Biology and morphology of the immature stages of the cleptoparasitic bee Coelioxys chichimeca (Hymenoptera, Apoidea, Megachilidae)

2010·2.2 MB·English

by  Rozen, Jerome G., (Jerome George)

A tamerican museum
Novitates
PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY
CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024
Number 3679, 26 pp., 73 figures, 1 table March 4, 2010
Biology and Morphology of the Immature Stages of
the Cleptoparasitic Bee Coelioxys chichimeca
(Hymenoptera: Apoidea: Megachilidae)
JEROME G. ROZEN, JR.,1 S. BRADLEIGH VINSON,2 ROLLIN COVILLE,3 AND
GORDON FRANKIE4
ABSTRACT
Herein we investigate the behavior and anatomy of all larval instars of the cleptoparasitic bee,
Coelioxys (Cyrtocoelioxys) chichimeca Cresson. The species is found in Central America with its
host, Centris (Heterocentris) bicornuta Mocsary, one of the cavity-nesting members of the genus.
The egg/mature oocyte of C. chichimeca, unusually small (like known eggs of other Coelioxys), is
described, as is egg placement in the wall of the brood chamber. The anatomy and behavior of each
of the five larval instars is described. The first instar develops within the egg chorion, from which
the second instar emerges. The second and third instars apparently normally remain attached by
their posterior ends either to the egg chorion or to the place where the egg had been attached to the
cell wall. The second instar possesses an array of large spines on the outer surface of each mandible
thought to rupture the thick chorion, thus allowing eclosion. Both second and third instars have
modified head capsules and mandibles enabling them to attack host immatures. Both instars
possess an extremely large pair of spiracles on the eighth abdominal segment and lesser-enlarged
spiracles on the two preceding abdominal segments as well as enlarged internal lateral tracheal
trunks. These modifications are likely related to the need for the larva to acquire air from the
substrate while the body is submerged in nectar. Fourth and fifth instars, no longer attached to the
substrate, assume the morphological attributes and behavior of normal provisions-consuming
megachilid larvae. The last larval instar defecates and afterwards spins a cocoon bearing a
conspicuous nipple. A male pupa is also illustrated and described.
1 Division of Invertebrate Zoology, American Museum of Natural History ([email protected]).
2 Department of Entomology, Texas A&M University, College Station, TX 77843 ([email protected]).
3 6201 Tehama Ave., Richmond, CA 94804 ([email protected]).
4 Department of Environmental Science, Policy, and Management, College of Natural Resources, University of
California, Berkeley, CA 94720 ([email protected]).
Copyright © American Museum of Natural History 2010 ISSN 0003-0082
2 AMERICAN MUSEUM NOVITATES NO. 3679
INTRODUCTION METHODS AND TERMINOLOGY
Baker’s (1971) detailed study of Coelioxys All nests of Centris bicornuta examined were
has stimulated a number of recent investiga¬ in artificial trap nests. Each trap nest was
tions of that genus (Carre and Py, 1981; Rozen composed of a group of 10 individual pieces of
and Kamel, 2006, 2007, 2008) as well as of the wood, 4" XI" X 3/4" [" = inches; 1" = 2.5 cm],
related cleptoparasitic megachiline genus into one end of each had been drilled a 3" deep
Radoszkowskiana. These studies, though re¬ hole, which constituted the preformed cavity
stricted to only a few species, have document¬ in which bees nested. Bore diameters varied as
ed that within this large genus of more than follows: 3/16", 1/4", 5/16", and 3/8". Each
480 species, cleptoparasitic behavior and bundle of 10 pieces of wood was taped
related immature anatomy varies extensively. together with alternate pieces facing opposite
Vinson et al. (in press) present information on directions (fig. 4), so that each trap nest
adult behavior of Coelioxys (Cyrtocoelioxys) consisted of two stacks of five sticks. A double
chichimeca Cresson, which is known from stack (i.e., trap nest) held two boreholes of
southern Mexico to Panama (Discoverlife. each diameter except it held four with 1/4"
org). In the current investigation we examine boreholes. Casual observations indicated that
the same species, in this case exploring larval Centris bicornuta nested primarily in the 1/4"
behavior and associated morphology and and 5/16" boreholes rather than in the 3/16"
providing comparative descriptions of all and 3/8" holes. Each taped trap nest was
immature stages. Females of C. chichimeca provided with a string so that it could be
attack nests of Centris (Heterocentris) hicor- suspended from a nail driven into a tree trunk
nuta Mocsary, an abundant, cavity-nesting or branch. The intent was to have the
bee in Guanacaste Province, Costa Rica. They boreholes approximately horizontal. Groups
may also attack nests of other cavity-nesting
of approximately 10 trap nests were hung on
species of Centris in the same area. one or several adjacent trees in three separate
This investigation was carried out at but adjacent areas of Hacienda Monteverde
Hacienda Monteverde, a ranch owned by (figs. 1-3) at approximate eye level to be
D.A.S. Stewart, 8 km north-northwest of
monitored for nesting activity. At one- or
Bagaces (centered at N10°34.110' W8515
two-week intervals trap nests were collected,
18.419'), a locality used by Frankie and
either to be held in the field lab5 so that adults
colleagues for several years to investigate the
could be reared or to be split open in the field
bee fauna of Costa Rica. This area is a
lab for analyses and collection of immatures
lowland forest (elevation at trap-nest sites
(fig. 7). Simultaneously with the collection of
360-370 ft) on the dry side of the mountains,
trap nests, we replaced them with fresh ones.
dominated in undisturbed areas by low to tall
When emerging adults were to be collected,
trees (maximum height 25 m). The three trap-
trap nests were disassembled in the lab, sticks
nest sites (figs. 1-3) for the study were along
were individually labeled for locality and time
the edge of a forested area (N10°35.506'
of collection, and a vial was taped to each
W85° 18.280') with a large open agricultural
opening to receive emerged adults (fig. 6).
field immediately to the south. Although
Observations in Costa Rica were made with
J.G.R.’s participation in the field study in
a Leitz stereomicroscope and recorded with a
Costa Rica extended from February 10-24,
Cannon PowerShot SD880 IS camera held to
2009, S.B. and G.F. had conducted an
the ocular lens of the stereoscope.
extensive trap-nesting study in the late 1990s
Immatures in the American Museum of
and early 2000s in the area surrounding the
Natural History lab were always examined
main study site referred to in this paper. In
first with a stereoscope. If they were to be
addition to a wealth of year-round informa¬
cleared for study, larvae with heads partly
tion on the bees and wasps that use stick traps,
severed from bodies were boiled in an aqueous
the study also provided insight on the
locations for the greatest diversity of bee
5 The hotel where the authors stayed while in Costa Rica
species and their associates (Frankie and
kindly provided space for dissecting and examining trap
Vinson, in prep.). nests and for storing specimens and equipment.
2010 ROZEN ET AL.: BIOLOGY OF CLEPTOPARASITIC COELIOXYS CHICHIMECA 3
Figs. 1-7. Photographs of trap nests and the trap-nesting sites at Hacienda Monteverde, where Centris
bicornuta was induced to nest. 1. Approximate position of three sites (A, B, C) in the forest along the
northern edge of a large agricultural area. 2, 3. Trap nests hung from nails driven into trees and branches at
. .
sites A and C, respectively. 4 Close-up of one trap nest consisting of 10 individual sticks. 5 Female perched
outside nest waiting for host female to enter or leave (photo courtesy of Rollin Coville). 6. Individual sticks
being held to retrieve emerging adults of host and cleptoparasites. 7. An individual nest stick opened to
reveal nest structure and immatures.
4 AMERICAN MUSEUM NOVITATES NO. 3679
solution of sodium hydroxide until cleared. placement zone of Coelioxys chichimeca
eggs in cell wall
After staining with Chlorazol Black E in
ethanol, they were transferred to glycerin- "s
filled well slides for detailed examination with
stereoscope and/or compound microscope.
Numerous cast exoskeletons attached to lar¬
vae were also a source of valuable information
concerning the anatomy of the different
instars and early on solved the puzzle of the
sequence of instars.
Some immatures were examined with a
Hitachi S-5700 scanning electron microscope
(SEM) after they were critical-point dried and
coated with a gold/palladium alloy.
Fig. 8. Diagram of a cell of Centris cornuta,
We introduce here a new statistic, cranial
cross-section, side view, identifying the zone in
swelling index. With many cleptoparasitic bees
which eggs of the cleptoparasite, Coelioxys chichi¬
there is a tendency for the cranium to become
meca, have been found embedded in the cell wall, in
enlarged in the hospicidal instar, often in relation to the distribution of stored provisions.
association with thickening and resulting
darkening plus sclerotization of the parietal capsules, thereby enhancing mandibular
cuticle. Rozen (1991) postulated that this is strength and attacking dexterity.
probably due to the strengthening and enlarg¬ In describing mandibular shape we use the
ing of parietals required for operation of extra term fanglike: long, curved, tapering to a
adductor musculature involved with the large, single sharp point, sometimes with a more
forceful mandibles required for killing host extreme curvature near the apex (fig. 45).
immature or immatures of competing clepto- In the biology section, we use the terms cell
parasites. The index is determined by dividing wall and cell lining in regard to brood
the maximum horizontal width of the foramen chambers of Centris bicornuta. With this
magnum by the maximum horizontal width of species, the cell wall is simply the bore of the
the head capsule. Thus, the lower the index trap nest, the material that closes the borehole
value, the greater the swelling. However, in the at the rear of the chamber, and the thin,
case of third instar Coelioxys chichimeca the transparent to semitransparent coating that
low value of the index is probably also partly covers the inner surface of the cell. The cell
explained by the head capsule being wide, thus lining is that thin, transparent coating. It is
enhancing the chance of widely opened thought to be waterproof and a barrier to gas
mandibles (fig. 18) encountering and grasping exchange.
victims in a totally dark environment. Note In the figures, we use the following abbre¬
that the widest part of the head capsule is at viations: PTP = posterior tentorial pit. T =
the bases of the mandibles. metasomal tergum (e.g., T6 = sixth metaso-
Rozen (1991) has also hypothesized that mal tergum). S = metasomal sternum (e.g., S6
muscle strength in some cleptoparasitic larvae = sixth metasomal sternum).
is increased by lengthening of the head capsule
rather than by its swelling since both modifi¬
BIOLOGY
cations add more space for the attachments of
massive musculature. There is also a tendency All information on the nesting biology of
among hospicidal instars, whether with en¬ Centris bicornuta and the cleptoparasite,
larged, globose heads or elongate ones, to Coelioxys chichimeca, came from three trap-
have the labiomaxillary regions of the head nest sites (fig. 1). A fully provisioned nest cell
more extensively sclerotized than those of of this host species, diagramed in figure 8,
related solitary bees, often in association with contains a layer of opaque, densely packed
development of a ventral postoccipital bridge. pollen that the female host bee first loads into
These modifications add rigidity to head the rear one-third of the cell. The front face of
2010 ROZEN ET AL.: BIOLOGY OF CLEPTOPARASITIC COELIOXYS CHICHIMECA 5
the pollen is deeply concave. The host then around the entrance. These summary obser¬
deposits a similar quantity of clear nectar vations have been described and documented
(Vinson et al. 2006) against the pollen surface by Vinson et al. (submitted).
to which it adheres because of its sticky, thick We observed eight or nine cleptoparasitic
consistency. The nectar’s surface is also oviposition sites with eggs in place, all
concave, more or less conforming to the partially buried lengthwise. In each case the
concavity in the pollen. The cell wall in front long axis of an egg was more or less parallel to
of the surface is barren except for the cell the inner cell surface. All had been inserted far
lining; the nectar does not extend foreword to enough to reach the substrate beyond the cell
the cell closure. Thus the front end of the cell lining (fig. 14), possibly a significant require¬
is empty; a “dry” area remains on the sides, ment for obtaining air, as discussed below.
top, and bottom of the cell wall between the Egg insertion sites were either where the
cell closure and the voluminous nectar and pollen-covered surface was shallow (fig. 8) or
pollen provisions. Figure 8 identifies the zone in the nectar area (fig. 8) in front of the pollen
where we have detected the egg insertion pits surface. A few eggs were not covered even by
of C. chichimeca in the dry area of the cell wall clear nectar (i.e., inserted in the dry area of the
in front of the provisions, as well as in the cell cell wall) and others were shallowly covered,
wall under the clear nectar area, and also but in some cases the nectar covering may
under the densely packed pollen. Vinson et al. have resulted accidentally during our trans¬
(submitted) noted that most of these egg porting the trap nests to the field laboratory.
insertion pits were placed in the upper 3/4 of In all cases the egg was positioned in the
a cell, but the distance from the cell cap was excavation with the broad anterior end facing
not determined. the cell closure and the narrow posterior end
Oviposition: The distance between floral inserted in the opposite direction and buried
resources and the trap-nest sites was not more deeply than the anterior end; hence, eggs
determined, but abundance of host females were inserted slightly obliquely (i.e., “toe-
at the trap nests demonstrated that resources nailed”) into the cell wall. Excavations were
were clearly nearby in the form of flowering elongate ovals, just sufficiently large to ac¬
trees. Coelioxys chichimeca visits to the three commodate the egg (i.e., about 1 mm long)
trap-nest sites were moderately frequent but and presumably made by the female at the
mostly single events in that usually only one time of oviposition, probably with the elon¬
parasitic female was seen at a time. She would gate, sharply pointed median process of
suddenly appear at one trap nest, swiftly circle metasomal sternum 6. Depth of excavation
around it, then swoop to the next trap nest, relative to the cell’s inner surface varied from
and on to other nests, until she discovered an shallow (so that the exposed surface of the egg
appropriate one. When a female cleptopar- projected above the cell surface; fig. 10) to
asite detected an opening of interest, she deep (exposed egg surface well below the cell
hovered briefly in front of the entrance, and surface). Mature oocytes/eggs are described in
occasionally she alighted and entered head¬ Ovarian Statistics and Descriptions of
first. On emerging she either departed or Immatures, below.
reversed her direction at the entrance and re¬ In addition to these successfully inserted
entered backward. Emerging again shortly eggs, we observed a number of elongate-oval
afterward, she would fly away. We interpret insertion pits that in a few cases showed
the backward entrance of the female as an remnants of vacated egg chorions (presumably
indication that she was about to oviposit in evidence of successful insertions) (fig. 13),
the cell. Occasionally, we observed a female of which are sufficiently thick that they do not
C. chichimeca with raised antennae perching seem to dissolve as do chorions of nonpara-
outside an entrance presumably waiting for sitic, solitary bees, or, more frequently,
evidence of a host female’s departure or return exhibited insertion pits without vacated cho¬
(fig. 5). Such behavior might continue for rions (fig. 14). Such pits were encountered in
some minutes, often with the cleptoparasite cells without other evidence of cleptoparasit-
taking short flights to reposition herself ism as well as in cells with another pit holding
6 AMERICAN MUSEUM NOVITATES NO. 3679
Figs. 9-14. Microphotographs of egg and egg insertions of Coelioxys chichimeca in cells of Centris
. . .
cornuta. 9 Individual egg extracted from cell wall. 10 Egg in shallow pit. 11 Eclosing second instar with
. .
head emerged from chorion. 12 Egg with dark mandibles and parietals of second instar visible. 13 Egg
.
insertion pit where only chorion of cleptoparasite remains. 14 Egg insertion pit lacking evidence of egg.
an egg. An insertion pit without even a had already been attacked and removed the
vacated chorion may represent an incomplete first egg or (2) that a returning Centris
act of egg deposition, perhaps occasioned by bicornuta female destroyed an offending par¬
sudden return of the host female, but it may asite egg.
also be evidence (1) that a second female Although discovered oviposition sites were
Coelioxys chichimeca encountered a cell that in cell walls where there was either no pollen
2010 ROZEN ET AL.: BIOLOGY OF CLEPTOPARASITIC COELIOXYS CHICHIMECA 7
- .
Figs. 15-19. Photomicrographs of Coelioxys chichimeca. 15 17 Three frames of single third instar
.
demonstrating reach of activity while posterior end attached to egg chorion imbedded in cell wall. 18 Close-
up of head of another third instar showing spread of mandibles enabling it to seize victim immediately on
.
contact. 19 Second instar immersed in nectar while posterior end attached to chorion inserted in cell wall
under pollen layer of provisions.
or only a shallow layer, we also discovered sharply defined tubercle of questionable ho¬
several second instars (sometimes with only mology. Whatever the instar’s adaptive func¬
their heads visible through the nectar extend¬ tions, it represents a life stage that obviously is
ing from a hole in deeper pollen, figs. 8, 19), necessary for development of the second instar
an indication that eggs are sometimes also with its distinctive, darkly pigmented head
deposited farther back toward the rear of cells. capsule and mandibles, i.e., the stage that
Such submerged larvae raise the interesting hatches from the egg.
question of how these active larvae acquire Eclosion, i.e., the hatching of the larva from
oxygen, a subject discussed below. the egg, occurs as the second instar slowly
Larval Instars and Their Behavior: Like emerges, leaving first-instar exuviae behind in
other Coelioxys species that have been studied the chorion, as evidenced in figure 32. We
in detail, C. chichimeca has five larval instars were able to monitor eclosion of the second
(Baker, 1971; Rozen and Kamel, 2006). The instar in detail on one occasion, and we also
first instar (fig. 32) is known only from cast observed the early stages of eclosion in two
exuviae in a single egg chorion still attached to other cases. During the monitored eclosion we
the rear part of the abdomen of a second looked through the chorion to see the open-
instar that had been preserved. The cast skin ing-and-closing movement of the mandibles
was discovered appressed to the inner surface and their developing pigmentation. We think
of the chorion near the rear end of the egg. As it highly likely that the mandibular motion
indicated in the description, below, it is causes the array of sharp-pointed, diverging
without pigment and weakly sclerotized. Its basal mandibular tubercles as well as the more
tracheal system and internal head ridges apical tubercle on the outer mandibular
cannot be identified. Only a pair of mandibles surface to rupture the chorion, thus allowing
is visible, except laterad of each is a small, the larva to emerge. In both instances of
AMERICAN MUSEUM NOVITATES NO. 3679
observed eclosion, the second instar had its Japanese, not read by current authors) for C.
ventral surface facing the exposed chorion {Coelioxys) elongata Lepeletier. The bodies of
(fig. 11), so that its dorsal surface was buried the larger second and third instars of C.
against the cell wall. In one instance, the chichimeca (figs. 33, 38, 41) appear unusually
opening-and-closing mandibles were detected elongate (more so than comparable instars of
around 9 p.m. and by the following morning, C. bicornuta) suggesting that elongate body
the larva had partly emerged from a large form was involved with their attachment to
circular hole near the anterior end of the their natal origins. We found a few second
chorion (fig. 11); the rear part of the body was instars submerged in nectar in thicker layers of
still clearly contained in the posterior end of pollen (fig. 19), but in hindsight, after exam¬
the chorion. Thus the larva was bent U- ining photographs, we had apparently over¬
shaped, so that its anterior part pointed looked that attachment in some of the third
toward the rear of the chorion. When touched instars because their posterior ends where
with forceps, the anterior end immediately obscured in provision. When one sees a larva
rose up with mandibles opening and closing in attached to a relatively dry surface (e.g.,
an aggressive display so that the anterior end figs. 15-17), it is clear such seemingly gravi¬
was at right angles to the cell wall. The ty-defying acrobatics requires that the larva be
erection of the anterior part of the body and attached by it posterior end.
gnashing of mandibles was accompanied by We think that such attachments may serve
searching gyrations of the anterior body two needs: (1) to obtain air in cases in which
region, a behavioral pattern that J.G.R. has the small cleptoparasitic larva is submerged
seen with third larval instars of other under nectar (fig. 19), and (2) to provide a
Coelioxys species. This behavior indicates that stable fixed surface so the hospicidal larva can
the second instar of this species is equipped to successfully attack the host immature on or in
fight other cell inhabitants, a conclusion a surface covered by nectar. We explain these
supported by the strongly sclerotized and two hypotheses as follows:
pigmented mandibles and head capsule, by
(1) The need for air relates to observations
the aggressive behavior of the second instar
that at least some eggs of C. chichimeca
observed in a number of cases, and by dead
are attached to the substrate where they
host immatures in cells with second instars of
are submerged below the nectar surface
Coelioxys. or even further into the pollen provisions.
The second instar whose eclosion we mon¬ The fact that the posterior ends of the
itored remained attached to the egg insertion second and third instars have greatly
point all of the second day, feeding on the enlarged spiracles (see Ovarian Statistics
nectar that coated the surroundings of the egg and Descriptions of Immatures, below)
deposition site, so that the larva grew in size. suggests that larvae obtain air by use of
During the second night, it molted to the third enlarged spiracles. Although this discov¬
instar and was preserved the following morn¬ ery at first seemed counterintuitive be¬
ing. cause the posterior ends of these larvae
We think it likely that second and third are submerged deeper into the nectar than
instars (the latter often with cast skins of the anterior ends, we think that sufficient
the previous instar clinging to their bodies) air to supply the larva comes from or
are normally attached by their posterior ends through the substrate even if it is only
to the chorions embedded in the cell walls. wood. This hypothesis proposes that the
Although some free-ranging young instars egg deposition pits, penetrating through
were also sighted, attachment of a small the presumably airtight cell lining to the
larva to the egg placement was a signi¬ wood fibers below, are the source of air
ficant and noteworthy phenomenon. Baker for the larvae until they can rely upon air
(1971) reported this phenomenon for C. in the brood cell. This connection would
(Boreocoelioxys) octodentata Say and C. also permit larger larvae to submerge
{Boreocoelioxys) sayi Robertson, as apparent¬ while they feed beneath the liquid surface.
ly did Iwata (1939) (fide Baker, 1971; in This hypothesis is supported by the fact
2010 ROZEN ET AL.: BIOLOGY OF CLEPTOPARASITIC COELIOXYS CHICHIMECA 9
that all spiracles in the fourth and fifth expressed by other early instars in the
instars, which are no longer attached to family?
the substrate, are subequal in size (i.e., the This leaves unexplained the free-roving
norm for bee larvae). Questions that small larvae of Coelioxys chichimeca that we
require further study include, How do occasionally saw. These may be individuals
enlarged spiracles of second and third that have already destroyed the host or
instars connect to air supplied by the perhaps had been accidentally dislodged by
substrate? what role (if any) does egg our manipulations.
chorion play in the transfer of air to the The two final instars did not appear to be
spiracles? and what mechanisms enable attached in any way to their chorions but
the larva to remain attached to the egg simply fed on the provisions, as do larvae of
insertion point (although we wonder the host species.
whether the unusually small 10th abdom¬ The observations reported above only partly
inal segment might remain in the egg answer the requirements for successful ovipo-
chorion and thus anchor the larva)? sition and eclosion of C. chichimeca. We have
(2) Attacks on host immatures are often observed some eggs inserted in the cell wall
preceded by strong, gyrating, searching where there is no pollen or nectar that a second
movements of the sometimes elevated, instar could ingest if it hatches, and we have
anterior part of the larva’s body (fig. 15- also seen that second instars feed and grow as
17) or by the nearly motionless, elevated they gradually emerge from their chorions
anterior part of the body while mandibles surrounded and covered by a thin layer of
are widely opened (fig. 18). Mandibles provisions. Does this mean that those eggs
are rapidly closed when the larva encoun¬ removed from larval resources will not survive?
ters the host (or is teased with a probe). We have seen none do so, but data are scant.
Second and third instar bodies are slender
Although position of the apical tubercle on
and agile and can rapidly twist and bend
the outer apical surface of the mandible suggests
to subdue host immatures. The body
that it may be instrumental in rupturing the
actions are enhanced if the cleptoparasite
chorion, future investigations should consider
has a firm point of contact with a stable
the possibility that it might also function to limit
substrate (i.e., egg insertion point) since
the penetration of the mandibular apex deep
the entire muscular force of the larva’s
into the host, thus preventing entanglement of
body can be directed toward the host.
the mandible with the host. This possibility
Without a fixed point, the body would be
should also be considered for the smaller, but
unable to muster the same strength
now more apical, basal mandibular tubercles of
because the immediate environment (nec¬
the third instar (fig. 45).
tar) is fluid and therefore too yielding.
In summary, our observations, supported
The elongate length of the larva anchored
by larval anatomy, indicate that the first instar
only by its posterior end permits the larva
remains in the chorion and has no direct
with mandibles widespread to extend the
contact with the environment in the cell. The
search area for the host (figs. 15-17).
second instar is the one that ecloses, has
It seems unlikely that attachment of the special anatomical modifications (spines on
posterior ends of second and third instars to the outer mandibular surface) to do so, and,
their eggs is a special adaptation to overcome during and after eclosing, can and often does
the thick layer of nectar on the surface of the kill (with strongly curved, sharply pointed
provisions because of the identical attach¬ mandibles) the host egg or young larva. The
ments reported for other species where hosts third instar has reduced mandibular spines
do not cover the provisions with a separate (the subapical one completely lost) and has
layer of nectar (Baker, 1971; Iwata, 1939). We even longer and more apically curved mandi¬
note that many Megachilidae have early bles than before (fig. 45), so that it is equipped
instars that remain sessile on egg insertion morphologically and behaviorally to kill the
points; might the behavior in Coelioxys be host larva and/or larvae of other cleptopar-
merely an expression of the sessile behavior asites. Both second and third instars feed on
10 AMERICAN MUSEUM NOVITATES NO. 3679
provisions as evidenced by their increase in number for all bee families except the
body size within and between stadia. We have Apidae. On average each female carried eight
insufficient data to estimate which of these mature oocytes or 1.33 mature oocytes per
two instars is more successful at eliminating ovariole. These are high numbers for non-
the immature host. Fourth and fifth instars cleptoparasitic bees but within the range for
are probably the main feeding instars and, in cleptoparasitic ones including other species of
addition, the fifth instar defecates (but we are Coelioxys (Rozen, 2003; Rozen and Kamel,
uncertain whether defecation commences soon 2007). Rozen (2003) explored the possible
after the start of the stadium or only after reasons for cleptoparasites having so many
food is totally consumed). After provisions are mature oocytes. The egg index (i.e., the length
consumed and defecation is finished, the last of the largest mature oocytes, divided by the
larval instar spins its cocoon, as evidenced by distance between the outer rims of the tegulae,
the presence of fecal pellets only on the outside a statistic developed by Iwata and Sakagami,
of the cocoon. 1966) of Coelioxys chichimeca averaged 0.33
The single pupa, a male, recovered from a for the two females. This value places this
cell was found in a thin-walled, almost species in the dwarf category (Iwata and
transparent cocoon that conforms to the inner Sakagami, 1966: table 2), with other members
shape of the cell. Its front end was faintly of the genus, all of which are either dwarf or at
convex (conforming to the cell closure), least small, as is characteristic of most
bearing a central, dark brownish-red, opaque cleptoparasitic bees (Rozen, 2003).
nipple of fibrous silk (i.e, the “disc” of Rozen
and Kamel, 2007). Pale, elongate fecal pellets,
Description of Egg/Mature Oocyte
mostly less than four times their maximum
diameters, were loosely attached to the outer Figures 9, 20-23
surface of the cocoon except for its front (cell
closure) end. The pupa is described below. Diagnosis: The egg/mature oocyte of
Coelioxys chichimeca can easily be distin¬
OVARIAN STATISTICS AND guished from those of other Coelioxys and of
DESCRIPTIONS OF IMMATURES Radoszkowskiana by the ridge that extends
lengthwise around it (figs. 20, 21, 23); this
We obtained all specimens described here feature has not been reported before for other
between February 10 and 24, 2009. Identi¬ congeneric species (Graenicher, 1905; Iwata,
fication of larval instars was simplified because 1939, 1955, 1965; Baker, 1971; Rozen, 2003;
the cast exoskeleton of previous instars (though Rozen and Kamel, 2007). Shortness compared
not the first) often remained on the sides or with its maximum width and its tapering
undersurface of the live specimen. Not uncom¬ shape in dorsal or ventral views are also
monly, we encountered fourth instars attached unusual, though perhaps more difficult to
to which were skins including head capsules of compare with similar features in other taxa.
the previous two instars. Table 1 compares the Nonetheless, the micropyles of all that have
diagnostic features of the larval instars. been studied with an SEM are similar (fig. 22;
Descriptions of larval instars 2-4 are com¬ Rozen, 2003: figs. 60, 61; Rozen and Kamel,
parative to explore changes in anatomy that 2007: fig. 33)
take place. Description of the last instar Description: Length approximately 1.0 mm;
addresses the same anatomical features but approximate maximum width 0.4 X 0.45 mm
also incorporates structures that have been (two dimensions because eggs/mature oocytes
referred to in accounts of other larval Coelioxys are slightly flattened), which is close behind the
(e.g., Baker, 1971; Rozen and Kamel, 2007). anterior end. Shape slightly curved with ventral
surface concave in lateral view; anterior end
broadly rounded in dorsal/ventral views; max¬
Ovarian Statistics
imum breadth near anterior end, tapering
Two females of Coelioxys chichimeca each evenly posteriorly toward narrowly round
had three ovarioles per ovary, the basic posterior end in both lateral and dorsal views