Isepeolus luctuosus (Spinola)

ROZEN, JEROME G., 2003, Eggs, Ovariole Numbers, and Modes of Parasitism of Cleptoparasitic Bees, with Emphasis on Neotropical Species (Hymenoptera: Apoidea), American Museum Novitates 3413, pp. 1-36 : 12-14

Isepeolus luctuosus (Spinola)

Because of pronounced dissimilarities, the eggs and mature oocytes of this species are described separately below.

DESCRIPTION OF EGG (fig. 9): Length (not including the flange; see Remarks) 1.63–1.75 mm (N = 3), maximum width 0.69–0.92 mm (N = 3), maximum dorsal/ventral thickness approximately 0.25–0.38 mm (N = 2); egg index not calculated since intertegular distance of female unknown, but see description of mature oocyte. Shape greatly dorsoventrally flattened relative to width, bilaterally symmetrical along its moderately straight long axis; anterior end subtruncate in dorsal/ ventral outline, posterior end tapering abruptly with rounded apex in dorsal/ventral outline; sides in dorsal/ventral outline gently curved with greatest width near middle, tapering somewhat more posteriorly than anteriorly in dorsal/ventral outline; micropyle a rosette on dorsal surface just posterior to anterior end as seen through stereomicroscope (for details, see description of mature oocyte, below). Color of ovum apparently slightly yellowish. Chorion dorsally and ventrally smooth, clear, except posterior end conspicuously, finely roughened ventrally; eclosion line not evident through stereoscopic exam­ ination, but see description of mature oocyte; chorion of hatched egg apparently split along front and one side.

MATERIAL STUDIED: Three eggs, Chile: Limari Prov. , Las Placetas, 6­XI­2000 (J.G. Rozen); one partial chorion same except 2­ XI­2000. Las Placetas is a village a few kilometers southeast of Pisco Elqui .

REMARKS: The three eggs were glued longitudinally to the inner surface of the cellophanelike interior lining (two separated layers of lining clearly distinguishable, with threadlike strands extending from one layer to the other, as described by Torchio, 1965, for Colletes ciliatoides Stephen and by Rozen and Favreau, 1968, for Colletes compactus compactus Cresson ). The inner surface was identifiable because the outer surface supported the fine filaments that ran to the outer layer. The inner lining was complete (i.e., without holes).

I interpret the extremely flattened appearance of these eggs to be an artifact created by their adhering so closely to the cell lining, in contrast to the more cylindrical mature oocyte (below). What causes the adhesion is unknown; it could result from a sticky ventral surface of the chorion itself or may be created by the female secreting some transparent substance on the lining at the time of egg deposition. The egg not only adheres to the surface, but it may also impress the lining to partially accommodate the thickness of the egg. Consequently, the egg projects little into the cell lumen. When first examined, the pointed posterior end of the egg appeared to be free from the cell lining. On closer examination, I detected a thin, totally transparent sheet of colorless, cellophanelike material (faintly visible in fig. 9) extending from the posterior end a short distance, where it was attached to the cell lining. Examination of the mature oocyte (fig. 10) revealed a flange of finely wrinkled chorion circumscribing the entire dorsal/ventral outline of the oocyte. On the oocyte, the flange drapes down and is more or less appressed to the body of the oocyte. It is longer toward the rear of the oocyte than on the sides or front. On the deposited egg, the flange extends out and attaches to the cell lining, thus forming a continuum with the cell lining that presumably helps to hide the egg from the returning host. Although the rear part of the flange was detected on the egg, I am uncertain whether the sides of the egg in figure 9 are outer boundaries of the flange or of just the body of the oocyte. Examination of freshly deposited eggs should lead to a better understanding of their structure.

There is strong circumstantial evidence that female Isepeolus luctuosus enters host cells that are still open to oviposit. The ventral surface of her egg is attached firmly to the cell lining, and she must somehow manipulate it with her metasoma to extend the flange and to stretch and dorsoventrally flatten the chorion as she oviposits. Cleptoparasites (i.e., Melectini, Ericrocidini, Tetrapediini , Rhathymini, Exaerete ) that open closed host cells insert eggs that are freestanding or loosely attached to the cell closure or wall; their eggs are the more typical elongate ellipsoid eggs without flanges, similar to those of solitary bees. Further, it is unlikely that the parasite female would have time to open the elaborately folded cell closure of cellophanelike material, attach her egg to the lining, and then refold the closure, all while the host female was away gathering food for the next cell to be provisioned in the linear cell series. Eggs of parasites that open host cells tend not to be dwarfs and are obviously not concealed from returning foraging hosts because the host has finished with the cell after its egg deposition and cell closure. Cleptoparasites (e.g., Nomadinae, Protepeolini ) that oviposit in cells still being provisioned while the host is away tend to have dwarf eggs that are hidden in various ways in the cell wall. Melectoides triseriatus has dwarf eggs (Alexander, 1996; table 1, herein), as do the two species of Isepeolus (table 1), and the egg of at least I. luctuosus is hidden by being flattened with a smooth exposed dorsal surface and flange that become a continuum with the cell lining. The oocyte of M. triseriatus is also fitted with a flange, suggesting similar concealment.

The lengthwise attachment of the eggs of Isepeolus luctuosus to the cell lining corresponds to the hole molds on the outer surfaces of the cocoons of Melectoides bellus (Jörgensen) illustrated by Michelette et al. (2000), which were questionably attributed to lengthwise cleptoparasitic oviposition holes in the cells wall of Canephorula apiformis (Friese) . Lengthwise attachments of cleptoparasite eggs to cell surfaces are also known for the nomadine tribes Hexepeolini ( Rozen, 1994b) and Biastini ( Rozen et al., 1997), both of which oviposit in cells before they are closed.

The egg­laying behavior of Isepeolus luctuosus can be compared with that of other cleptoparasites that lay their eggs in colletine cells. Rozen and Michener (1968: figs. 5, 8– 12) reported on the egg deposition of Sphecodopsis (Pseudodichroa) capensis (Friese) in nests of Scrapter longula (Friese) and Sph. (P.) fummipennis Bischoff in those of Sc. crassula Cockerell. Rozen and Favreau (1968 : figs. 1, 2) described the egg deposition of Epeolus pusillus Cresson in the nests of Colletes compactus compactus . Torchio and Burdick (1988: figs. 1–19) provided an exceptionally detailed account of the egg deposition habits of E. compactus Cresson in the cells of C. kincaidii Cockerell. All of these parasitic bees enter the host cells while the cells are still open, so that their eggs are subject to discovery by host females returning with provisions. However, only Isepeolus deposits her eggs lengthwise on the inner surface of the cell lining. All others make small holes in the cell lining and insert their eggs through them so that only the anterior ends of the eggs are flush with the lining. In Epeolus , the exposed end of the egg is a flat or domed surface, presumably helping to obscure the egg from a returning host. With both species of Sphecodopsis , the anterior end of the egg is similarly modified but in addition has a thin flange radiating in all directions over the cell lining. This flange, appressed to the lining, is presumably a homolog of the flange identified in eggs of oth­ er ammobatines ( Rozen, 1986a, 1986b; Rozen and Özbek, 2003) and may help seal the hole from liquids that might seep in or out (nests of Scrapter were in very moist sand) and/or may assist in hiding the egg from the host female.

DESCRIPTION OF MATURE OOCYTE (figs. 10– 12): Length 1.08–1.3 mm, maximum diameter 0.35–0.50 mm (N = 7); egg index 0.31 (dwarf). Shape bilaterally symmetrical along its gently curved long axis with dorsal surface incurved; anterior end broadly rounded, posterior end more narrowly rounded; widest diameter near anterior end; midsection of oocyte very gradually tapering posteriorly; flange of finely wrinkled chorion circumscribing entire dorsal/ventral outline of egg; flange folded ventrally so closely to sides of egg below line of attachment that it is nearly invisible, not forming a conspicuous ridge as in Melectoides triseriatus ; flange more visible toward posterior ends of oocytes because of series of elongate, blisterlike folds as seen in lateral view (fig. 10); micropyle a dorsal, slightly elevated rosette near anterior end consisting of perhaps 40 openings (as judged from fig. 12). Ovum white. Chorion of flange clear, presumably finely wrinkled; chorion elsewhere clear, reflective, and smooth except for finely roughened area ventrally at posterior end; eclosion (hatching) line not visible on uncoated oocyte, but visible on coated oocyte as a narrow band of polygonal plaques with elevated outlines extending around front of oocyte and along both sides, much as in Melectoides triseriatus (fig. 10).

MATERIAL STUDIED: Two females, Chile: Elqui Prov., Las Placetas, 2­XI­2000 (J.G. Rozen); three females, same except 14­X­ 2001 (J.G. Rozen, A. Ugarte, C. Espina) .