Ammobatoides abdominalis (Eversmann, 1852)

ROZEN JR., J. E. R. O. M. E G., 2001, Ovarioles and Oocytes of Two Old World Cleptoparasitic Bees with Biological Notes on Ammobatoides (Hymenoptera: Apidae), American Museum Novitates 3326, pp. 1-12 : 3-5

Ammobatoides abdominalis

BIOLOGY: I discovered males and females of the host bee, Melitturga clavicornis foraging from Trifolium repens Linnaeus on June 21, 1999, at the Central Asian locality identified below under Material Studied. Both sexes of Ammobatoides abdominalis were collected in the vicinity, feeding on the same plant. I searched for nests of the host bee near patches of Trifolium and found one, described below. Where Ammobatoides females were most abundant, I could see several patrolling at one time as they meandered low over the ground, a search flight typical of other nomadine bees.

The male flight behavior of Ammobatoides abdominalis was noteworthy. They perched on elevated prominences such as large stones on barren patches of ground. They swiftly and suddenly took pursuit when they observed other insects approaching on the wing. After chasing an insect, the male usually returned to the same perch. When I threw a small stone toward a perching male, he arose quickly to pursue. This test was conducted about 10 times, with some pebbles soaring 30 cm above them, and in most cases the males responded the same way. I have observed similar chasing behavior on the part of males of Melitturga clavicornis (Rozen, 1965b) , Meliturgula braunsi (Friese) (Rozen, 1968) , and Xylocopa virginica ( Apidae : Xylocopinae ) (unpubl. obs.), as have Linsley and Michener ( 1962) and Cazier and Linsley ( 1963) for Protoxaea ( Andrenidae : Oxaeinae ). In the case of Melitturga , Protoxaea , and Xylocopa , males hover in the air and chase oncoming insects (and pebbles). With Meliturgula , males rested on the ground, as did those of A. abdominalis when not chasing.

This behavior appears to be a form of territoriality. Cazier and Linsley ( 1963), after discussing the function and significance of male territorial behavior in Protoxaea gloriosa (Fox) , suggested that it may reduce competition for nectar and pollen by other species and thereby allow a greater supply for conspecific females. However, this explanation does not readily explain such behavior on the part of a cleptoparasitic bee, which does not provision nests. Since males of the host Melitturga clavicornis exhibit aggressive behavior toward other insects, might territorial aggressiveness of the Ammobatoides male be reinforcing that of the host male and thereby assure the provisioning of more host brood cells? 2 The answer to this question is

2 One of the anonymous reviewers disagreed with this possible explanation of territoriality in male Ammobatoides . He believed that it ‘‘is most likely due to one of two reasons: (1) the males are establishing territories over a resource valuable to females (possibly host nests), and (2) the males are waiting for female Ammobatoides to mate with.’’ He, of course, may be correct, but his explanations do not address how territoriality arose uniquely in Ammobatoides of all the Nomadinae . Nor do they acknowledge the peculiar fact that both host and parasite exhibit territoriality, accompanied by strong sexual dimorphism. Almost all hosts of the Nomadinae are nonterritorial. Why is territoriality not exhibited in these other cleptoparasites (even closely related ones such as Holcopasites )?

unknown. An alternative explanation of this male behavior in Ammobatoides might involve spacing of males for dispersal and mate seeking.

As in the case of Xylocopa , Protoxaea , Melitturga , and Meliturgula , males of Ammobatoides have compound eyes that converge above (contrasting with parallel inner orbits or inner orbits that diverge dorsally in females). The converging of the upper part of the male’s eyes in these taxa presumably enhances the ability to detect oncoming flying insects. Male dorsal eye convergence is uncommon among cleptoparasites, but a similar sexual dimorphism, though less pronounced, occurs in Epeoloides . Whether it is accompanied by similar behavior is as yet unknown.

Because other differences between the sexes of Melitturga clavicornis and Meliturgula braunsi are suspected of being involved with male hovering/territoriality (Rozen, 1968), antennae and hind­wing differences were inspected in Ammobatoides . Male Ammobatoides exhibit no clublike modifications of the antennae as has been noted for the two panurgines, and their hind wings were of about the same proportions as those of the female, contrasting with those of M. braunsi .

In regard to sexual dimorphism of Ammobatoides not related to hovering/territoriality, color pattern and hair­length dissimilarities are pronounced. Females have the typical black head and mesosoma and red metasomal color pattern often found in such cleptoparasitic bees as Sphecodes and Holcopasites . This pattern is associated with short body hair. In contrast, males are all black with long, grayish hairs on the mesosoma, first metasomal tergum, and most metasomal sterna; they also have distinct pale apical hair bands on terga 2–6. The significance of this strong dimorphism is unknown.

In a single case, a female’s search behavior differed from the wandering patrolling referred to above. A female sat on the ground, facing a tumulus. She shifted her position several times by hovering slowly, but she always alighted and remained facing the tumulus. Because such behavior of cleptoparasites has led to the discovery of host burrows in the past, I inverted a plastic drinking glass over the tumulus in an unsuccessful attempt to capture a departing female Melitturga or to slow the flight of a returning, pollen­laden female. Several hours later I excavated the nest.

Below the surface, the burrow meandered downward to a depth of 5 cm and then curved sideways to end in a single open cell that contained a flattened, apparently complete ball of provisions without a Melitturga egg. A search of the cell surface revealed an egg of Ammobatoides abdominalis inserted in a hole in the wall toward the rear of the cell. When first discovered, the egg was not visible, and the hole was covered with a raised, roughly circular piece (about 0.8 mm in diameter) of the cell lining with soil adhering to the underside. When I explored the raised area with forceps, the piece with the egg attached immediately broke away from the cell wall. This piece may have been the ‘‘flap’’, still attached on one side to the cell lining, as described for Holcopasites (Rozen, 1965a) , but further observations are needed to confirm the attachment and whether any part of the egg is normally visible. It is unknown why the egg adhered to the flap, but it could have been either because the female had cemented it to the flap with a secretion or because it had been damaged as it broke away with the flap. Subsequent examination of the egg in the laboratory showed that the anterior end was pointed toward the wall surface and the textured anterior part (see description below) clung to the flap. One wonders if the textured sculpturing of the egg might provide a rough surface for gluing the egg to the flap.

The hole into which the egg had been inserted was 0.4 mm in diameter, about 0.8– 0.9 mm in depth, and it penetrated at about 45° from the cell surface, that is, more sharply than that illustrated by Rozen (1965a: fig. 3) for Holcopasites .

The anterior end of the egg was identified by the fact that oocytes of bees are directed with their anterior end toward that of the mother; eggs are deposited posterior end first. The dorsal surface of the egg and oocyte of Ammobatoides abdominalis was presumed by the fact that the egg was inserted under the flap with the textured part attached to the flap so that the emerging first instar would crawl out with its venter in contact with the cell wall.

DESCRIPTION OF MATURE OOCYTES ( figs. 1, 2, 4–9): Size small relative to distance between outer rim of tegulae (i.e., egg index 0.27); length 1.02–1.06 mm; maximum diameter 0.30–0.31 mm; total number of mature oocytes per ovariole 14–16. Shape ( figs. 1, 2, 4) bilaterally symmetrical with anterior dorsal surface slightly flattened and anterior ventral surface bulging; oocyte slightly constricted ventrally somewhat more than halfway posteriorly; maximum diameter of anterior part somewhat greater than that of posterior part as seen in lateral view; anterior end produced as sharp, curved point, which appears irregularly roughened under SEM examination ( fig. 2); small, pedunculate process ( figs. 5, 6), presumably the micropylar apparatus (Margaritis and Mazzini, 1998), occurring midline at base of point on dorsal surface 3; this process with large, deep, angular pits (presumably micropylar pores, ibid.); each side of oocyte with apparent ridgelike line arising from anterior point and gradually fading posteriorly; under SEM examination ( fig. 4, 5), line consisting of a number of irregular alveoli marking boundary between deeply pitted dorsal surface and smooth lower surface of anterior part of oocyte; posterior end of oocyte broadly round­ ed. Color nearly white.

Chorion under stereoscopic examination ( figs. 1, 2) smooth, transparent, shiny except finely pitted area extending along dorsal surface from pointed anterior end between lateral lines almost to posterior end. Chorion under SEM examination ( figs. 4, 5) minutely, roughly pitted except dorsal surface more coarsely pitted almost to posterior end; chorion at posterior pole with faint, evenly distributed, shallow depressions ( fig. 8); chorion of roughly pitted area in cross section ( fig. 7) consisting of two layers, outer one of spongelike matrix with many holes, and inner one, of about equal thickness, of consolidated, finely granulate matrix lacking fenestrations; chorion of smooth, shiny area in cross section under high magnification ( fig.

3 This process was seen on many, but not all, of the oocytes. Its absence from some presumably results from being accidentally scraped away during dissection.

9) consisting of film of more coarsely granular outer material and thick layer of consolidated, finely granular material lacking fenestrations.

REMARKS: The egg index of this species is low, reflecting the small size of the oocyte relative to female body size. Alexander ( 1996) listed the egg index of several species of the related Holcopasites as also being low compared with that of many other Nomadinae . The shape and pattern of chorion ornamentation of the oocyte of Ammobatoides abdominalis is not known to occur in any other cleptoparasite. The pedunculate process at the base of the anterior point, first noticed by Molly Rightmyer, is a peculiar feature, as is the anterior point. The process was not clearly visible under stereoscopic examination because of light glare of the nearly white eggs. It was also sometimes obscured because of specimen orientation under SEM viewing, but almost certainly is present in all oocytes.

Although Rozen (1965a: fig. 3) illustrated the egg of Holcopasites , eggs/oocytes of that genus should be examined with a scanning electron microscope so that they can be compared with those of Ammobatoides abdominalis .

MATERIAL STUDIED: Two females, Kyrgyzstan: Dzhalal­abad , Chandalash R. 6 km N jct Chatkal R., 1630 m, 41°44′19̎N, 70°52′22̎E, VI­20–1999 (J. G. Rozen, J. K. Bouseman) .