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Oocytes, Larvae, and Cleptoparasitic Behavior of Biastes Emarginatus (Hymenoptera: Apidae: Nomadinae: Biastini)

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Oocytes, Larvae, and Cleptoparasitic Behavior of Biastes Emarginatus (Hymenoptera: Apidae: Nomadinae: Biastini) PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024 Number 3667, 15 pp., 30 figures, 1 table November 30, 2009 Oocytes, Larvae, and Cleptoparasitic Behavior of Biastes emarginatus (Hymenoptera: Apidae: Nomadinae: Biastini) JEROME G. ROZEN, JR.,1 JAKUB STRAKA,2 AND KATERINA REZKOVA2 ABSTRACT We present information on the nest-searching and parasitic behavior of the European cleptoparasitic bee Biastes emarginatus (Schenck), found attacking nests of Rophites quinquespi- nosus Spinola in the Czech Republic. Its mature oocyte, first instar, and last larval instar are described and illustrated by SEM micrographs, microphotographs, and diagrams. These stages are compared with those of other members of the Biastini. Because the first instar of the related Neopasites cressoni had not been described before, its description is appended, so that comparisons can be made with B. emarginatus. In most respects, the biology and immature stages of B. emarginatus closely resemble what is known concerning other tribal members, but we note that the mature larva, though agreeing morphologically with those of close relatives, has an anatomy that invites investigation into adaptive function. INTRODUCTION genera totalling12 named species is restricted to the Holarctic region, with Neopasites and This study reports on the biology and imma- Rhopalolemma in North America and Biastes ture stages of the cleptoparasitic bee Biastes in the Palearctic (Michener, 2007). Known emarginatus (Schenck) and compares the infor- hosts of all biastines belong to the Rophitinae mation with existing knowledge concerning (Halictidae), as follows (host names in parenthe- other members of the Biastini, one of the ses): Neopasites (Dufourea), Rhopalolemma numerous tribes of the Nomadinae, all of which (Protodufourea), Biastes (Systropha, Rophites, are cleptoparasites. This small tribe of three and Dufourea) (Michener, 2007; Westrich, 1989). 1 Division of Invertebrate Zoology, American Museum of Natural History ([email protected]). 2 Faculty of Science, Charles University in Prague, Department of Zoology, Vinicˇna´ 7, 128 44 Praha 2, Czech Republic ([email protected]). Copyright E American Museum of Natural History 2009 ISSN 0003-0082 2 AMERICAN MUSEUM NOVITATES NO. 3667 Beyond host associations, biological infor- Miller), but much of the area received consid- mation concerning these cleptoparasitic gen- erable sunlight during a large part of sunny era is limited. Torchio et al. (1967) described days.Groundcover,mostlytallgrasses(ca host-searching behavior of adults, the eggs, 30 cm high), obscured much of the surface, so egg-laying habits, and larval behavior of that many nest entrances were partly or Neopasites cressoni Crawford. Rozen et al. completely hidden. Nest entrances, surrounded (1997) reported on various aspects of the by tumuli when fresh, were left opened during biology of Rhopalolemma rotundiceps Roig- foraging. The main burrows of host nests Alsina. However, details concerning the biol- descended vertically with sharp turns to avoid ogy of Biastes have been lacking. rocks. Cells in a nest were arranged singly (i.e., The immature stages of these three genera not in linear series). Scattered nests were found have been examined on a number of occasions. a few meters away from the main site, but Egg/mature oocytes of exemplars of all genera activity of B. emarginatus was low there. At have been described. Most of these descriptions least 10 Biastes females flew over the main part were accompanied by information concerning of the nest aggregation during the peak of the number of ovarioles per ovary found in activity on sunny days. dissections because among the Nomadinae there The aggregation was studied during 3–18 is extensive variation in ovariole counts from August 2008. Rophites females were active one species to the next. Egg/oocyte descriptions from early morning to late afternoon, flying are as follows: Neopasites cressoni (Torchio et even when the sky was overcast. In contrast, al., 1967; Rozen et al., 1997); Rhopalolemma flight activity of Biastes depended on weather rotundiceps (Rozen et. al., 1997); Biastes brevi- conditions. They flew only during warm, cornis (Panzer) (Rozen and O¨ zbek, 2003). sunny, windless days (temperatures 25–30uC), Information concerning ovary statistics is sum- and on such days they preferred host nests marized in Rozen (2003). Descriptions of first situated in sunny places. In addition, search- instars of the Biastini have been lacking until ing Biastes females moved with the sunny now. Because we describe here the first instar of areas as these areas shifted during the day. Biastes emarginatus, we append a comparative Only during the warmest days, when the account of the first instar of N. cressoni.Mature temperature rose over 30uC, did Biastes biastine larvae have been described, as follows: females prefer shaded parts of the nesting site. N. cressoni (Rozen, 1966, 1996a; McGinley, When the temperature fell below 25uC, the 1981) and R. rotundiceps (Rozen et al., 1997). bees flew strictly in shafts of sunlight or were An intermediate stage larva of Biastes emargi- inactive, behaving similarly to the thermoph- natus was treated by Rozen (1993), as was the ilous behavior of another cleptoparasitic bee pupa of N. cressoni (Rozen, 1997). Epeoloides coecutiens (Fabricius) (Straka and Bogusch, 2007a). Because the site was com- BIOLOGICAL OBSERVATIONS pletely shaded in the morning and late afternoon, Biastes females were active only J.S. and K.R. made the following observa- from 10:30 A.M. to 4:00–5:00 P.M. (CEST). tions on Biastes emarginatus at a dense nest- While searching Biastes females usually flew ing aggregation of Rophites quinquespinosus slowly close to the vegetation, scanning the Spinola in a large, unattended garden in ground surface for host nests. Because nests Praha-Misˇkovice, a district of Prague, Czech were often well hidden in the grass, Biastes Republic. This nesting site was discovered in would usually land when they spotted suspi- 2006 and checked yearly since then. The cious places and finish their inspections by Rophites nest aggregation occupied about a 3 crawling through the vegetation. The efficien- 3 3 m section of a 40–45u sloping surface on the cy of finding nests seemed rather low, in that sunny edge of a deciduous forest. More than 40 cleptoparasites usually spent a long time nests were observed there at a single time during searching before finding active host nests. the course of our observations. The site was Females of Biastes always immediately enter partly shielded by the forest canopy from rain, a newly discovered nest and probably check its particularly by one old linden tree (Tilia cordata contents. Of 21 visits, most took only a very 2009 ROZEN ET AL.: BEHAVIOR OF BIASTES EMARGINATUS 3 short time (5–47 sec, on average 29 sec), probably indicating that the cell conditions were inadequate for successful egg laying. Seven attempts were probably successful as they took on average 1 min, 48 sec (the longest took 2 min, 30 sec). Interestingly, in about half these cases, the cleptoparasite waited 3–8 sec at the nest entrance before flying away, probably checking the conditions outside but risking confrontation with the host. If the entrance became shaded during the inspection, the parasite waited at the entrance several more seconds. Parasitic behavior at the aggregation often resulted in conflict. Owners of active nests visit their nests many times a day, in that a female of Rophites quinquespinosus spends approxi- mately 15 min inside her nest and 45 min foraging for every hour of daily activity. This means that the nest is protected at least one quarter of the time. Females of Biastes emarginatus fly away immediately when they encounter host females at the nests. A conflict situation happens when a host female returns while a Biastes female is inside the nest. The host grabs the parasite with her mandibles and throws her from the nest entrance. No egg was found even when cell walls were carefully checked. The eggs could be well hidden or possibly laid on/in the spherical provision mass. We encountered six first instars of Biastes emarginatus in four cells; two first instars were Figs. 1, 2. Microphotographs of Biastes emar- found on the surface of the food sphere in ginatus. 1. Mature oocyte, lateral view, showing each of two cells and a single first instar was transparent, glassy chorion. 2. First instar appar- found in each of the other two cells. In one ently attacking another first instar. case of dual occupancy one larva appeared to be attacking the other (fig. 2). This discovery obtain mature oocytes and data concerning demonstrates that in two cases two eggs had the number of ovarioles and mature oocytes been deposited in the chamber, but whether by (summarized in table 1). The number of a single female or separate females remains ovarioles is expressed by a notation that unknown. It almost certainly indicates that on provides the number of ovarioles in each of hatching, this species, like most cleptopara- a female’s two ovaries. For example, the sites, immediately rids the host cell of all but ovarian formula 4:4 refers to four ovarioles one individual, as is necessary if there is stored in each of the female’s two ovaries; this food adequate for only one individual. number is the plesiomorphic number for the Apidae (Michener, 2007). One female of B. OVARIAN STATISTICS AND emarginatus possessed an ovarian formula of MATURE OOCYTE 7:6 (or 7) and the other female was 8:8. Although these counts are uncertain because We dissected and later examined the ovaries of difficulty interpreting the maze of ovarioles of two adult females of Biastes emarginatus to on such small specimens, they confirm that 4 AMERICAN MUSEUM NOVITATES NO. 3667 TABLE 1 Egg Indices, Number of Mature Oocytes, and Number Ovarioles of Biastes emarginatus Compared with Other Biastini Figures in first three columns are averages; data for other Biastini from Rozen (2003: table 1).
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