again. This whole yro- cess sometimes gives a wavy line to the flight. It seems to me that the partncrs are unable to achieve synchronization of their wing movements, that the motions of the 8 alone suffice to maintain flight elevation, and that attempts OF the 0 to fly cause a fall. This would explain the extremely long hairs of thc metatarsus: besides ensuring that the tarsus lies firmly over thc 0’s eyes without slipping, they might also serve to screen those compound eyes from optical stimuli, and so hinder any flight manoeuvering.

After copulation the 0 is suddenly released and flies away, the B returns to the flood plants. I cannot say in what way the 8 6 recognize thc willing- ness of the ?? to copulate. Sometimes a 8 follows a collecting ? as far as 10 flower stations on a bush, and clutches it as soon as i t is sufficiently clear of the foliage. Those ?? set free after having been anaesthetized and marked were particularly often followed by 8 8, but there was no copulation.

Ethological Study of African Carpenter Bces of the Genus Xyiocopa 355

X . flavorufa: Swarming 6 6 await the 99 a t the feeding localities, seize arriving or collecting 99 in flight and copulate. The copulation flight is as already dcscribed, 99 hold their wings still and stretchcd horizontally, only the d 6 making flight motions. Attempts of the 9 to fly result i n immediatc loss of hcight. In this connection I several times obscrvcd a particular behaviour in X. flavorufa. The d 6 flew mainly among Papilionaccae a t the water’s edge, and copulation flights always proceeded out over thc watcr. The shore vcgctation formed a high, wide wall, and may have prcvcntcd inland flights. A copulating pair, having lost much height through the 0’s manoeuvres, parted about 1 i n from the water’s surface, both rose, and the 6 again scizcd thc 9. They may part simply to avoid a wetting, or perhaps. 6 B of this spc- cics simply let go more easily, for I never succeeded i n pulling down to cyc level a tethered 9 together with the riding 6. I can thereforc rcport only that thc mid legs (which in common with the other legs have no spccial structurc) clutch a t the thorax of the 9, her abdomen is slightly raised by the hind legs, and the forelegs do not participate in the embrace. I n this species, too, copulation lasts approx. 20 s, the 9 then flies away, while the d returns to his territory.

Xylocopa nigrita: As mentioned in describing territories, 6 d circle bushcs not i n bloom. Once I observed a pair copulating on a twig. After a fcw s thcy disengaged, whereupon the 9 flew off. I cannot say whether the copulation actually started there, or whether the pair landed there while copulating. T offered tethered 99 to the swarming d 6 of this species too, but they rc- sponded quite differently from 66 of other species. They did not approach the 99 to seize then1 but, as soon as I approached with thc flying, tcthcrcd 9, circled closcr to the bush. From time to time they flew into the bush, but did not settle on leaves or branches. This response could be elicited at any timc by presenting a tethered 9: as if the B 6 were fastened by an invisiblc string which was shortened by the presence of 99, the radius of thcir circling thc bush decreased.


The behaviour of Xylocopa d d is described by BRAUNS (1913), FRIESE (1923), LIEFTINCK (1955), HURD (1958), JANZEN (1964), and by CRUDEN (1966) and VELTHUIS and CAMARGO (1975), who also deal with territorial behaviour, while SAGE (1968) and MICHENER in HURD (1958) list indications for this. I consider that only VELTHUIS and CAMARGO actually succeedcd in proving thc existence of individual territories, in X . hirsutissimu, in showing that certain d 6 drive intruders from the home range. The mandiblc gland secretion of the 8 6 plays a decisive part in the recognition of othcr d 6: scraps of paper drenched with this secretion were equally subject to attack as intruding 6 6. There are many indications, for this species and X . tubani- formis melanosoma ( JANZEN 1964) that swarming 6 6 perform scent-marking, as many solitary and social Apid species are known to do. Certainly thc authors did not observe that the scent-markings were also attractive for tlw 99, i. c. served to bring the sexes together, nor could they prove this indircct- ly. But this is probably an oversight, and we may assume that i n Xylocopcs conditions corresponding to those of their relatives obtain.

If thc species I observed are regarded from the angle of their swarming and copulatory behaviour combined, distinct differences cmerge. Numbcrs of X . torrida 6 6 fly round the food plants, are less mutually aggressive and meet the collecting 99 there. X. flavorufa 6 6 energetically defend individual


territories at food plants against other 8 8 and wait there for the 99. These 2 species therefore show “feeding locality courses”. In contrast the “simple swarming courses” of X. nigrita 8 8 have no recognizable link with the food plants. Encounters with 99 occur in the male territories, and not by chance elsewhere. But how do the 99 recognize the territories? We do not know how well carpenter bees hear. It is feasible that the inordinately loud flight noise of the 8 8 could have a signal function for the 99. As already indicated, 1 think it probable that in some Xylocopa species the 8 8 scent-mark their tcr- ritories, as do other Apid 8 8. But SCHREMMER (1972 b) pointed out that i t was long mistakenly assumed that all bumble-bee 8 8 had such scent-marlccd swarming courses, bu t that these had merely not yet been discovered. He thcre- fore investigated the behaviour of the large-eyed Bombus C O ~ ~ U S Z L S 88 and was able to show that their courses are not olfactory but visual. HAAS (1949) had already considered this possibility for Bombus mendax 8 8 because of their “drone-like’’ eyes.

From the portraits of 8 8 of 3 Xylocopa species (Fig. 9), a graduation in the proportions of eye/head surface is evident. If we exclude the clypeus, thc eyes of X. torrida 8 8 take up almost the whole head front. In X . flavorufa i3 8 the eye/head proportion is similarly high, whereas i n contrast the eyes of X . nigrita 8 8 are only half as big. And we recall that the swarming coursc type of X . torrida and X . f lavorufa was different from that of X . nigrita. It is my hypothesis that the “feeding locality courses” of the 2 former species can be regarded as visual. whereas the “simple swarming course” of X. nigrita is also (or exclusively) olfactory.

Certainly the eyes are not only useful to identify points on the flight courses, however; visual stimuli will figure largely among others in recogniz- inq 99. And here, too, different demands are made of the visual performance of $6, if we examine more closely the meeting of the sexes and female behaviour thereat. X . torrida and X . f l avoru fa d d encounter the 99 g t the food plants. The 99 therefore meet the 8 6 at a locality visited by 99 for collecting (even if the 8 8 do scent-mark the feeding locality courses, which according to my observation is unlikely). From numerous 99, the 8 8 choose those ready to copulate and seize them for copulation in flight, virtually as- saulting them. For X. n i ~ r i t a there is no combination of interests, as the swarming courses of d 8 do not centre on the food plants. The 99 must therc- fore seek out mates wherever these are. Moreover. copulation secins to talcc place while sitting, for 8 8 were not attracted to 99 presented in fliqht - indeed, their behaviour indicates that they were endeavouring to entice the 99 into the bush.

A comparative investigation of the X.ylocopa species’ various swarming course types would be a most attractive task, especially as so far, in contrast to the abundant findings for bumble bees and other Apids, no results are available.

V. Defence Behaviour of 99 1) Guarding the Brood

Having constructed her breeding cells the bee sits in the burrow nearly all day, protecting her progeny by her presence. By now wings and haircover are sadly worn, and the animal looks extremely passive. She leaves thc burrow 2 or 3 times a day, first about an hour after sunrise to defecate, hovering, just before the home plant, and fly back immediately. In the late afternoon

Ethological Study of African Carpenter Bees of the Genus Xylocopu

._ . . - . - . . .. -

357

I

I

I - 1

Fig. 9: Same-scale portraits of 3 Xylocopa species, left male, right female heads: a) X . torrida, b) X. f luvowfa , c) X . nrgrita

shc undcrtakes a collecting flight, or perhaps two?). Upon her return thc pollen is brushed from her hairy coat, for which she sits immediately abovc thc burrow cntrancc hole, with only the abdomen and the intensively grooming hind

2) Leaving the burrow, thc Lee docs not fly directly from the entrance hole, but first crawls a few cni higher, pushes off and flies away. In returning, howcver, she flies directly in a t the hole, stretching out the forelegs to land and pulling herself inside, the wings now folded close. The bee never alights beside the hole to continue “on foot”.


legs visible. The pollen is no longer hoarded, but deposited outside. Apparent- ly the food carried in her crop suffices until the next day’s collecting flight. Collecting flights of cell-guarding 99 usually last longer than those of cell- provisioning ones. A flight could last up to 45 min. This may be due to the heavy wear and tear of wings, or to the fact that cells are now closed, although this does not mean that closed cells are safe; if the mother is lost, ants may be observed to enter the burrow within a day, break open the cells and destroy and carry off all their contents, even pupae just before the imaginal moult. The loss of a guarding 9 means the inevitable loss of her entire progeny.

A carpenter bee burrow can be very effectively defended. A single entrance leads to the bore system, of just sufficient diameter that the bee’s body fills it. Any noise in the vicinity (e. g. flight sounds of other insects), or a shadow falling upon the hole, a t once alerts the bee to look out. This de- monstration nearly always suffices for protection. Other carpenter bees, especially d 8, or sometimes other Hymenoptera species, may show interest in the burrow.

2) Special Defence Behaviour

The following behaviour patterns were artificially induced, mostly by inserting a dry grass stem into the burrow entrance.

Defence with the mandibles: immediately I started scratching lightly at the hole with the grass stem the bee appeared and buzzed quite audibly, with vibrating wings. This buzzing consists of a series of short regular sound ejacu- lations, and can best be described as a “buzzing churr”. If I pushed the stein into the hole the bee bit into it fiercely, buzzing all the time, and tried to push i t out. Directly I let go she succeeded. I once observed this mandible defence in a natural situation, when a 9 defended her entrance against a 6 . The buzzing churr of a 9 promptly brings all other 99 in the same home plant to their entrances, to look out.

Defence by defecation and sting: If I held on to the grass stem and waggled it in the entrance, the bee desisted after a short time and settled above the entrance hole, in the bore. She sat straight up, with the abdomen visible a t the upper edge of the hole (Fig. 10a) . At short intervals, and nc- companied by rhythmic buzzing, she squirted out watery bowel contents, nnd now and then the “flash” of the sting could be seen.

Defence by blocking the entrance with the abdomen: If all else fails, the bee attempts to block the entrance with her abdomen; she slips further down in the bore, then braces her body with her legs sideways and - probably with the notum pressed opposite the entrance - she wedges the curved-up abdomen against the inner rim of the hole (Figs. 10, b, c). The dorsal side of 3 shiny black abdominal rings is visible. As in the earlier stages of defence, this blocking of the entrance is accompanied by loud buzzing. The bee stays there until the disturbance stops, when she again sits directly above the cntrancc. She never jerks up suddenly from this blocking position to use her sting.

The three forms of defence behaviour occur in the order described, and depend on intensity and duration of the disturbance. I could observe them in X . torrida, X . flavorufa and X . imitator.


It is known of many carpenter bee species that 99 remain i n the burrow after constructing the breeding cells. It has even been shown, for most tropical

Ethological Study of African Carpcnter Bees of the Genus Xylocopa 359

a b C Fig. 10: Nest dcfcncc. a-c dcfcnce positions. First the sting is used (a), then the bee settles (b),

and finally (c) blocks the entrance with her abdomen

and subtropical species, that the mother encounters her newly-emcrgcd young. There is however no indication of this for the European X. violncea and X. wafga, which simply leave the provisioned cells in their burrows, although X. wafga does finish off a row of cells with a particularly thick closure (MALYSHEV 193 1 ).

X. caffra and X. fenestra seem to have developed a really perfect method of protecting the nest from unwelcome intruders (see chap. IV,I b), even if entrance impregnation alone is an insufficient protection for the brood. J sharcd with various other authors the experience that the animals do not even sting when one breaks open their burrows. Only X. frontalis is, according to SCHROTTKY (after MALYSHEV 1931) and MICHENER and MOURE (after HURD 1958) very aggressive and attacks when there is a disturbance at the nest. X. fimbriata OQ squirt faecal fluid out of the burrow with considerable strength when disturbed (JANZEN 1966).

LOVERIDGE (1923) observed nest-blocking behaviour in X. tovvidu carlicr than I, and considered that bees blocked while resting. Although he dcscribcs exactly how the dorsal surface of the abdomen is pressed hard against the entrance hole, he nevertheless thinks this is done in readiness to sting. I cannot agree, as with a curved abdomen blocking the entrance the sting points inwards (Fig. 1Oc). Entrance blocking is in my opinion a defcncc against other insects, principally ants, whenever these attack in large numbcrs. Two cxainples may illustrate this. Naturally I often reflected how 1 could watch what was going on i n the living tunnels and breeding cells. To this end I cut tiny windows in the bores, covered them with cellophane and scotch tape and placed pieces of bark over them. But I quickly abandoned this method, as ants unfailingly entered through the windows and destroyed the wholc burrow. LAMPRECHT (pers. com.) had a similar experience when trying to watch thc development of X. flavorufa. A few days after the observation windows had been made, the whole burrow was cleared out by sausage ants (Anommn spec., Dorylinae). These are eloquent examples witnessing to the efficacy of entrancc-blocking by the bee. It makes sense when there is i n fact one ciitraiicc hole only, and this is guaranteed, as the bees newr break through into a ncighbouring system when boring, or to the outer world (see chapter I1 2 a). A furthcr examplc illustrates how scrupulously the bees attend to thc intact state of their burrows. Having abandoned the window incthod of obscrvation as impracticable, I tried inserting a wooden plug about 3 cm ahcad of new

3 60 GUSTL ANZENBERCER

bores only a few cm long. These plugs fitted very exactly and tightly across the bore direction, and I expected the bees simply to tunnel on through the plug, so that later I had only to remove it to inspect the inside of the burrow. But in every case the bee either stopped the bore about 1 cm before the plug, or led it past the plug at a similar distance.

A single entrance, an intact burrow, and the survival of the mother until the young emerge are indispensible conditions for the survival of the brood.

These conditions also apply for X. nigrita, although here indeed another 0 may substitute for the mother in protecting the young. In burrow N 5 (sec Table 2) I once caught the second ? and kept it captive for a day without any harm befalling the breeding cells, although the burrow was certainly within reach of ants. In the ocher 3 species removal of the 0 for a day results in loss of the brood. One surviving X. nigrita ? of a commune is therefore able to protect the progeny of several 99. I was unable to induce or observe entrance- blocking in this species, defence is by biting with the mandibles, pushing motions of the head and use of the sting. Several 09 living together in one burrow system also defended it together. If I pushed a grass stem into thc in- trance, one ? promptly alarmed the others with her buzzing churr, and these crowded behind the entrance hole. They attacked the grass stem in turn, and one can well imagine an intruder would have a job to force entry past this female phalanx, with their concerted buzzing to boot.

VI. Ontogenesis

1) TheEgg

The southeast Asian X. orichalcea and X. auripennis lay the largest known insect eggs (IWATA 1964). MALYSHEV (1931) found a sexually specific size difference in X. valga eggs. BODKIN (1917) writes that X. fimbriata eggs increase in size as they ripen. The incubation period of X. orpifex and X. vn- ripunctata is “about 1 week” (NININGER 1916), and of X. valga 5 days (MALYSHEV 1931).

I collected eggs of X. imitator (3), X. nigrita (2) and X. f lavorufa (2) and observed their development. The eggs of all 3 species are a dirty hynlinc

Fig. 11: X. fi’uvomfu egg on its provisioning mass (here not in its natural form). cm scale below


yellow, taut, slightly curved, rounded off a t the ends and with a round cross- section constant along nearly the whole length. The length of a flavorttfa egg (Fig. 11) is 13 mni, diameter 2.5 mm. The measurements of X . imitator (10 mm, @ 2.3 mm) are a little less, those of X . nigrita (15 mm, @ 2.7 mm) a little more, corresponding roughly to adult size proportions. Within the spc- cies the eggs were of equal size, those of X. imitator were 2 99, 1 8 , and of X . nigrita and X . f lavorufa 2 O O respectively.

The egg lies with its concave side to the provisioning mass, adhering along its whole length. No alteration in the egg is apparent during the firs1 2-3 days after laying. On about the 4th day one sees in the front quarter a faint constriction all round the egg, with a more pronounced curvature i n this region and an increased volume of the back part. The larvae hatch out a day later, so that egg development lasts some 5 days.

2) The Larval Stadium

The larva leaves the egg head first, the chorioii is sloughed, it stays at first appended to the end of the body and falls off finally after 1-2 days.

The larvae are light yellow, the 14 parts of the body are divided by distinct constrictions. Part 1 carries the head capsule, parts 2-4 are separated by a dorsal indentation reaching down as far as the middle of the sides, thc constrictions marking parts 5-14 encircle the whole body. The anus opcning lies terminally, a short slit at rightangles to the longitudinal axis. The stigmata opcnings lie dorso-lateral in parts 2 and 3, and 5-12. In X . nigrita larvac these are framed a reddish-brown (Fig. 13).

P

I I

I

I - - A ..

I-_-_-- -

Fig. 12: 7-day-old X . flav0~14fu larva from above with provisioning mass

As typically apodal Apid larvae they have no clinging organs, but adhere to the provisioning mass with the curved ventral side. A few hours after hatching the larva begins to feed, and one sees scraping motions towards the body. The front part describes a flat arc from left to right and back. Sonic 100 feeding motions per min are made, almost without pause, except briefly for thc larva to alter position on the mass. The head end however does not move while the abdomen shifts right or left, perhaps the larva holds itself i n position by its mouthparts. Finally, when the abdomen has come to rest in a new


I ‘t - r” Fig. 13: Two X . nigrita larvae,

(left), and (right) still consum-

_I

--

#. i s in the curled pupation position

ing the provisioning mass, removed for photography. The dark-framed stigmata openings

are visible

, .

spot, the head is moved after it. Within a week the constrictions have beconic more defined, and little dorsal and dorso-lateral bulges appear along thc animal’s whole length. Dark faeces can be seen shimmering through at the end of the body. At this juncture the larva has about doubled its weight, in- creasing in proportion to the provisioning mass decrease. Tne larva now no longer lies on the provisioning mass but beside it, or sometimes undcr i t (Fig. 12).

On the 7th to 8th day the first faeces are eliminated, dark brown and firm, a chain of many thin sausages some 2-3 mm long. The larva curls further round the provisioning mass, lies under it and gnawing, rolls it towards its ventral side. The provisioning is finally consumed 15-17 days after hatching.

3) Pupation

For the next few days the larva lies more or less quiescent in its cell, but continues to void, and raises itself until it leans erect against a wall, supported only by segments 8-14 on the cell floor. Some 3 days before pupation thc rudimentary extremities are recognizable; the larva has reached the pre-pupal stadium (Fig. 14). Gradually now a fluid fills the whole body beneath the surface, and the larval hull bursts dorsally, the pupa emerges. 8 days havc passed since the last intake of food; the larval stadium totals 23-25 days.

According to NININGER (1916), for the North American species X. orpifex and X . varipunctata the feeding period lasts 22-28 days, the larval resting period approx. 20 additional days. These data greatly exceed those noted for other species, e. g. X. violacea (feeding time 20 days, resting 5-6 days,

Fig. 14: Pre-pupa of X . imitator. Head and extremities are visible shimmering through

Iirhological Study of African Carpenter Bees of the Genus Xylocopa 363

REAUMUR 1742), X. fimbriuta (21 days, 2 days, BODKIN 1917) and X. valgu (23 days, 7 days, MALYSHEV 1931). NININGER’S long larval resting period may have rcsultcd from laboratory breeding. The possibility of such an artefact cannot be quite excluded i n my results, but for the total period of development (egg to imago) for the animals I bred ab ovo, there was no discrepancy between my results and those in the field.

4) The Pupal Stadium

Newly-cmergcd pupae (type pupa libera) are whitish-yellow for the first 6 days. All bcdily appendages and extremities lie more or less f lu sh with thc body; only the galeae stick out like a pen-nib under the mandibles and roof the glossa, which is twice as long and protrudes still further, ventrally curved. The antcnnae with their scapcs lie on the head, the other limbs hang straight down. The 3 pairs of legs are so astricted that each tibia lies against a femur, and tarsae pairs touch each other. The wing sheaths also contact the body and arc additionally protected by their position between the 2nd and 3rd Icg pairs. Thc pupae rest upon the abdomen, curved towards the thorax, so that they arc supported chiefly by the 2nd abdominal segment; this and thc first scgmcnt are fully extended, whereas segments 3-6 are telescoped (Fig. 15). As the main weight is on the 2nd segment, and at the utmost the 3rd and 4th still contact the substratum, the pupa can circle the last 2 segments to change its position, helped by a triangular appendage on the 6th abdominal ring (Fig. I7), which is braced on the substratum. The animal raises its wholc body by stretching thc abdomen, i t shifts a little to one side and again subsides, resting oncc more on segments 2-4, with the last 2 segments free to initiate furthcr

Fig. 15 (left): X . nigrita pupa some 10 days after pupation. Upright, as in the natural position in the cell

Fig. 16 (right): X . nigrita pupa some 10 days after pupation. Portrait, compound eyes and ocelli show darker on the head, as yet scantily pigmented


Fig . 17: X . imitator pupa shortly beforc the imaginal moult. The legs are already capable of functioning. The tibial spike on the right mid leg and the triangular appendage on the sixth abdominal segment arc clearly

visible. Explanation in text

movements. Such movements are to be seen however only when external influence has changed the pupa's position, otherwise it rests motionless in its chamber. Its inner development can be assessed by pigmentation increase.

Pigmentation begins on the 7th day of age. First one sees a delicate ochre colouring of the eyes, wings, frontal antennae segmcnts and front tarsae. Pig- mentation of the eyes progresses rapidly, some 3 days later they are already a decp red-brown. The ocelli too already appear as dark points a t this timr (Fig. 16). The other body parts darken gradually from the edges to the middle, becoming brown, while thorax and abdomen so far retain their original whitish-yellow colour. 14 days after the moult one sees here, too, a colour change, a dark peripheral ring forms on the notum and pigmentation gradually spreads to the middle; the abdominal rings too slowly darken from their margins. Within a few days the colouring of all body parts has become similar.

Three weeks old, the pupa is uniformly brown-black, and thc size and position of the compound eyes already betrays the sex. Two days later the last moult occurs. The pupal stadium lasts some 23 days in all 3 species.

MALYSHEV (1931) estimates roughly the same period for the development of X. valga pupae, and BODKIN (1917) for X. fimbuiata.

Oddly enough, about 5 days before the moult the pupae become restless. b'rom then on they circle frequently with the abdomen, changing position as described, propped too now by the mid and hind legs, no longer lying con- tiguous to the body but extendable sideways (Fig. 17). The forelegs attain this mobility some days later. This development, preceding the imaginal moult by scveral days, enables the pupa to climb about slowly in the bore in its un- transformed state, aided chiefly by the mid legs whose tibial spikelets are fully developed and hardened (Fig. 17). They already allow locomotion in the form described for adults (see chap. II,2,6). The possible adaptive value of this pupal mobility is discussed in the following chapter.

**

VII. Emergence of the Young

1) General Preface

No other aspect of Xylocopa biology has been so diversely reported as the emergence from the breeding cells. As the mother constructs a series of cells one behind the other, the problem is, how does her earlier progeny emerge without disturbing or damaging theif younger siblings? The following is a review of the many assumptions found in the literature.


REAUMUR (1742) thought the mandibles of newly-hatched X. violacea would be too weak to gnaw a passage through firm wood, so that the mother had to provide a second opening a t the bore’s far end, and close it with sawdust before constructing cells. The young could then leave the cells through this plugged opening in the order of birth, without traversing the cells of the younger siblings. This opinion is also held by KIRBY (1802)3) and WESTWOOD (1840)3), and acccptcd by FRIESE (1923).

LEPLETIER (1841):1) postulatcd a similar route for the young. H e found that the adult bcc bored into the rear end of the tunnel, close to the periphery of the timber, leaving only a thin layer easily penetrable by the young. WRAZIDLO (1883)3) supposed that the 0 prepared holes a t the sides of the cells, closing them again with sawdust. TURNER (1878)a) statcs that the young leave the burrow through the only available opening, but he docs not dcscribc emergence from the cells. DAVIDSON (1893) found burrows of X. o r p i f e x with the front cells already evacuated, but with pupae still in the rear cells. In his opinion these wintered there - a procedure unknown for any other species of Xylocopa. And he found 8 8 in thc front cells and 99 in the rear ones. MALYSHEV (1931) also reports this for X . v a l g a , but he scems to contradict himself, stating (i) that the 99 sit in the rear cells and the 8 8 in the foremost, and (ii) that the period of development is about 52 days for 8 8 , 43 days for 99. This means that young 99 would have to wait in their cells a t least 9 days before emerging - aftcr the 8 8. This 1 think i s impossible. MALYSHEV’S insistence upon allowing the later-hatched bees to cmcrgc first is shown in the following quotation: “Individuals having developed with the head towards the cell floor arc forced to turn round to traverse the common nest channel into the open. For this turning however they have to grow much stronger, and this needs a certain interval, which gives those individuals lying in front of them a chance to end their dcvclop- mcnr.” This argument is inconclusive, as elsewhere he writes of the pupae that “thcir heads point now to the floor, now to the cell cap”. FRERE (1927)z) writes, without giving further details, that young X.anzethystina leave the nest “in an order opposite to that in which the cclls wcre built”.

2 ) Own Observations

Newly metamorphosed young bees are recognizable by their light silvcry wings and the exuvien remnants still clinging to parts of thc body; thc galcac are not yet clapped against the lower part of the head, the glossa protrudcs beneath them like a bow. While the exuvien remnants take several days to fall or to bc groomed off completely, it is only a matter of hours beforc thc wings attain their final colouring; they are a shining blue-black aftcr about 6 h. Within this period the glossa is drawn in between the galeac, and thcsc arc clappcd against the underneath of the head, corresponding to thcir position at rest.

According to my laboratory observations the newly metamorphosed bcc spends thcse 6 h still i n the cell, from which i t then frees itself, the way out Icading through the cells of the younger siblings.

But what directional stimuli has the young bee in leaving thc ccll? All cells show the same textural features: side walls and one end arc smooth, thc other end is rough (see chap. IV, 1, a). In all cells of a burrow the rough wall leads - from the young bee’s perspective - to the inside of the burrow, whereas the smooth end wall leads away. If the bee gnaws through the rough wall it arrives in the burrow, and can then fly out through the single entrance hole.

In experiments to test this I cut windows in the cell sides of carpcntcr bee burrows and extracted larvae, which were kept in other receptacles in the laboratory unt i l shortly before the imaginal moult.

They were replaced in altered cells. Individual cells were sawn i n half across thcir longitudinal axis, and with these “building units” cells having either 2 rough or 2 smooth ends were constructed. Apart from thc joins, and the cellophaned and blacked-out windows, these resembled perfectly normal cells.

3) Original paper not seen; quoted from MALYSHEV (1931).


I observed the emergence of 23 animals, 9 from untreated cells having one smooth and one rough end wall (Series I) , 14 from composite cells. Of these, 8 cells had both ends rough (Series 2), 6 had both ends smooth (Series 3). In all experiments the cells lay horizontal during emergence, and the animals were placed in them a t least a day before the moult.

Scratching and gnawing noises from the cells indicate that wall-piercing has begun; and this some 6 h after the imaginal moult. Froin cells having a t least 1 rough end (Series 1 and 2 ) , the bees freed themselves in an average of 30 min, whereby (in Series 2) they pierced one rough end wall, leaving the other untouched.

To emerge from cells with both ends smooth (Series 3), the bees needed on the average 190 min (shortest period 150 min, longest 240 min). The animals were very “restless” all the time from the first gnawing sounds to emcrgciice, i. e., one could hear them constantly scratching and crawling. The smooth cnd walls apparently offered insufficient grip for the mandibles, and the animals tried to break out anywhere. O n later examination particularly numeroils mandible marks were found a t the junction of the end with the side walls.

In all 3 experimental series the hole was always gnawed on the periphery of the end wall, although the whole wall was of uniform texture. The hole is just large enough for the bee to crawl through, the rest of the partition is left standing.

Having freed itself from its own cell the young bee arrives in the for- lying cells of its younger siblings. These too are then broken through, until the bee arrives in the living quarters, where it meets with the mother. It is remarkable that it is always the eldest animal of one cell row which by its own emerging prepares the way for the younger ones. These, having already ac- quired ful l leg mobility before the imaginal moult, are able to evade their emerging siblings. Normally, such pupae stay in the cells, probably sitting on the rest of the partition, and emerge into the living quarters only after the m ou 1 t.

I am unable to say whether the adult bee helps in emerging, but this is unnecessary in any case, as the laboratory experiments showed. She does however carry out the sawdust produced.

The young of all four species emerged from the cells in the order of ovi- positing, i. e., from the rear cells first. All young left the maternal burrow by the single entrance hole.


Carpenter bees are not the only Apoidea building linear dwellings. Some species of the genera Osmia (Megachilidae) and Anthophoru (Anthophoridae) also construct their breeding cells in reverse progression. In the European species, however, the larvae winter in the cells, minor age differences are canccll- ed out; in spring all animals are concurrently ready to emerge, and do so one after another. But of all the Apoidea constructing linear dwellings, only Xylo- c o p young fly in their birth year. Naturally entomologists are puzzled, esye- cially as we might picture the younger pupae “helpless” in their cells, vulner- able to any damage caused by the passage of their elder siblings. But the ad- vance development of leg mobility dispells these misgivings, a t least for those species I observed.

This mode of emerging has one enormous advantage, outweighing m y possible sibling damage by young bees traversing the cells. I t is the prerequi-

Ethological Study of African Carpentcr Bees of the Genus Xylocopa 367

site for the use of the same burrow by a following generation. As shown, :L single entrance is essential for brood survival; and this is guaranteed only i C the young emerge into the burrow itself, and not directly into the outside world.

DAVIDSON (1893) presumed for X. orpi fex , and MALYSHEV (1 93 I ) for X. valga that 8 8 and 99 lie in a certain order in the cells, and havc diffcrcnt periods of development, so that the young in one bore emerge roughly at the same time. HURD (1958) writes of X. frontalis: “The uppermost ncst con- tained 3 cells which in descending order had a malc pupa, a recently cnicrgcd fcmalc (unpigmented wings), and a female pupa.” Here it is evident that a Q has emerged before her elder brother. HURD and MOURE (1963) rcproduce 3 photograph of the inside of a X. californica burrow, where light and dark pupae lic indiscriminately mixed in the cells; if we may assunic a progressive pigmentation increase in this species too, as time goes on, then thcse animals show a stage of development either too precocious or retarded for thcir positions in the cell row. There is no commentary to this photograph, and possibly the positions shown are not the original ones. HURD and MOURE (1960) write of X. nogueirai: “The randoin occurrence of the inale and fcmalc pupae within the examined cell series is merely determined by chance.” If anywhere, then precisely in this species, nesting in bamboo and constructing up to 8 cells in a row, a certain order would be beneficial.

VIII. Encounter of the 2 Generations

1) Behaviour of the Young after Emerging, and Feeding by the Mother

After emerging the young bees a t first remain more or less quicsccnt i n the burrow. They rarely crawl about, and never leave the burrow. They will groom a t times, thus removing exuvien remnants. Some 3 days after emerging they grow more active, climb about more and look out of the entrance; a t nny disturbance they already buzz, and let the sting “flash”.

There is no immediate change in the mother’s behaviour after thc young emerge. She continues sitting all day in the tunnel, and flies out oncc or twice to forage in the late afternoon. It is not only amazing that here, in a solitary species, the mother encounters her young, but I could observe, for X. iniitator, X . nigrita and X. flavorufa, that she even feeds them. Just inside, near the

t

, - - - . ~ --- -___-_ 0 0.5 Is . _- - -__ -.__---- -I__--_ -

Fig. 18: Sound spectrogram of begging noises of X . rmitator


entrance, they await her return from collecting and literally rush a t her; groping contact with the antennae is established. Sometimes a young bee will clutch a t the mother with the forelegs, and one soon sees a niouth-to-mouth feeding, accompanied by short sounds (drr - drr - drr). I suspect that only the young bee produces this noise, as I also heard it while observing young bees begging (in vain) from elder siblings which had flown out. Fig. 18 shows the sound spectrogram of these utterances.

Only mouth-to-mouth feeding occurs, pollen is never taken from the mother’s body hairs. After feeding the young, the adult ? grooms this off out of the entrance.

A sign of the emergence of young bees in a burrow is that pellets 2-3 cm long hang from the lower rim of the entrance or stick to the wood. Whilc the young are cared for by the mother, that is before they forage for themselves, they defecate from the entrance hole, usually immediately after feeding. For this they sit in the bore just above the entrance and stretch out their abdomens. After their first excursion young bees defecate only in flight as adults do.

2) Dissolution of the Community

I do not know for how long, or even whether a t all, the young bees depend on food given by the mother. Possibly guarding the brood up to the imaginal moult is sufficient maternal care, and the young can then fend for themselves. In any case, young bees emerging later must do without the satis- faction of being fed by the mother, as the adult 99 die within this period in which the young emerge. Either they do not return from collecting, or onc finds them dead in the burrow, whence a body will be removed by a young bee.

Although I could not observe that siblings fed each other, I did observe that in case of disturbance the elder young 09 defend a burrow just as effectively as the mother, thus protecting the unemerged pupae. In 2 X . tmitator burrows young bees still emerged after the mother’s death.

After the imaginal moult the young invariably spend about 8 days within the burrow, then fly out for the first time to forage. After these excursions the young 99 return to the maternal burrow, whereas the young 8 8 do not. An exception is X . nigrita, in which brothers and sisters live in life-long com- muni t y .

I cannot say exactly how the sisters part company in X . imitator, X . {lavorufa and x. torrida, but at any rate I never witnessed any strife between them. Finally, one of the young remains alone in the maternal burrow, and soon begins constructing her own breeding cells. On Rubondo and in the Sc- rengeti X . tmitator, X . nigrita and X . flavorufa produce 2 generations yearly, but I can make no statement on this point for X . torrida.

3) Colonizing Experiments with Young Bees

It was attempted to colonize 7 laboratory-bred 99 ( 3 X . imitator, 4 . X . nigrita) in the field.

After the imaginal moult the animals were first placed in artificial laboratory burrows of wood, and were fed twice daily with a honey solution from a pipette. To drink, the bees stretched the galeae into the mouth of the pipette, then stuclr out the glossa and drew in the solution, while constantly moving the glossa back and forth. If I placed a drop on the galeae between the mandibles, the galeae parted slightly, the drop trickled into the gap and was drawn

Ethological Study of African Carpenter Bees of the Genus Xylocopa 3 69

into thc pharynx by the glossa. The young bees sometimes made begging noiscs whilc feeding, although never as intense as I have heard in the ficld. TIic young bees remained thus some 8 days in their artificial burrows, after which time there is no holding them, and they fly out. Returning them to tlic burrow is useless, they will not stay in it. After the first laboratory excursion T attempted to colonize the animals in the field. The following is a description of thc rcsults.

X . imitator: Case I : 2 sisters (age difference 1 day) were placed togctlicr in an cmpty bore within a colony in which were 5 other 99 with their ncwly- ciiicrged young. After a day only one sister remained. After about 3 wcck i l l

the burrow she constructed breeding cells, and then enlarged thc burrow. Thc sccond 9 was not seen again. Case 2: a young 9 was placed i n an empty borc i n a colony where 2 other 09 with their newly-emerged young wcrc scttlcd. This 9 bcgan by enlarging the burrow, then constructed breeding cclls aftcr about 2 weeks.

X . nigrita: Case 1 : A 0 placed in a deserted X. ftavorufa burrow rcmain- rd there for 2 days, then wandered off. 3 weeks later I discovered hcr i n a tree-trunk near the shore, where in the meantime she had constructcd a burrow. Case 2: I placed a 9 in the field, together with “her” laboratory burrow. Shc did not return to it from her first excursion. Case 3: 2 sisters (agc diffcr- mce 2 days) were placed together in a burrow where young had just cnicrgcd. At first they were attacked and chased around in the bore system by thc adult bees, to the accompaniment of a permanent buzzing, but finally they were accepted, and from then on they flew in and out normally.

Unfortunately these are only a few results, bu t they serve to prove that young bees will accept old species-specific burrows to live and nest in .

4) Review of Literature and Discussion The uncommon circumstance, for solitary bees, that the mother encounters her youn ,

is described for various Xylocopa species. JACOBSON (1927) writes of X . caerulea that the aduft 99 live together with their progeny. MALYSHEV (1931) showed that this also applied for X. frontalis and X.lunulata. WAGNER (1958) observed the meeting of mother and young in X. firnbriata. IWATA (1964) reports of X.aurtpennzs that an adult bee (with damaged wings) lived with 3 daughters and 3 sons: after the mother’s death the siblings remained in the maternal burrow until the next spring, when the community dispersed, I 9 stayed in the maternal burrow and the others Constructed burrows of their own. This account of IWATA’S is the only reference to the dissolution of a family.

I would like to add a short digression. The more complicatcd a burrow, and the more effort it took to build, the more important it becomes - from the point of view of kin selection theory (WILSON 1975) - to pass it on within the family. As female carpenter bees will accept and occupy a strange burrow (as shown through observations and colonizing experiments), there are several conditions for such an inheritance. However, guarding of the brood, and the meeting and peaceful coexistence of mother and offspring, combine to niakc inheritance of the burrow by a direct descendant possible.

Feeding of the young by the mother has been described, before my observations, only by RAU (1933) of X . virginica. This subject mattcr dcscrvcs more attention in future observations of Xylocopa species. If we call to mind that not only does the mother feed the young, but after her death the cldcr feed the younger siblings, we realize that an essential condition for thc origin of a colony is fulfilled.

Carpenter bees can therefore give us valuable insight into thc evolution of a colony.

2 . Tierprychol. . B d . 44, Heft 4 24

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Summary

1) During a 3-month stay on Rubondo, an island in Lake Victoria, East Africa, 4 Xylocopa species ( X . imitator, X . nigrita, X . torrida and X . f l m o - 7ufa) were subjected to comparative ethological study.

2) The preferred dwelling-plants and nest-building behaviour are described. All 4 s ecies construct their burrows in dry timber, and only the ??

rida and X . flavorufa there is invariably only one 9 to a burrow, in X . nigrita several adult 99 usually inhabit one burrow system.

3) Rehaviour at the feeding plants is described, and a particular collecting technique on Caesalpinaceae, observed for all species but X . imitator.

4) O? provisioning breeding cells carry in pollen and nectar all day, save for the midday hours, to form the provisioning mass. A breeding cell takes an average of 11/2 days to complete. Cells are sealed with a flat spiral of sawdust gnawed from the inner walls of the bore and mixed with saliva.

5) The sexes encounter each other at the feeding localities ( X . torrida and X . flavorufa), or in male territories located elsewhere ( X . nigrita). For fecundation 6 6 seize the 99 in flight and copulate in flight ( X . torrida and X . flavorufa). In X . nigritu copulation probably occurs while sitting. The copulatory hold of a Xylocopa species ( X . torrida) is reported in detail for the first time.

6 ) After completing the breeding cells the 0 sits almost all day in her burrow and guards the brood. Defence behaviour of the 4 species is described. All species except X . nigrita show a special defence behaviour in which the abdomen blocks the burrow entrance hole. The mother’s guarding is essential for brood survival, her early death means its destruction within a day by intruders. One X . nigrita 9 can successfully defend the progeny of several ??.

7) The ontogeny of the 4 species is reported in detail. The egg stage lasts some 5 days in all of them. The apodal larvae consume their provisioning mass in 14 days, then are quiescent for about 8 days until pupation, SO that the whole larval stage lasts 3 weeks. The pupal stage lasts equally long. Some 5 days before the imaginal moult the pupae attain full leg mobility and can climb about in the cell.

8) To emerge from the breeding cells the first-hatched young bee (in the rearmost cell) breaks through the forelying cells of its younger siblings, and meets with the mother inside the burrow. In all 4 species a meeting occurs bctwecii the mother and her progeny.

9) Feeding of those young which have not yet flown out is described (for X. imitator, X . flavorufa and X . nigrita), and the first sound spectrogram of begging sounds of Xylocopa is given.

10) Experiments showed that for a bee emerging from the breeding cells partition texture indicates direction.

11) The life of the mother ends soon after the young have left the cells. Sometimes she does not meet all her progeny. In this case the elder siblings ensure the emerging of the younger ones. Mutual feeding of siblings, however, could not be observed.

12) The maternal burrow is taken over by a daughter. The rest of the progeny wanders off. Whereas 99 immediately construct a burrow, 8 8 inake do with any sort of shelter ( X . imitator, X . flavorufa, X . torrida). In X . nigrita, siblings of both sexes continue living together in the maternal burrow.

13) A few experimental attempts a t colonization in the field were made with laboratory-bred 99 of X . imitator and X . nigrita. These showed that the

build. Several f 9 may settle side by side in one trunk. In X . imitator, X . tor-


animals will accept used species-specific burrows left empty, in which they construct breeding cells.

14) My own observations are supplemented in each chapter by a review of the literature.

Zusammenfassung

1) Auf Rubondo, einer Insel im Viktoria-See, Ostafrika, wurden wahrend eines dreinionatigen Aufenthaltes vier verschiedene Xylocopa-Arten ( X . imitator, X . nigrita, X . torrida und X . f l a v o ~ u f a ) vergleichend ethologisch untersucht.

2) Die bevorzugten Wohnpflanzen und das Nestbauverhalten werden beschrieben. Alle vier Arten legen ihre Bauten in trockenem Holz an, und es bauen nur die 99. Dabei konnen mehrere 99 im gleichen Stamm nebenein- ander siedeln. Bei X . imitator, X . torrida und X . flavorufa findet man stets nur ein erwachsenes 9 in einem Bau, bei X . nigrita leben meist mehrere er- wachsene 99 in einem Gangsystem zusammen.

3) Das Verhalten an den Futterpflanzen wird dargestellt. Daruber hinaus wird eine besondere Sammeltechnik an Caesalpinaceae beschrieben, die aufler bei X . imitator-99 an allen Arten beobachtet werden konnte.

4) 99, die Brutzellen versorgen, tragen den ganzen Tag uber - rnit Aus- nahme der Mittagstunden - Pollen und Nektar ein und formen daraus einen Honigkuchen. Sie fertigen im Durchschnitt in l l / e Tagen eine Brutzelle. Die Zellen werden mit einem spiraligen Holzdeckel verschlossen. Die Holzspane dafur werden von der Innenseite der Rohre genagt und mit Speichel ver- misch t .

5) Die Geschlechter treffen an den Futterpflanzen zusammen (X. torrida und X. f lavorufa) oder in anderswo liegenden 8 -Revieren ( X . nigrita). Zur Kopula ergreifen die 8 8 die 99 im Flug und begatten sie im Flug ( X . torrida und X . flavorufa). Bei X. nigrita findet die Kopula wahrscheinlich im Sitzen statt. Die Kopulationshaltung einer Xylocopa-Art ( X . torrida) wird erstmds genau dargestellt.

6) Nach A d a g e der Brutzellen sitzen die 99 fast den ganzen Tag uber in ihren Rohren und bewachen die Brut. Das Verteidigungsverhalten der vier Arten wird beschrieben. Mit Ausnahme von X . nigrita zeigen die Arten ein spezielles Schutzverhalten, indem sie den Rohreneingang rnit dem Abdomen verschlieflen. Das Bewachen der Brut durch die Mutter ist lebensnotwendig fur die Nachkommenschaft. Beim Tod der Mutter wird die Brut innerhalb kiir- zester Zeit von Eindringlingen vernichtet. Bei X . nigrita kann ein 9 die Nach- kommenschaft mehrerer 99 erfolgreich schutzen.

7) Die Ontogenese der vier Arten wird eingehend beschrieben. Das Ei- stadium dauert be1 allen etwa 5 Tage. Die apoden Maden zehren wahrend 14 Tagen ihren Honigkuchenvorrat auf, liegen noch etwa 8 Tage ruhig und verpuppen sich dann. Das Madenstadium dauert somit 3 Wochen. Ebenso lange dauert das Puppenstadium. Die Puppen konnen bereits etwa 5 Tage vor der Imaginalhautung ihre Beine voll einsetzen und in der Rohre klettern.

8 ) Beim Ausschlupfen aus den Brutzellen durchbricht die erstgeschlupfte Jungbiene ( in der hintersten Zelle) die (davorliegenden) Zellen ihrer jungeren Geschwister und trifft im Rohreninnern rnit der Mutter zusammen. Bei allen vier Arten kommt es zur Begegnung der Mutter mit ihrer Nachkommenschaft.

9) Das Futtern der noch nicht ausgeflogenen Jungen durch die Mutter wird (bei X . imitator, X . flavorufa und X . nigrita) beschrieben und erstmals ein Klangspektrogramm der Bettellaute von Xylocopa vorgelegt.

24"

3 72 GUSTL ANZENBERGER

10) Versuche zeigten, dai3 fur das Ausschlupfen aus den Brutzellen die Textur der Trennwand richtenden Charakter hat.

11) Kurz nachdem die Jungen geschlupft sind, stirbt die Mutter. Manch- ma1 begegnet sie nicht mehr allen ihren Nachkommen. In diesem Fall gewfhr- leisten die alteren Geschwister das Ausschlupfen der jungeren. Eine gegenseitige Futterung der Geschwister konnte allerdings nicht beobachtet werden.

12) Der mutterliche Bau wird von einer Tochter ubernommen. Die ubri- gen Nachkommen wandern ab. Wahrend die 99 sofort einen Bau erstellen, nehmen die 8 8 mit allen moglichen Unterschlupfen vorlieb ( X . imitator, X . flavorufa und X. torrida). Bei X . nigrita leben die Geschwister beiderlei Geschlechts weiterhin im Bau der Mutter zusammen.

13) Mit - im Labor aufgezogenen - X . nigrita-99 und A’. imitator-99 wurden wenige Ansiedlungsversuche im Freiland unternommen. Diese zeigten, dafl die Tiere leerstehende arteigene Altbauten akzeptieren und in diesen selbst Brutzellen anlegen.

14) In jedem Kapitel werden die eigenen Beobachtungen durch eine Lite- raturubersicht erganzt.

Acknowledgements

I would like to thank particularly my tutors, Prof. M. RENNER for the many stimulating suggestions during my studies, and for the constant promotion of this work; and Prof. W. WICKLER for rendering me every help during my time a t Seewiesen, and for enabling me to visit Africa, and so carry out this investigation. I thank also my friends in Seewiesen and Miinchen, especially Dr . T. HEINZELLER and Dr . T. OSTEN for lending me their ears, and for many hours of fruitful discussion. Prof. P. D. HURD helped me classify X.imitator . Mr. H. KACHER was good enough to prepare the drawings, Miss M. SCHMUTZ typed the manuscript, Mrs. P. RECHTEN translated it, I thank them all. Last but by no means least come my parents, who supported me unfailingly through all m y studies.

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77-85.

374 G. ANZENBERGER, Ethological Study of African Carpenter Bees of the Genus Xylocopa

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Author’s address: Gust1 ANZENBERGER, Psychologisches Institut der Universitat Zurich, Abteilung fur Biologisch-Mathematische Psychologic, Attenhoferstrafie 9, CH-8044 Zurich, Switzerland.

Ethological Study of African Carpenter Bees of the Genus Xylocopa (Hymenoptera, Anthophoridae)

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