A key to the puparia of 27 species of North American Protocalliphora hough (Diptera: Calliphoridae) from bird nests and two new puparial descriptions

39 Pages·2003·11.4 MB·

by  Terry L Whitworth

)
PROC. ENTOMOL.SOC.WASH.
105(4).2003.pp.995-1033
A KEY TO THE PUPARIA OF 27 SPECIES OF NORTH AMERICAN
PROTOCALLIPHORA HOUGH (DIPTERA: CALLIPHORIDAE) FROM BIRD
NESTS AND TWO NEW PUPARIAL DESCRIPTIONS
Terry L. Whitworth
Whitworth Pest Solutions Inc., 2533 Inter Ave., Puyallup. WA 98372. U.S.A. (e-mail:
[email protected]
—
Abstract. Keys are provided to the puparia of 27 species of North American Proto-
calliphora Hough (Diptera: Caliiphoridae) (bird nest blow flies) for which puparia are
known. Previously undescribed puparia are described fortwo species, P. hriinneisc/iicinui
Sabrosky, Bennett, and Whitworth and P. hesperia Shannon and Dobroscky, and the 25
remaining species are redescribed. Hosts, distribution, and habits are discussed for each,
A table ofbird hosts and associated bird blow fly parasite species is included.
Key Words: birdblowflies,birdhosts,birdparasites,Caliiphoridae,keys,Diptera.North
America. Protocalliplioni. puparia
Species of the genus Protocallipliora males, andpuparia. The key tosinglemales
Hough are obligate blood-sucking parasites is usually reliable for specimens in good
of nestling birds. They are rarely collected condition, but the key to single females is
using conventional insect collecting tech- reliable for only about 10 species. Keys to
niques, most are found only in bird nests. thirdinstarlarvaewereprovidedfor 16spe-
Thetaxonomyofthisgenusin NorthAmer- cies and to puparia for 22 species. Third
icawaspoorly understooduntil Sabroskyet instarlarvae are not included in the present
al. (1989)redescribedthe 11 known species study, because, when larvae are available,
and described 15 new species. Their work they shouldbeallowedtopupateandadults
also included a detailed review ofprevious emerge. This provides both adults and pu-
taxonomic and biological studies on Pro- paria for identification. Some species are
tocalliplioru. bestidentifiedbypuparia,whileothershave
Bennett and Whitworth, co-authors with distinctiveadults. Nestscollectedmorethan
Sabrosky, subsequently published three ar- 10 days or so after young fledge have only
ticles which elaborated further on the life empty puparia and this is the form ofPro-
history, ecological relationships, and path- tocalliphora most frequently collected.
ogenicity of Protocalliphora (Bennett and Bennett (1957) conducted pioneering re-
Whitworth I99I, 1992; Whitworth and searchontheidentificationofProtocallipho-
Bennett 1992). Whitworth (2002, 2003) re- ra puparia. He identified numerous pupaiial
cently described three new species ofPro- features, which could be used to separate
toccilliphora. bringing the total number of species,anddevelopedtechniquestoprepare
species known in North America to 29. puparia for identification. His efforts were
Sabroskyetal. (1989) alsoprovidedsev- included in Sabro.sky et al. (1989), but there
eral keys, the most useful being based on was little opportunity to test his keys prior
reared material with matched males, fe- topublication. Subsequently. 1 haveencoun-
PROCEEDINGSOFTHEENTOMOLOGICALSOCIETYOFWASHINGTON
tered a variety of problems with them. Al- puparial key is unreliable, the cunent study
though photos ofeach species were provid- wasinitiatedtodevelopamoreeffectivekey
ed, many were of poor qiiahty and of httle to the puparia ofNorth American Protaccd-
value in support ofthe key. No other illus- liphora.
trations for immatures were included and,
Materialsand Methods
without them, interpretation of some ofthe
terminology is confusing. The puparial key When I began studying this genus, I per-
relies heavily on the length of prothoracic sonally collected bird nests in Utah, Idaho,
fringespines,asmeasuredinlarvae.Butthis and Wyoming (Whitworth, 1977). Some
characterisuselessforpupariasincethepro- were easily found, like the colonial nests of
thoracic region is inverted during pupation most swallow species, and the conspicuous
making the measurement of individual nests of magpies and robins. For birds with
spines impossible. For this character to be nests that were difficult to locate, I enlisted
used, third instarlarvaewouldalsobe need- the help ofornithologists who where study-
ed. Bennett's puparial key is fairly effective ing birds such as raptors, chickadees, small
forspecimensofthe 10orsospecies,which spaiTows, warblers, and vireos. More re-
occur in southeastern Canada where his cently, I have been able to acquire many
Ph.D.studieswereconductedbutIfoundthe nests from nest boxes via Internet contacts
characters variable and unreliable for the with birders who send me nests once nest-
same species in other areas. Descriptionsof lings fledge. Most contributors were con-
puparia for 13 species were based on spec- tactedwiththehelpoftheCornellBirdhouse
imens collected from only one geographic Network, which made it possible to obtain
area and the 9 remaining puparial descrip- nests from throughout North America.
tions were based on specimens from only 2 Nests were examined, puparia removed
or 3 areas. For many species, puparia were and counted, and ifstill viable, adults were
simply not available from otherareas at the reared. Unemerged puparia were either vi-
timekeysweredeveloped.WhenIbeganthe able, parasitized or rarely dead. Dead pu-
current study, Bennett was deceased, thus paria were lighter weight, adults emerged
making problems encountered in the keys from viable puparia within about 10 days,
more difhcult to resolve. One complication while in parasitized puparia, wasps
was that Bennett did not clearly identify emergedfromdays tomonths later Puparia
specimens ofpuparia used to write descrip- were sometimes loosely scattered through
tions, so it was difhcult to verify features. nests (P. brcnieri (Hendel)), some were
Ultimately,Iobtainedabout200ofhisslides wrapped in dirt or hair cocoons {P. sialia
from the National Museum of Natural His- Shannon and Dobroscky and P. pororwn
tory, Smithsonian Institution, Washington, Sabrosky, Bennett, and Whitworth) or bur-
D.C. and about 100 slides from the Memo- ied in dried mud (P. hirimdo Shannon and
rial University of Newfoundland. Most Dobroscky). If viable puparia were avail-
slides contained only fragmentary data, able, some were sorted into individual vials
many were identified by species names that so adults and puparia could be matched if
were neverused and no synonymywasever mixed infestations or unusual species were
provided. Fortunately, I was able to recon- suspected.
struct data for most of his slides and inte- Many species were readily identified
grate his material with mineforthisstudy. I from empty puparia; some were so distinc-
determined his measurements and descrip- tive that they could be determined with a
tions were accuratebasedonthe material he darkfield microscope (e.g., P. sialia and P.
had, thus I have let his puparialdescriptions hraiteri). Ifidentification could not be con-
stand. Because ProtocalUphora are readily firmed with this method, slides were made.
collectedasemptypuparia,andtheavailable If possible, only fully developed puparia
VOLUME 105, NUMBER4
were selected for slides, becausecharacters Bennett and Whitworth's early studies, as
in undersized puparia are usually distorted well as the collections ofother researchers
and they may not key properly. Infested prior to 1992. Since 1992, a total of4.077
nests usually included mature puparia, but nests of79 bird species were examined by
if nestlings fledged or died before some the author. Of these, 41% (1,691) from 52
third instar larvae matured, undersized bird species were infested with 20 species
specimens resulted. Slides were prepared ofProtocalliphora (Table 1).
by heating puparia for several minutes in Since this study began in 1992, no new
10% potassium hydroxide solution in awa- material has been acquired for P. avium
terbath to soften and clean them, then they Shannon and Dobroscky, P. bicolorSabros-
were rinsed in distilled water. Specimens ky, Bennett, and Whitworth, P. rognesi
over-heatedorleftinsolutiontoolongwere Thompson and Pont (previously P. duysor-
overcleared, andthisdestroyedspinesmak- rltoea (Meigen)), P. fallisi Sabrosky, Ben-
ing specimens difficult to key, especially nett, Whitworth, P. Iiesperioides Sabrosky,
those with slenderspines. Optimumheating Bennett, and Whitworth, P. seminucla. Sa-
times varied with the thickness and sclero- brosky, Bennett, and Whitworth, or P. ritii-
tization of the puparia. Softened puparia clrae Sabrosky, Bennett,andWhitworth. Im-
were sectioned with microscissors intodor- matures for P. beameri Sabrosky, Bennett,
sum, venter, stigmatal area, prothoracic and Whitworth and P. sapphira Hall, have
fringe, and the cephalopharyngeal mecha- never been collected. For P. avium, P. Iii-
nism was removed and mounted. The sec- color. P.fallisi, P. hesperioide.'i, and P. tun-
tions were then cleared in specimen clear- drae I relied on Bennett's slides for key
ing fluid for 1-3 days, rinsed in 95% and characters. I was also able to get a few pu-
then 100% ethanol, thendriedandmounted parial specimens of each of these species
in Euparal. Once slideswere prepared,they from seriesofadults in museums. 1 prepared
weredried in aconvectionovenat65°C for slidesofthesepupariaand verifiedthat Ben-
10-14 days. Proper drying was important, nett'sslidesmatchedthespecies,sincemany
because, ifthe medium was not dry, spec- of his slides did not have correct species
imens tended to drift to the edges ofslides names. For P. rognesi and P. semiiuida I
in thethickmedium. Slidesofpupariawere was able to re-examine specimens retained
examined with a compound microscope at from my study conducted between 1969-
upto400X. Measurementswere madewith 1975 (Whitworth 1977). A total of about
a micrometer installed in the ocular lens, 4,150 slides were prepared forall 27species
calibrated to microns. ft)r which puparia were available.
Sabrosky et al. (1989) is cited regularly Most puparial characters used here are
throughout this work and is the only Sa- defined in Sabrosky et al. (1989) where a
brosky reference cited. Hereafter any ref- glossary of terms is provided. Sketches of
erence to Sabrosky refers toSabrosky et al. importantcharactersareincludedheresince
(1989). References to Bennett are G. F. they were lacking in Sabrosky. Puparia of
Bennett and references to Whitworth are Protocalliphorahaveavarietyofcharacters
the author. which are useful fordistinguishing species.
Over 15.000 puparia from approximately The most important are found in the stig-
3,000 infested bird nests of99 bird species matal area (Fig. 1) and on the venter (Figs.
were examined forthis study. Material was 8-9) and dorsum. The cuticle ofmost spe-
studied from 46 ofthe 48 contiguous Unit- ciesisthicklycoveredwithspinesandoften
ed States (Protocalliphora has not been has folds or ridges.
lound in Florida and Louisiana), Alaska, Spines on puparia are extensions of the
throughout Canada, and Greenland. About cuticleandmostarereclinate,whichappears
half of the material examined was from to help larvae maintain their position in the
PROCEEDINGSOFTHEENTOMOLOGICALSOCIETYOFWASHINGTON
V
K
•^ ^ i ' . ^o«
1
Fig. L Diagrammaticviewofstigmatalarea, but = button;csf= circumstigmatalfolds;dsp = diameterof
stigmata! plate; hyo = hypostigmatal region; hyr = hyperstigmatal region; irr = irregular folds; Icp = lower
cuticularplaques; mes = mesostigmatal region;per = pcritrcme;stp = stigmatalplate;tub = tubercles;ucp =
uppercuticularplaques; wsa = widthofstigmatalareaal level ofthebuttons(lineisdrawnbelowihebuttons
toreduceclutter).
ne.st, especially when feeding on nestlings measured. The longestspinesonthedorsum
(Fig. 2a). Some spines are upright and ap- are usually nearthe centerofeach .segment.
pear in profile (Fig. 2b). while some, espe- Exceptionally long, aberrant spineswerenot
cially in the stigmatal area, are proclinate included. All spine measurements were
(Fig. 2c). Most spines are translucent and made at 4()0X and spines were classified as
appear2-piirt,composedofaspinebaseand long,medium, short,reducedtotubercles,or
the spine, with spines in profile, the base is absent(Figs. 3-7). Spinesalsovary inthick-
notvisible. In most species, somespinesare ness and are mediumorslender(Figs.4-5).
reduced totubercles, whichisthespinebase The stigmatal region is divided into the
with no spine projection (Fig. 7). Spine hyperstigmatal, mesostigmatal, hypostig-
length is an important character (see Fig. 2 matal, and is bounded by circumstigmatal
for how to measure: measurements vary folds (Fig. 1). Spines in the lower hyper-
with orientation ofthe spine). Spine lengths stigmatal areaareshorterwhilethoseabove
given in Sabrosky were averages ofseveral are longer. Spines in the upper mesostig-
spines ineach area. I found averagestended matal area are often reduced to tubercles
toobscuredifferencesbetweenspecies,soin with longerspines below. Spines in theup-
this work the longest spines in an area were per hypostigmatal area are shorter, while
VOLUME 10?. NUMBER4
©®©0
A /\ /-. /x /x
Figs. 2-7. Puparial spines. 2. How u sure: (a) reclinale;(h) profile; (elproeMiiate; (d)measurementol
spinelength. 3.Longspines.4. Medium width. .';. Slenderspine width.6,Shortspines. 7,Tubereles.All
examplesofFigs. 3-7.450X.
PROCEEDINGSOFTHEENTOMOLOGICALSOCIETYOFWASHINGTON
those below are longer. The stigmatal re- acter is useful when present, but is variable
gion may have pronounced folds (Fig. 21a, within species. Protocalliphorahalliexhib-
P. aenea Shannon and Dobroscky), mod- its the full range of variation from no re-
erate folds (Fig. 22a, P. asiovoru Shannon duction in the posteriorband in some spec-
and Dobroscky), faint folds (P. halli Sa- imens, to extreme reduction in others. Ifin
brosky, Bennett, and Whitwoilh) or folds doubt, measure the ventral band ratio in an
absent (Figs. 25a, 26a. P. interriipta Sa- anterior and posterior segment to verify if
brosky, Bennett, and Whitworth, P. metcil- reduction is occurring.
licaTownsend). Bennettusedthetermfolds The ventral band ratio is an important
for the stigmatal area and ridges for the species character but can be difficult to
venter and dorsum, folds were considered measure properly. This ratio is determined
largerthan ridges. Thisterminology iscon- by measuring the sum of band widths of
tinued here for consistency, although some ventral bands and dividing it by the total
species have very large ridges and others distance between margins of ventral pads
have smaller folds. (Figs. 8-9, see Sabrosky, for details). Nor-
Ridges of the dorsal and ventral cuticle mally, bands should be measured in the
may be pronounced (Fig. 21c, P. aenea), center of each segment. In some species,
moderate(P.paronon).faintorabsent(Fig. the medial bandisreducedordividedinthe
25b, P. interriipta). This characteris some- middle where band width is usually mea-
what variable, but with practicecan be use- sured (Fig. lOe. 22b, P. asiovora. Fig. IOf,
fulfordistinguishingsomespecies. Insome P. interriipta). When this condition wasen-
species with broad ridges (P. hirimdo, P. countered. 1 measured band width to one
lata Sabrosky. Bennett, and Whitworth), side of the gap. When measuring band
ridge width isa useful character.Theventer widths, 1 assumed there was no space be-
normally has 3 distinct spine bands, thean- tween the rearoftheposteriorbandandthe
terior, medial, and posterior bands on each adjacent ventral pad. Rarely, a distinct gap
segment, bounded by ventral pads (Figs. 8- is present, if so, the actual band width is
9). On each segment the anterior band measured. Bands may be broad which pro-
varies little between species, while the me- duces a high ratio (Fig. 11, 29d, P. .spatu-
dial band may be regular (Fig. 10a, P. sia- lata Sabrosky, Bennett, and Whitworth), to
lia), thinned in the center with opposing narrow with a low ratio (Fig. 12. P. halli).
spines (Fig. lOb. P. halli). irregular and Bennett (in Sabrosky) advised ignoring
thinned in the center (Fig. 10c, P. ciiprina, small spines and tubercles when measuring
[Hall]), thinned in centernot irregular(Fig. bands,and Iconcur. However,somespecies
lOd, P. hennetti Whitworth) interrupted like P. paronim (Fig. 13. 27b) and P. hen-
(Figs. lOe, 22b, P. asiovora), or center re- netti have medial and anteriorbands witha
duced to tubercles (Fig. lOf, P. interriipta). broad row oftiny spines to the rear ofthe
In species with reduction in the medial main band. When this condition was en-
band, reduction usually progresses toward ciiuntered, I includedthe small spinesinthe
the rear. The posterior band is sometimes measurement. Finally, when puparia are
reduced or absent, especially to the rear heavily ridged as in P. hiriinda and P. rii-
(Figs. 14a, b, P. halli). This condition is gosa Whitworth, bands can be so distorted
also present in P. aenea. P. fallisi, and P. that they are very difficult to measure
timdrae. Because of this reduction, ventral (Whitworth 2002). It may be necessary to
band ratio measurements will generally be measure several specimens to get an accu-
lower to the rear in those species. In some rate measurement of ventral band ratio in
species, the posterior band is reduced these species.
steadily tothe rear, in othersreductiondoes The prothoracic fringe is a band of long
not occur until the last sesment. This char- spineson the anteriormargin ofthe protho-
VOLUME 105.NUMBER4
meb
Figs. 8-9. 8. Diagrammatic viewofventer,prf= prothoracic fringe;emc = emergencecap;an = anus;
= anal tubercle. 9. Expanded view ofsegment nnniber 7. anb = anterior band; nieb = medial band; pob
posteriorband;vep = ventralpad.
lacic segment of larvae and puparia. This mens, it was determined that when Bennett
character is unique to most of the genus made this measurement he did not stop at
Protocalliphora (Figs. 8, 15). although this the outer margins of the plates (as defined
character is absent in pupariaofP. hraiieri. in thetext), butextended it tothefull width
It isofminimal valuefordistinguishingpu- ofthe stigmatal area, roughly delineated by
paria of most species, which have an aver- the circumstigmatal folds. Rather than re-
age total diameter ofabout 350 [jl, but it is measureeverythingtoconformwiththedef-
useful for identifying P. sialia and P. oc- inition provided in Sabrosky, 1 have rede-
cideiitalis. which have exceptionally long fined this measurement as the width ofthe
fringe (500-800 fx) (Fig. 15b). Protocalli- stigmatal area, at the level of the buttons
phora interrupta has an unusually short (Fig. 1). Anotherproblem was encountered
fringe, which averages 225 |jl (200-250 jjl), tneasuring the diameter of the stigmatal
whileP.paroruin hasalongerthan average plate. This measurement is defined in Sa-
fringeof425 (x(400-450 jjl). Anotherchar- broskyasextendingfrom thetopoftheper-
acterthat was studied was the cephalophar- itreme throughthe ventral slittothebottom
yngeal mechanism. Unfortunately,itproved ofthe button (Fig. 1). However, McAlpine
variable within species and was often dis- et al. (1981) define the stigmatal plate as
ttirted when mounted on a slide. Ifa better bounded by the peritreme and technically
methodcan befoundtoprepareitforstudy, the full diameter ofthe plate would extend
it may prove to have useful characters. past the button to the bottom ofthe peritre-
Problems were encountered calculating me. Again, rather than remeasure every-
ihe distance across the stigmatal plates at thing, the measurement, as defined in Sa-
ihe level ofthe buttons as explained in Sa- brosky, is used forall measurements in this
brosky. After measuring numerous speci- study.
1002 PROCEEDINGSOFTHEENTOMOLOGICALSOCIETYOFWASHINGTON
Bennett included a variety of puparial deeply incised. Calliphorid puparia have
measurements, such asthediameterofstig- posterior spiracles exposed at the apex of
matal plates, stigmatal ratio, distance be- the terminal abdominal segment, and the
tween buttons, and width across stigmatal dorsal cornu is not incised. Puparia of the
plates (Fig. 1). 1 have included these mea- subgenus ProtocaUiphora are distinguished
surements in my descriptions, becausethey by the presence ofa prothoracic fringe and
help characterize species. However, they three distinct ventral spine bands (Figs. 8-
have proven to be oflittlevalue inthekeys 9). Larvae ofthe subgenus Trypocalliphora
and vary primarily with the size ofthe pu- lackaprothoracic fringe,the ventral medial
paria. band is absent, and the ventral anteriorand
posterior bands are weak or absent. Most
Results
scavenger calliphorid species have strong
I have identified 18 new bird hosts and ventral anterior spine bands, or bands of
90 new host-parasite relationships sincethe spines associatedwithintersegmentalareas.
publication of Sabrosky (Table 1). Thirty- The folk)wing key separates 27 species
six of the host-parasite relationships were of ProtocaUiphora puparia. Some species
from material 1 collected, the remaining 54 are still poorly known, and key characters
relationships were from other researcher's selected for them may be variable, making
studies, and most were confirmed from ma- keying difficult. Species with puparia un-
terial sent to me for identification. known and not included in the key are P.
To aid species identification. I have pre- heaitieri Sabrosky. Bennett, and Whitworth
pared alistof 160 infested bird speciesand and P. sapphira (Hall).
the species ofProtocaUiphora known from
their nests (Table 1). New relationships Key to PuPpraortioacoafllNiophrotrhaAmerican
from otherstudiesare identifiedby citation,
ifpublished, orifunpublishedthe research- 1. Dorsal ciiticular spines very sparse; \ciitral
er's name and affiliation are given. This ta- amnetdeirailorsapinndepboasntedrsioarbssepnitnefrboamndasllrseedgumceendtso,r
ble combines data from Sabrosky where absent to rear: prothoracic fringe absent;
bird hosts were listed by ProtocaUiphora spinesinallregionslessthan 10p.;obligatory
species. When using puparial keys, it isim- subcutaneousnestlingparasite.Proioccillipho-
portant to check known host-parasite rela- rci(Ti-ypocalliphora)(onespeciesinthissub-
tionships, new relationships identified from - gDeonrusasl) cuticular spines numerous; three dibsr-aueri
puparia alone should be determined with tinct ventral spinebandson.atleast,anterior
caution. Puparia of similar species can be segments (Figs. 8-9); distinct fringe on the
difficult to distinguish, but when hosts and anteriorendoftheprothoracicsegment(Figs.
species range are considered, distinctions S. 15a.b);pupariacoveredwithspines,rang-
may be made with confidence. (iFnigg.fr6)o.mortulbeorncglesspin(Feisg.(Fi7g).t3o).shsopritnesspminaeys
Most fly pupae found in bird nests in be medium (Fig. 4). orslender(Fig. 5); not
North America are ProtocaUiphora. Occa- normally subcutaneous. Protocalliphora
sionally, sarcophagids or other genera of (Protocalliphora) (28 North American spe-
calliphorids are found in nests, usually as- cies in this subgenus, puparia known for 27
msoocrieatecdomwimtohncairnriotnh.eTnheestsseolfatthearwtkasxaaanrde 2. Cslepeaenscttieerss)oomfemesdeigamlensptisne(Fbiagsn.dilnOte.err2u2pbt)e.dionntera-t 2
owls, which feeddead animals to nestlings. ruption usually narrow and may be incom-
They also may be found in nests where plete orwith no interruption in a few speci-
nestlings have died. Sarcophagid puparia mens in a series; hyperstigmatal spines usu-
may be distinguished by having posterior aflollyds25mo|id,eorraltees;s,raidfgeewstoof.3d0o(rjl:sumemsoasnldigvmeanttaelr
spiraclesindeepcavitiesandthedorsalcor- fainttoabsent;ventralbandratio0.63(0.57-
nu of the cephalopharyngeal mechanism 0,68/10)(usuallyinopennestsoflargerbirds
VOLUME 105. NUMBER4
ik ^
^ = ^
.£ - ; ^ s?,;:
.2 '5; ~ 5 .2 'c St 5i; ^ •-. :3
Ci.j:i-a-i3 :i,:: - ::
-5
II III
4J "5 '^ •= £ i S! 2 I
^•= 1-1 J5 iI ^S £u a§.
PROCEEDINGSOF-THEENTOMOLOCilCAI,SOCIETYOFWASHINGTON
^ ^ ^
a 5r c .= ^ -i .= ^ S a 3
a a a c S-.2 ii t3 S. 5 i; = ? -ii 2 5 .2 aaaaoaac
•S