Hospicidal Behavior of the Cleptoparasitic Bee Coelioxys (Allocoelioxys) coturnix, Including Descriptions of Its Larval Instars (Hymenoptera: Megachilidae)

2008·13 MB·English

by  Jerome G. Rozen

PUBLISHED BY THE AMERICAN MUSEUM OF NATURAL HISTORY
CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024
Number 3636, 15 pp., 29 figures December 31, 2008
Hospicidal Behavior of the Cleptoparasitic Bee
Coelioxys (Allocoelioxys) coturnix, Including
Descriptions of Its Larval Instars
(Hymenoptera: Megachilidae)
JEROME G. ROZEN, JR.1 AND SOLIMAN M. KAMEL2
ABSTRACT
In an attempt to determine whether Coelioxys and Radoszkowskiana, both cleptoparasitic
members of the Megachilini, had a common cleptoparasitic ancestor, an investigation of the
nestingbiologyandimmaturestagesofC.(Allocoelioxys)coturnixPe´rezwasundertakeninEgypt.
Thepurpose wasto compare these aspects of this species withthe results of a recentstudyof R.
rufiventris(Spinola)andcertainotherspeciesofCoelioxys(RozenandKamel,2007).TheeggofC.
coturnix is deposited on the egg of Megachile minutissima Radoszkowski after the host female
departs to collect cell-closure material. On hatching, the first instar, still surrounded by egg
chorion,bitesthedevelopinghosteggandconsumestheentireeggcontentbeforefeedinguponthe
host provisions. This behavior contrasts with certain other species of Coelioxys, whose eggs are
hiddeninthehostcellwhileitisbeingprovisionedandthirdinstarsnormallykilltheyounghost
larvae. Because the behavior of C. coturnix closely mirrors that of R. rufiventris, the authors
concludethattwomodesofcleptoparasitismhavedevelopedinCoelioxysandthatCoelioxysand
Radoszkowskiana possibly had a common cleptoparasitic ancestor. The five larval instars of C.
coturnix are described and compared with those of other Coelioxys species, and its first instar is
comparedwiththatof R.rufiventris.
1AmericanMuseumofNaturalHistory([email protected]).
2DepartmentofPlantProtection,FacultyofAgriculture,SuezCanalUniversity,Ismailia,Egypt(soliman_90@hotmail.
com).
CopyrightEAmericanMuseumofNaturalHistory2008 ISSN0003-0082
2 AMERICAN MUSEUMNOVITATES NO. 3636
INTRODUCTION generahadacommoncleptoparasiticancestor
or whether each evolved their cleptoparasitic
Well over a century ago, Ferton (1896) lifestyle independently. Sharply different
reportedtwoinstanceswhereheobservedthat
modes of parasitism would suggest the latter;
females of Coelioxys (Allocoelioxys) afra
similar modes would argue for a common
Lepeletier oviposited so that the anterior ends
cleptoparastic ancestor.
of their eggs rested on the host eggs while the
To summarize our finding, we concluded
posterior ends were in the provisions. This
that the
occurred while the host females were presum-
ablygatheringleafsnippetstoclosethecellsin
female Radoszkowskiana rufiventris en-
the same nests. In one instance, he noted that
ters the host nest when the host is away
twodayslaterthecleptoparasiticeggandhost
presumably gathering closure material,
egg were in the same position. In the evening
deposits her egg on top of the host egg,
of the second day the parasite’s head had
which is resting on the surface of the
becomedefined,andheconcludedthattheegg
provisions,andthendeparts.Itsembryo
had hatched. The resulting young larva then
developsrapidlysothatithatchesbefore
sucked the contents of the host egg, which
the host does. Still surrounded by most
subsided into the food, and within two days
ofitschorion,itkillstheembryonichost
the egg was entirely empty. Afterward, the
by biting it with strongly curved but
parasitelarvafedontheprovisions.Hisreport
short, fanglike mandibles that bear a
thus indicates that the Coelioxys egg is
tiny spined second tooth basally.
deposited after the host female has deposited
Without moving its head, it then pro-
her egg and implies that the first instar (and
ceeds to ingest the entire contents of the
perhaps subsequent ones) of the Coelioxys
chorionoveraperiodofmorethanaday
killsthehosteggandfeedsontheeggcontents
whileremainingmotionlessontopofthe
before feeding on the provisions.
host egg. Its body slowly swells as the
As noted by Rozen and Kamel (2007) these
host egg is depleted. Except for the
observations do not match the detailed ac-
fanglike mandibles and short incubation
count by Baker (1971), who found that the
period, there are no other obvious
third instars of Coelioxys (Boreocoelioxys)
adaptations of the first instar for its
octodentata Say and C. (B.) sayi Robertson,
parasitic role. The second instar starts
with highly modified head capsules bearing
feeding on the provisions by moving the
elongate mandibles, are primarily responsible
anterior part of its body to one side or
for eliminating the host immatures (by that
the other of the deflated host egg. Its
time larvae); furthermore, their eggs are
introduced into the host cells before the hosts mandibles are apically bifid as are those
have deposited their eggs. Baker’s finding of all subsequent instars, presumably
corresponded exactly with those of Carre´ adapted for feeding on the provisions.
and Py (1981) on a species they called C.
rufocaudataSmith,questionablyasynonymof These results seemed highly suggestive of
C. (Allocoelioxys) echinata Fo¨rster. Baker’s those of Ferton. Our next step was to verify
discovery was also fully supported by our what Ferton had reported. In the absence of
investigation of Coelioxys (Liothyrapis) deci- Coelioxys afra, we had available a close
piensSpinola(RozenandKamel,2006,2007). relative, C. (Allocoelioxys) coturnix Pe´rez.
The apparent discrepancies between Thisspeciesisabundantinthevicinityoftrap
Ferton’sreportandthesubsequentonescame nestsonthecampusofSuezCanalUniversity,
into focus while we were studying the biology where it attacks the nests of Megachile
and immature stages of Radoszkowskiana (Eutricharaea) minutissima Radoszkowski.
rufiventris (Spinola) (Rozen and Kamel, This paper intends primarily (1) to report on
2007). The latter genus, like Coelioxys, is our investigation into the behavior and
cleptoparasitic and also a member of anatomical adaptations involved with clepto-
Megachilini. One of the questions we hoped parasitism in this species and, on the basis of
toresolveinthatstudywaswhetherthesetwo these findings, (2) to consider further the
2008 ROZENAND KAMEL: BEHAVIOR OFCOELIOXYS COTURNIX 3
Figs.1–3. Trap-nestpanels,SuezCanalUniversity,Ismailia,Egypt.1.Fivepanelsdeployedoncampus.
2.Close-upofpartofonepanelshowingnestingstrawsprojectingfromholesinpaintedfoamplasticanda
femaleofCoelioxyscoturnixatoneentrance.3.Neststrawremovedfrompanelandopenedtoexposeleaf-
linedcellsof Megachile minutissima.
origin(s) of cleptoparasitism in the Megachi- of more permanent construction materials.
lini. The current study was greatly assisted by the
availability of abundant immatures obtained
from the array of large trap-nest panels
MATERIAL AND METHODS
(sometimes referred to as ‘‘polystyrene nest
Fieldwork for this paper took place from blocks’’) used in this program (figs. 1, 2).
April 24 to May 10, 2007, on the campus of Thesepanelsconsistoflargeblocksofpainted
Suez Canal University, Ismailia, Egypt foam plastic (described elsewhere in greater
(N30u379100 E32u159580). There one of us detail: http://www.pollinatorparadise.com/
(S.M.K.) has been pursuing a solitary-bee Egypt.htm) in which are inserted rows of
rearingprogramtodeveloppollinationservic- hollow paper tubes (‘‘straws’’) about 12 cm
es for alfalfa and other crops because of the long and 5 mm in diameter. The blocks are
dwindling nesting opportunities for solitary placed in the field close to the crop plantings,
bees in old, adobe structures (see Rozen and and bees such as Megachile minutissima that
Kamel,2007)duetotheincreasingavailability nest in preformed cavities find and use these
4 AMERICAN MUSEUMNOVITATES NO. 3636
straws for their nests. When removed and parasite and only a few of the hosts were
taken to the lab, straws containing nests are observed there, but they were swept from
slit longitudinal so that nest contents can be blooming alfalfa plants adjacent to the nest
examined and appropriate immatures of host panels. It seems likely that mating of C.
and cleptoparasite collected for study (fig. 3). coturnix does not occur at nest entrances but
We also availed ourselves of specimens that takes place in the vicinity of the host plants.
S.M.K.isrearingattheIsmailiaExperimental Although we occasionally observed female C.
Station, Agricultural Research Center, coturnix enter nest straws, their visits were
Ismailia. Because this locality is only a few brief, suggesting that they did not result in
kilometers from the university, observations ovipositing.
from there are not differentiated from those A number of other hymenopterans in
recorded at the university. addition to Coelioxys coturnix were seen
In our investigations dealing with develop- around the nest panels, including Osmia
ment, we relied heavily on retrieving the cast submicans Morawitz (Megachilidae) and
exoskeletons (hereafter termed skins) to dis- Sapyga luteomaculata Pic (Sapygidae). The
tinguish instars on an anatomical basis. The latter species is a cleptoparasite of Megachile
skins are stacked one on top of the preceding minutissima and O. submicans (Rozen and
one under the feeding larva and can be gently Kamel,2007).Asamplingofspecimensbynet
removed, separated from one another, and sweeping over the surface of the panels on
examined.Preservedinstarswereclearedinan May 28 for a period of about 5 min yielded
aqueoussolutionofpotassiumhydroxideafter the following proportions: M. minutissima: 3
the head was partly severed from the body. males, 38 females; C. coturnix: 0 males, 18
Heads were washed, transferred to ethanol, females; O. submicans: 2 males, 0 females; S.
lightly stained with Chlorasol Black E, and luteomaculata: 0 males, 2 females.
studied in glycerin on well slides. Cast skins EGGS AND EGG DEPOSITION: The mature
were simply retrieved, washed, and placed in oocytes of Coelioxys coturnix were previously
glycerin on the same well slides with the described (Rozen and Kamel, 2007). We
preserved instar. foundthatfourdepositedeggshadanaverage
Because first instars remained cloaked by lengthof1.1 mmcomparedwith1.47 mm,the
the egg chorions, details of their anatomy are average length of four oocytes in the previous
hidden from view. We removed parts of the study (Rozen and Kamel, 2007). The average
chorion from specimens after they had been length of four eggs of Megachile minutissima
critical-point dried and placed on a scanning was 2.56 mm. Thus the length of the clepto-
electron microscope (SEM) stub by gently parasite egg isconsiderably less than half that
pattingthechorionwiththestickysurfaceofa of the host.
sharply pointed sliver of cellophane tape. Wefoundnumerous(50+)eggsofCoelioxys
Patches of the chorion were thus removed. coturnix. Most were either parallel to and on
Preserved specimens were examined with a the top surface of the host eggs (fig. 4), which
Hitachi S-5700 SEM after being critical-point floatedonthesurfaceofthestickyprovisions,
dried and coated with gold/palladium. Others draped somewhat diagonally across the host
were studied with a Zeiss EVO 60 SEM. eggs on the provisions (fig. 6), or lying on
their side, firmly attached to the chorions of
HOSPICIDAL BEHAVIOR the hosts while both were floating on the
provisions (fig. 7). Most were affixed to the
ADULT ACTIVITYAND ABUNDANCE: During rear half of the host egg, but a few were
our observations in April/May, females of farther forward. Many of them were so far
Coelioxys coturnix flew in considerable num- back on the host egg that their posterior ends
bers over the vertical trapnest panels (fig. 1), wereintheprovisions(fig. 6),althoughothers
on which they occasionally alighted. They didnotcontacttheprovisionsatall.Inalmost
were accompanied by host females, which allcasestheanteriorendofthecleptoparasitic
were arriving, departing, and searching for eggpointedinthesamedirectionasthatofthe
suitable nest straws. No males of the clepto- host.
2008 ROZENAND KAMEL: BEHAVIOR OFCOELIOXYS COTURNIX 5
Figs. 4–8. Macrophotographs of live eggs and early instars of Coelioxys coturnix and eggs of its host,
Megachileminutissima.4.EggofC.coturnixonhostegg.5.ShroudedfirstinstarofC.coturnixfeedingon
partlydepletedeggofhost.6.LiveeggofC.coturnixwithitsposteriorendslightlysubmergedinprovisions
andpositionedslightlydiagonallyonhostegg;notesecondeggofC.coturnixremovedfromhosteggand
restinginprovisions.7.EggofC.coturnixattachedtohostegg,bothrestingontheirsides.8.Livefirstinstar
ofC.coturnixfeedingonhosteggwithlargeeggofSapygaluteomaculata,readytoeclose,nearbyonsurface
ofprovisions.
Obviously, these cleptoparasite eggs were bydifferentfemalesratherthancasesofdouble
deposited after the host female had laid her or triple oviposition by a single cleptoparasite
egg, probably at the time that the host female becauseoftheinfrequencyoftheiroccurrence.
was gathering leaf snippets to close the cell. We suspect that if double oviposition by
Cellscontainingtheseeggsgavenosuggestion females were normal as proposed for certain
that they had been opened by the cleptopar- Nomada (Linsley and MacSwain, 1955), we
asite after the host female had sealed them, wouldhaveencountereditmorefrequently.In
and all cleptoparasitic eggs were deposited on many of these cases one of the parasitic eggs
freshlydepositedhosteggsthathadnotimeto seemed to have been removed from the host
develop. Hadtheybeen found witholder host egg,perhapssuggestingthatthesecondclepto-
immatures, this would imply that the clepto- parasite female to arrive had dislocated the
parasitic female had oviposited by somehow earlieregg.Inthefewcasesinwhichmorethan
inserting her egg into the cell after the host one egg survived for a time, we observed no
female had closed it. cases in which both eggs survived longer than
Although most of the eggs were deposited beyond the second instar. Unfortunately, we
onetoabroodcell,anumberofcellscontained were unable to gather data as to whether a
two (fig. 6) or even three eggs of Coelioxys cleptoparasitic egg could survive without first
coturnix. These are assumed to be depositions feedingonthehostegg.
6 AMERICAN MUSEUMNOVITATES NO. 3636
As reported elsewhere (Rozen and Kamel,
in press) eggs or young larvae of Sapyga
luteomaculata were occasionally encountered
in cells also occupied by immatures of
Coelioxys coturnix (fig. 8), indicating that
these two cleptoparasitic species are in com-
petition for the same host (although S.
luteomaculata also attacks Osmia submicans,
whichisnotattackedbyC.coturnix).Because
the first instar of S. luteomaculata is highly
active and substantially larger than the first
instarofCoelioxyscoturnix,onemightassume
S. luteomaculata would destroy the competi-
tor. We did encounter this situation, but we
also found a cell containing a mangled egg of
S. luteomaculata and an active third instar of
C.coturnix.WesurmisethatinthiscasetheC.
coturnixeggmighthavebeendepositedearlier
than that of S. luteomaculata.
Duration of the egg stage of Coelioxys
coturnix is estimated to be brief and is
certainly shorter than that of the host, since
all cleptoparasitic eggs on host eggs hatched
before the host embryo started to absorb the
surrounding amniotic fluid prior to hatching.
Although we were unable to identify newly
deposited eggs as such, the absence of older
immaturesofeithercleptoparasiteorhostand
the presence of numerous fresh eggs indicated
that the nesting season had just begun. In a
sample of 17 cells containing eggs of C.
coturnix monitored in the laboratory, all
hatched within three days of being collected.
We identified hatching by the appearance of
gas-filledtracheae,accompaniedbythevisible Figs. 9, 10. SEM micrographs of second instar
constriction between head and the rest of the (identified by its mandible, as in fig.20) of
Coelioxys coturnix. 9. The somewhat flaccid egg
body as well as by more or less visible body
of Megachile minutissima to which is attached the
segmentation (figs. 5, 8).
chorion and presumably first instar skin of C.
DEVELOPMENT: The first instar is shrouded coturnix. 10. Close-up of micropyle (identified by
byitschorionasitstartstofeedonthehostegg. rectangle in fig.9) matched with micropyle of
It remains motionless on the host for the next mature oocyte(Rozenand Kamel, 2007:fig. 33).
day or two (exact timing not determined, but
nomorethantwodays)duringwhichtimethe During this time the cleptoparasitic larva
hosteggfirstbecomesflaccid(figs. 5,8).Some gradually swells due to the ingestion of the
evidence suggeststhatshedding ofthechorion host yolk and subsequently the provisions. As
and first instar exuviae occurs while the host the larva feeds, the opaque, yellowish content
eggisonlypartlyingested(figs. 9,10).Thehost of its digestive tract indicates ingestion of
egg gradually flattens with a finely wrinkled pollen, and the larva continues to increase in
chorionandthenbecomesconcave,afterwhich size. While still a second and third instar, it
it flattens and floats as a dull film on the reacts to teasing with a probe by rearing its
provisions. After depleting the host egg, the head from under the surface of the provisions
second instar starts feeding on the provisions. andopeningandclosingitsmandibles.
2008 ROZENAND KAMEL: BEHAVIOR OFCOELIOXYS COTURNIX 7
Thisspecieshasfivelarvalinstars.Defecation While the egg-deposition and host-killing
commences at the beginning of the last larval behavior of this species of Coelioxys and
stadiumorshortlythereafterwhileconsiderable Radoszkowskiana rufiventris appear identical,
foodremainstobeeaten.Asmentionedabove, there is an anatomical difference between the
castlarvalskinsofpreviousinstarspresumably first instar of C. coturnix, as detailed in the
normallyaccumulateundertheposteriorendof ‘‘Descriptions of Larval Instars,’’ below, and
the feeding instar. In one case we collected a thatofR.rufiventris(RozenandKamel,2007).
fourth instar shedding to a fifth instar and all Although the mandibles of both species are
threepreviousskinsweresequentiallyflattened shortandstronglycurvedapically,theapicesof
onto its venter. Such a finding facilitates those of C. coturnix bend caudally whereas
determinationofinstarnumbers. thoseofR.rufiventrisquestionablycurveorally.
More significantly, both species exhibit a
DICUSSION AND CONCLUSIONS secondary mandibular projection that in both
caseswetentativelyhomologizewiththedorsal
BASED ON HOSPICIDAL BEHAVIOR
mandibular tooth of the typical, bidentate,
Clearly the eggs of Coelioxys coturnix are larvalmegachilidmandible.Thistooth,howev-
deposited as has been described by Ferton er, is structurally very different in these two
(1896) for the related C. afra, although the species: that of C. coturnix is long, tapering,
variationofpositionsofthecleptoparasiteegg apicallysimple,andstronglydivergingfromthe
relative to the host egg was greater than curved mandibular apex (figs. 13–15) and that
encompassed by his account based on only of R. rufiventris is short, inconspicuous, and
two sightings. Identical in the accounts of apically bears a cluster of long (relative to the
both species is the fact that parasite eggs are tooth) fixed spines (Rozen and Kamel, 2007:
deposited afterthose ofthe hosts, presumably figs.20,21).Itisdifficulttopostulateascenario
when the host female is gathering material to whereby these very different structures could
close the cell. In addition, his description of haveacommonfunctionalorigin.Unfortunately
the hatched larva of C. afra feeding on the the mandibles are tiny structures on very small
host egg, slowly reducing it to an empty larvae that are hidden beneath their egg chori-
chorion, is essentially identical to our obser- ons,sothatinvivoobservationsareimpossible.
vations. In both cases, after the host egg is Perhapsstudiesofrelatedspecieswillilluminate
eliminated,thecleptoparasiticlarvacommenc- theanatomyandfunctionofthesestructures.
es feeding on the provisions. If one accepts the hypothesis that Coelioxys
Thus,thesetwospeciesarenearlyidenticalin and Radoszkowskiana had a common clepto-
their hospicidal behavior, which is also shared parasitic origin, one then has to explain the
with Radoszkowskiana rufiventris (Rozen and origin of the second mode of parasitism within
Kamel, 2007). This behavior was possibly the cleptoparasitic clade, that is, what evolu-
derived from a common cleptoparasitic ances- tionary steps could account for a shift from a
tor of Coelioxys and Radoszkowskiana, and, situationinwhich(1)aparasiticeggisplacedon
therefore, supports the hypothesis that there a deposited host egg and the first instar of the
was a single origin of cleptoparasitism in the cleptoparasitekillsthehosteggtooneinwhich
Megachilini.However,unexplainedisthestudy (2)theparasiticeggishiddeninthehostcellasit
by Carre´ and Py (1981) on C. rufocaudata in is still being provisioned before the host egg is
which they identified the third instar as the depositedandthethird-instarcleptoparasitehas
principle hospicidal form and stated the clep- thecapabilityofkillingthehostlarva?3
toparasitic egg is inserted in the cell that was
still being provisioned. This species is presum- 3ThisquestionisbasedontheassumptionthatCoelioxys
is monophyletic. If it were discovered that
ablyacloserelativeofC.coturnixandC.afra,
Radoszkowskiana arose from within Coelioxys, then the
andwewouldhaveexpectedacloseagreement polarity of behavioral character state might change,
intheirbehavior.Wealsonotethattheirlarvae implyingthateggdepositionofthecleptoparasiteonthe
are illustrated as having hypostomal tubercles host egg was the derived condition. This seems unlikely
since it would involve a reversal of the specialized
(5 ‘‘pleurostomal thickenings’’), which are
anatomical features of third and presumably second
lackinginC.coturnix. instarstotheplesiomorphiccondition.
8 AMERICAN MUSEUMNOVITATES NO. 3636
Figs.11–15. SEMmicrographsoffirstlarvalinstarofCoelioxyscoturnix.11.Head,coveredbychorion,
bitingeggofMegachileminutissima,frontolateralview.12.Close-upoffrontofhead,showingmicropylar
sculpturing of chorion. 13. Head of larva, now removed from host egg, showing mouthparts, near lateral
view.14.Same,approximateventralview.15.Mouthparts,witheggchorionandlateralpartofparietalnow
removed, approximatefrontal view.
Atthispointwelackconcreteevidenceasto tential host bees do not have to depart from
how this might have happened, but we can the nest to gather closure material since they
speculate on the selection pressure that might canclosethecellswithmaterialonhand(such
account for this diversification in modes of as soil). Such potential hosts do not provide
cleptoparasitism in Coelioxys. First, we note evenanarrowwindowofopportunitytohave
that there is a very limited time period for a their completed cells visited by such clepto-
cleptoparasite to enter an open host cell: parasites as Radoszkowskiana, C. coturnix,
between when the female host has deposited and C. afra.4 It could be argued that one
her egg and when she returns to seal the cell. reason that Coelioxys with its more than 300
There is presumably an advantage if a
parasitic female can oviposit in an open cell
4ThesetwospeciesbelongtothesubgenusAllocoelioxys,
since such a cell is accessible for a longer time
as does C. echinata, the species presumably studied by
period thantheshort period betweenhostegg Carre´andPy(1981)asC.rufocaudata.Ifoneassumesthat
laying and cell closure (although there is Allocoelioxys is monophyletic, then either one can
conclude that the shift from one type of egg deposition
admittedly a disadvantage in terms of the
to the other took place in that clade or one becomes
threat of a returning host female detecting a
skepticalthatC.rufocaudataofCarre´andPyisasynonym
cleptoparasitic egg). Furthermore, many po- ofC.echinata.
2008 ROZENAND KAMEL: BEHAVIOR OFCOELIOXYS COTURNIX 9
Figs.16,17. SEMmicrographoflarvalinstarsofCoelioxyscoturnix.16.Secondinstarshowingskinof
firstinstar attachedto venter. 17.Close-up of first-instar mandible (identified byrectangle in fig.16).
species(Michener,2007)issosuccessfulisthat DESCRIPTIONS OF LARVAL INSTARS
it was able to expand its roster of potential OF COELIOXYS COTURNIX
host taxa because it evolved another mode of
cleptoparasitism that permitted it to attack Inthefollowingaccountscomparisonswith
hosts that sealed their cells immediately after CoelioxyssayiandC.octodentataarebasedon
the descriptions and illustrations of Baker
ovipositing.
(1971) and with C. decipiens on the paper by
There is a preexisting condition that might
Rozen and Kamel (2006).
be regarded as a step toward ability to attack
host larvae rather than host eggs, i.e., an
evolutionary step toward the presumed de- FIRST INSTAR
rived mode of cleptoparasitism in Coelioxys:
Figures 11–17
larvae of Coelioxys beyond the first stadium
tend to be combative when teased with a
Although many of the details of the
probe,moresothanmanynon-cleptoparasitic
anatomy of the first instar are unknown
larvae.Suchacombativebehaviormaybethe
becauseofitssmallsizeandchorion-shrouded
result of having to compete with other
body, it can be immediately distinguished
cleptoparasitic individuals particularly during
from subsequent instars by its mandible.
the early instars.5 We can envision a hypo-
This structure is strongly curved, fanglike,
thetical situation whereby a parasitic first
and subapically bears a long, slender, sharply
instar should have killed the host egg but
pointed, dorsal, pronglike process, which is
failed to do so for whatever reason. When it
moreorlessacontinuationofthelongaxisof
encounters the host larva later, it is pre-
thebaseofthemandible(figs. 14,15).Beyond
adapted to kill it. Thus, there is a shift in
the branching of the prong, the mandibular
function of its combative ability from killing
apex curves strongly, so that its extreme apex
competitors to killing the host (which is, of
is at a right angle to the long axis of the
course, also a competitor) at a later time.
mandibular base and, when both mandibles
are closed, their extreme apices are almost
5In support of this idea, the first instar of Exaerete
parallel(figs. 13,15).Theprongispresumably
smaragdina(Gue´rin-Me´neville)(Apidae)hascurved,sharply
the modified dorsal tooth of the typical
pointed mandibles although the cleptoparasitic female
normallykillsthehostoffspring(Garo´faloandRozen,2001). megachilid bidentate mandible. Its function
10 AMERICAN MUSEUMNOVITATES NO. 3636
is unknown: It may stabilize or make taut the same except two cast skins, IV-29-2007; same
chorion (either that covering the first instar, except one cast skin, IV-27-2007.
that of the host, or both) while the curved
point of the opposing mandible tries to INSTARS TWOTO FOUR
penetrate the chorion. Alternatively, its sharp
Figures 18–27
apexandthefactthatitsapexextendsbeyond
the curved mandibular apex suggest that it
mightbeatearingdevisetoperforatechorion. HEAD: The integument of the parietals of
the second instar of Coelioxys coturnix is
The conspicuous apical labral tubercles of
distinctly sclerotized but only moderately
subsequent instars (figs. 20, 22, 15) are not in
pigmented, and the mandibles are perhaps
evidence on the first instar (figs. 14–16). Cast
slightly more pigmented than the parietals.
skins do not reveal any pigmentation to the
The maxillary and labial sclerites are unpig-
cuticle,andtheirspiraclesweretoosmalltobe
mented and presumably nonsclerotized. The
detected.Parietalsoffirst-instarskinscollapse
head capsule, labrum, and mandibles exhibit
and internal head ridges cannot be detected
sensilla, some of which are setiform and
with a compound microscope, all suggesting
sometimes arise from small tubercles.
weak sclerotization, whereas parietals of
Spicules are entirely absent from the head.
subsequent instars are distinctly sclerotized
Theheadofthesecondinstarismoreorless
and do not collapse after shedding, and
hypognathous (fig. 18) as is the case for all
internal head ridges are quite evident. For
subsequentinstarsandalmostcertainlyforthe
that reason (and the fact that they are small)
first instar as well. The parietals of all instars
first instar skins can be easily overlooked
are not enlarged, and their posterior bound-
whereas head capsules of subsequent instars
aries are only slightly constricted, so that the
flag the presence of the body exuviae that
widthofeachforamenmagnumisonlyalittle
adhere to the preserved instar. In contrast to
smallerthanthemaximumheadwidth.Paired
the rest of the head, mandibular apices
hypostomaltuberclesasfoundinotherknown
including the dorsal prong are more heavily
Coelioxys larvae (Baker, 1971; Rozen and
sclerotized on cast skins of first instars and
Kamel,2006)aretotallyabsent.Sclerotization
consequently can often be identified with a
of the parietals ends ventrally at the hyposto-
compound microscope (figs. 16, 17). Maxillae
mal ridges, and thus does not invade the
of first instars are represented by low mounds
labiomaxillary area; sclerotization posteriorly
posterior and mesad of the mandibular bases
ends at the postoccipital ridge. The tentorium
and lack obvious palpi or sensilla, as revealed
is complete and thin in the second instar and
by SEM (figs. 14, 15). The labium (figs. 14, continues to be present in subsequent instars;
15) is a shallow, median, longitudinal trough by the fourth instar it has become moderately
separatingthemaxillaeandalsolacksobvious robust. The anterior and posterior tentorial
palpi and sensilla. pits are in the normal position and are
The dorsal mandibular prong is possibly moderate in size in all instars.
homologouswiththe‘‘dorsalspine’’identified The postoccipital ridge is pronounced but
byBaker(1971)onthemandiblesofCoelioxys narrow, whereas the hypostomal ridge is
sayiandC.octodentata,whicharedepictedas strongly developed and wide in all instars.
very short. These structures are tentatively Similarlythepleurostomalridgeismoderately
consideredhomologoustothedorsalmandib- developed, as is the epistomal ridge below
ular tooth found on subsequent instars of (laterad of) the anterior tentorial pits but is
these taxa as well as on Radoszkowskiana absent between the anterior pits. Parietal
rufiventris.Carre´ and Py(1981) also refer toa bands seemed absent in the first instar, but
‘‘e´pine dorsale’’ on the mandible of C. they appeared on SEM micrographs of the
echinata, but it is impossible to interpret from instars 2–4, as suggested by a depression on
their diagram the length of this structure. each parietal (figs. 18, 23, 27). The antennal
MATERIAL EXAMINED: One first instar projection (fig. 19) is weak (far less than one-
feeding on host egg: Egypt: Ismailia, Suez halfitspresumedbasaldiameter)inthesecond
Canal University, IV-30-2007 (J.G. Rozen); instar and lacks a distinct papilla and basal