The large carpenter bees of central Saudi Arabia, with notes on the biology of Xylocopa sulcatipes Maa (Hymenoptera, Apidae, Xylocopinae)

Abstract The large carpenter bees (Xylocopinae, Xylocopa Latreille) occurring in central Saudi Arabia are reviewed. Two species are recognized in the fauna, Xylocopa (Koptortosoma) aestuans (Linnaeus) and Xylocopa (Ctenoxylocopa) sulcatipes Maa. Diagnoses for and keys to the species of these prominent components of the central Saudi Arabian bee fauna are provided to aid their identification by pollination researchers active in the region. Females and males of both species are figured and biological notes provided for Xylocopa sulcatipes. Notes on the nesting biology and ecology of Xylocopa sulcatipes are appended. As in studies for this species from elsewhere, nests were found in dried stems of Calotropis procera (Aiton) (Asclepiadaceae) and Phoenix dactylifera L. (Arecaceae).


Introduction
The tribe Xylocopini comprises the large carpenter bees (Xylocopinae: Xylocopa Latreille) species of which principally nest in dead wood (including the wood of human constructions), bamboo culms, and other similar substrates (e.g., Hurd 1958, Museum, Lawrence, Kansas, USA (SEMC). Photomicrographs were prepared using a Nikon D1x digital camera attached to an Infinity K-2 long-distance microscope lens. Morphological terminology in the diagnoses follows that of Engel (2001) and Michener (2007). Herein we follow the supraspecific classification of Xylocopini advocated by Minckley (1998) and Michener (2007).
The nesting biology of X. sulcatipes was studied in Amariah, approximately 25 km northwest of Riyadh, from September 2010 through December 2011. Nests were found on 6 June 2011 at the base of a large hill near an agricultural farm near Wadi Amariah and the highway to Riyadh. Prior to collection the nests were observed for at least an hour to note the coming and going of bees. Most nests were located around 9:00am and collected around 12:00pm. Nests were sealed with plastic and brought to the lab for dissection and study. During four visits (6,12,19 June and 28 September 2011) a total of 13 nests were collected (Table 1). Nests were in the dead branches of local milkweeds [Calotropis procera (Aiton) (Asclepiadaceae), more widely known as the "Apple of Sodom"] growing in a sparsely vegetative desert area and among date palms, Phoenix dactylifera L. (Arecaceae). Nests were measured, sketched, and photographed, and the inhabitants deposited in the KSMA repository.

Genus Xylocopa Latreille Subgenus Koptortosoma Gribodo
This is the largest and most widespread subgenus of carpenter bees, with at least 196 recognized species ranging throughout Subsaharan Africa to the Mediterranean countries of that continent, Dalmatia, the Arabian Peninsula, southwestern Asia, and southern Asia east to the Philippines, Taiwan, and Japan, and south through Indonesia, New Guinea, and the Bismarck Archipelago to southernmost Australia (Michener 2007). The subgenus can be recognized by the female mesoscutellum having a sharp truncation overhanging the metanotum (as in subgenus Mesotrichia Westwood) and surpassing the posterior margin of the latter, and males with unmodified tegulae (elongate in Mesotrichia) (Michener 2007 Diagnosis. Xylocopa aestuans can be most readily distinguished from other Saudi Arabian large carpenter bees by the following: female face with largely white or pale pubescence ( Fig. 5), mesosomal dorsum densely covered by yellow pubescence obscuring underlying integument (Figs 1, 2); mandible bidentate at apex; posterodorsal margin of mesoscutellum projecting beyond posterior margin of metanotum; pygidial plate unarmed. Male covered by dense yellow pubescence (Figs 3, 4, 6); first metasomal tergum with subhorizontal dorsal surface abruptly and angulately separated from declivitous anterior surface; gradulus of first metasomal tergum transverse, lateral extremities not directed posteriorly; male terminalia as in figures 7-11. Comments. Xylocopa aestuans is one of the widespread and ubiquitous of large carpenter bee species. There has been considerable debate regarding the identity of the species of Koptortosoma similar to X. aestuans (i.e., considering them synonyms, subspecies, or separate species), with different authors of varying opinions how to segregate the minor variation into natural taxonomic entities (e.g., Lieftinck 1964). The Saudi Arabian populations have been at times considered to the belong to the largely African, X. pubescens Spinola, although the genitalia of those populations are quite dissimilar from true X. pubescens. Indeed, the genitalia (Figs. 7-11) and other characters are certainly more alike the more easterly populations of X. aestuans and there seems little reason at this time to not consider the central Saudi Arabian populations as such, as was done by Shalaby (1961). The species has also been recorded from the United Arab Emirates (Harten 2005;Dathe 2009). Biological accounts, largely from India or Southeast Asia, have been provided by Dover (1924), Monod (1977), Binti (1992), El-Borollosy and Ismail (1972: note that these observations may be of X. pubescens, the identity of their material requires checking), and Punekar et al. (2010).

Subgenus Ctenoxylocopa Michener
This is a widespread, albeit not very diverse, subgenus of Old World carpenter bees (Maa 1970;Michener 2007). The lineage can be recognized by the prolonged posterior pronotal lobes and elevated process of the spiracles on the third metasomal tergum in  Diagnosis. Xylocopa sulcatipes can be most readily distinguished from other Arabian large carpenter bees by the following: Female with face with largely black pubescence (Fig. 16), mesosomal dorsum largely covered by black pubescence not obscuring underlying integument (Figs 12, 13); mandible tridentate at apex; mesoscutellum not projecting over metanotum, apical margin rounded in profile; pygidial plate armed on each side with subapical spine. Male covered by largely fuscous to black pubes- cence except face, dorsum of mesosoma, and apicolateral patches of first metasomal tergum with predominantly white or pale setae (Figs 14, 15, 17); first metasomal tergum with subhorizontal dorsal surface rounding into declivitous anterior surface; gradulus of first metasomal tergum laterally curved posteriorly; male terminalia as in figures 18-22.
Comments. Maa (1970) recorded X. sulcatipes from Saudi Arabia, Yemen, Israel, and Transcaspia (likely northern Iran, or southwesternmost Turkmenistan), while Vicidomini (2004) gave localities in Jordan. The records of X. fenestrata from the United Arab Emirates (Dathe 2009) are likely X. sulcatipes, and this material should be dissected and compared with the images herein (Figs. 18-22) as well as those of Maa (1970). We have found that Maa's (1970) characterization of the terminalic differences holds well for observed populations and the species he recognized appear to be good (Engel pers. obs.).  The biology of X. sulcatipes has been the focus of several extensive ecological and behavioral studies, principally in Israel (e.g., Eisikowitch 1986;Gerling et al. 1983Gerling et al. , 1989Hefetz 1983;Kronenberg and Hefetz 1984;Stark 1989Stark , 1992aStark et al. 1990;Surholt et al. 1990;Velthuis 1987;Velthuis and Gerling 1980;Velthuis et al. 1984;Willmer 1988). Our observations do not differ from those of the previous studies except that we have focused more on the architecture of the nests rather than the particular ecology of the species, which is already well characterized. The species is bivoltine and foraged from March through November. The area around Amariah, where our observations were made, is a typical central Saudi Arabian desert environment. Vegetation is thinly scattered and comprised mostly native plants, including several promising foraging flowers and nesting sites throughout the season. Among these, C. procera was found to be the most commonly used for nesting and provisioning resources. The pithy and rather straight stems of suitable diameter of C. procera make them ideal for nest construction (e.g., Figs 23-27). Secondarily, P. dactylifera was used as a nesting substrate (with five such nests collected). Detail measurements of the nests observed are provided in table 1. Given the different overall physical structure of these substrates it is not surprising that nests in C. procera had a single, linear nest tube extending to each side of the entrance (Figs 23-27), while those in P. dactylifera consisted of a more gallery-like structure, similar in this regard to the variation observed for X. (Stenoxylocopa) artifex Smith (Silveira 2002). In all of the nests the pollen masses were compact, well kneaded, and mixed with sufficient nectar to leave them moist (Fig. 26). Where observed, individual pollen loaves were fully consumed and the larvae defecated pellet-like feces which were placed to its back or at the bottom of the cell. As observed elsewhere for this species, cells were arranged linearly, but never with cells closer than 1-1.5 times an individual cell length from the nest entrance. Also similar to observations made elsewhere on this species (e.g., Gerling et al. 1989), some nests were found  to comprise several newly emerged females along with an older female, all of whom participated in foraging but apparently built their own cells, although further observations are needed to clarify this point.

Key to the Species of Xylocopa in Central Saudi Arabia
Although X. sulcatipes, like other Xylocopa, is polylectic, females were observed foraging mostly from C. procera and it was there that males were seen to approach and grab females for mating. In addition to foraging at C. procera, females were observed visiting Reseda alba L. (Resedaceae) and radish [Raphanus sativus L. (Brassicaceae)]. Given that species of Xylocopa may be useful for agricultural pollination (Keasar 2010) it may be beneficial for standing crops in central Saudi Arabia to be surrounded by suitable native vegetation including C. procera, thereby providing ample nesting sites to encourage the establishment of sustainable and large populations of these bees. No associated organisms were found among the nests observed.