J . E:>;TO.\IOL. Soc. BnI T CO I.L ,\IBIA 80 (1983). DI :C. 3 1. 198.3 2.5

TETRASTICHUS GALACTOPUS (HYM. :EULOPHIDAE), A HYPERPARASITE OF APANTELES RUBECULA AND APANTELES GLOMERATUS (HYM.:) IN NORTH AMERICA VINCENT C. NEALIS Institute of Animal Hesourcc Ecolog\' and Dcpartment of Plant Scil'nce. Un h'ersil\' of British Colu mbia Vancou\·er. British Coll',mbia 207,5 Wesbrook Mall. VancoU\"L'r. Fl .c:.

ABSTHACT Thc biolo;,,,' of Tetrastic/lIIs galactopus. a h\'perparasitc of i\palltelcs rubccula and A. glomeratlls in No rth Ameri ca, is reviewed. Thc female hvperpanlsitc at­ tacks its hosts while they' are larvae in their priman' , PierL~ rapac. although free-living cocoons of A. glomeratlls may also be attacked. In Vancouver. \\'he re A. rubenda is the onl\' available host, T . galaetoplioS is active from Juh' through Septcmber and probabh' overwinters as a pupa or adult within the host cocoon. The signifi cance of 11\"(Jerpa rasitislll to thc success of biological control efforts us ing Apanteles is discussed.

INTRODUCTION kn own if T. galartopus is also in the Okanagan. Tetrastie hus g lac top1ls (Hatz burg) is a This paper reports fi eld and laboratory data and gregarious eulophid Il\'perparasite of braconid la r­ reviews the biology of T. gaiactopus. . vae. In Europe, it has been commonly reared from MATERIALS AND METHODS Apallteles giomeratlls (L.) parasitizing Pi eris brassicae (L.), the large cabbage white. It is a true Field collections made during 1981-82 \\'ere from Il\-perparasite, depositing several eggs through the two sites in thc Vancouver area. One was a co­ primarY host directh' into the larval stagc of its own operative garden plot allotment near the Fraser host (Pi card 1921). Ferriere and Faure (1925) River in Burnab\' (BBY), which had been one of observed oviposition through newh' spun cocoons of Wilkinson's (1966) original sites: the other site was A. glomerat1ls but thought a different species of an isolated research plot of less tban 100 plants. on hyperparasite was im·oh ·ed. This dcw. although the Plant Science Field Station at the University of not supported I}\" ' morphological e\'idenee (Delucchi British Columbia (U FlC). From both sites in 1981 1950). has contributed to taxonomic confusions: and at BBY in 1982. P. rapae lan'ae were brought Tetrastichtls rapo vValker is the most common to the laboratory. separated by' instar and reared on svnonml in the literature (Krombien et al. 1979). potted kal e. If Apanteles emerged from the cater­ Pi card (1921 ). Gautier and Flonnamour (1924 ) and pillars, the cocoons \\'ere weighed and kept in­ Richards (1940) reported hq1erparas itism by' T. dividually in gelatin caps at 22 °C and a 16L:8D galactoptlS of Apanteles rubecliia Marshall. a photoperiod. Apanteles cocoons collected in the solitan' parasite of the imported cabbageworm , fi eld werc treated similarh-. In 1982 A. mhenda PierLv rapae (L .). Both A ruhecula and A . reared at UBC for diapau;e studies were an addi­ glomerattls attack earh- instar P. rapal' lar\";lc. tional data source. These priman' parasites \\'ere emerge fr om the fourth and fifth insta r, respccti\'e­ allowed to emerge from the host cate rpillar and Iv, and spin a pupal cocoon . The form er parasite spin a cocoon in the fi eld, then coll ected and held at normally lays one egg to producc a single lan'a: the 22 °C. and a 16L:8D photoperi od. T . galaetopus latter la\'s thirty· to sixty· eggs at a time in each host. that emerged from these cocoons were sexed and T. galae/opus must ha\'e entered ;'\orth Amcrica counted . This technique measured the density and with A. glomera/us \\'hich has been wide;\' sex ratio of T. galac/opus per A. mhecula cocoon distributed for biocontrol of P. rapac. In Britisil and permitted estimates of rates accor­ Columbia, T. gaiactopus attacks A. m bccula ding to the age of the prim an' host. through the (Wilkinson 1966). Wbere releases of A. mbecula season. Adult T. ga iactopus live several weeks at low have been made in areas formerh' inhabited bv A . glomeratus only. local T. galacto'pus para s iti z~ the temperatures if water and honey are avail a bl e. 1 progeny of the released A. miJecula (Parker et al. kept adults in stvrofoam cup-cages and exposed A. 197 1). rubecllia and A. glomerattls to them as cocoons and at \'arious stages witbin their host lan·ae. I was thus During 198 1-82, 1 made several collections of 1'. able to observe the oviposition beha\'iour of T. galactoptlS from A . rubecuia in the 10\\'er mainland gaiactopus. I also exposed non-parasitized cab­ of British Columbia and established colonies using bageworms to T . gaiactopus as well as final instar A both A. rllbeCll la and A. glomeratus stocks. A. r1lb ecula that had experienced a pre-treatment that glomeratus is availablc in the Okanagan Valle\' but would induce diapause i.e. less than 14 h it has not been collected around Vancoll\·er. I t is not photophase. Some Apallteles were exposed to un- 26 J. EI\Tmlol.. Soc. 811IT COIlJ\IH1A SO (lQS3), DE C. 3 1. 19S3

TABLE 1. "umber a nd pe r cent parasitism of Apantelcs rubcclIla b,' Tctrastichlls galactoplls according to the stage in w hich the prim ary host (Pieris rapac) was collec.:t ecl. Data pooled fr om all collecti ons I3I3Y , 1981 anti 1982.

HOST STAGE COLLECTED PARASITES

Apante1es rubecu1a Tetrastichus ga1actopus (%)

III 124 9 ( 7 . 2)

IV 352 132 (37. 5)

cocoons 94 37 (39.3)

mated female T. galac/opus to determine the sex of The number of 1'. galac/opus emerging from one haploid progeny. Attacked lan'ae were reared in­ host cocoon va ri es widely. More emerge from A. dividuallv on plants or. in cases where I intended whecula cocoons (10.6 ± 0.89 hyperparasites per onlv to confirm oviposition, were uissected cocoon: range 1- 21) than from the small er cocoons lIndersaline. of A. glu l1l ero/ns (4.3 ± 0.52 ll\verparasites per co­ coon: range 2-7). The hi ghest hyperparasite den­ sities may be due to supe rparasitism as morc than RESULTS AND DISC USS ION o ne r . goloc/opus is often seen on a single primar,' host in the fi eld. The data relating the densitv of T . M,' observa tions confirm earlier studies that T . galac/oplls to the weight of A mhecilio sho\\' that gala;;/opus a ttacks both A. rtlheCli la and A. host size does not significantly innucnce parasit e glomera/us wilile they are inside the primar,' cab­ densit v (r = 0.142: df = 52). Rather. a hi gh h vper­ bageworm hos t. Although oviposition is normal'" pa rasite densit,· per host leads to a small er ave rage directl,' into the primary parasit e, a few eggs \\'e re size as has been shown for other gregarious parasites found in the caterpill ar's body cavity. It is unlikel,' (Bouletreau 197 1). that these eggs can develop a nd eventuallv enter the Mature T. golor/oplls larvae bite emergence holes appropria te host (Richa rds 1( 40 ) . Picard (H)21 ) through the host body wall but remain within the described T . galac/opus a ttacking non-paras itiscd host cocoon to pupate. Adults emerge over a pro­ P. rapae but eggs were never found in the bod\' tracted period . through o nc to several holes in the cavity. I observed T . galac/opus inserting their hos t cocoon. ,Vhat appears to be a strong posith'c ovipositors through the bod y wall of several non­ phototaxis res ults in rapid dispersal of these adults. parasitised P. ropae but o nly once were eggs found 1'. galac/oplls is arrhenotokous: unmated females in the dissected caterpilla rs. O "iposition must re­ produced on'" male progenc,·. Most field coll ected quire a further stimulus provided onh ' b, the parasitized A mhectlla vielded both sexes of adult T. presence of a prima ry parasit e. galac/oplls: onl y a smail proportion were all female Most parasitism of A. rtlhecula Iw T. gala(' /opus (10.5 %) or all male (6 .6 % ). ~ eve rthcl ess, the sex occurs when the cabbage\\'o rm is in the fou rth in­ ratio in the collections aft er August was always star, that is. when A. rtlhecula is elose to emergence skewed in favour of females a nd varied through the (Table I). In laboraton' trials. A. rtlhr' cilla . one­ remainder of the season (Figure I a). Richards q uarter and midway through the total parasitic (1940) also found a preponde;:ance of female 1'. period, were ex posed to T. galoc/opus. The res ults golac/op!IS in field samples. showed that successful parasitism of A. rtlhecli/a W hen A. mbectlla were reared under fi eld or was unlikel \' before the second instar and in most labora ton ' conditions that normalh' induced cases not until a few days before emergence. I have diapause 'and were used as hosts of T. goloc/o p us. never succeeded in obtaining pa rasitism of A the ll\-pe rpa rasit e developed continuous" '. It is not ruhecilia after the la rva has emergcd fr om the known if there is a true d iapause in 1'. goiac/opiis priman' host a nd spun a cocoon. T. galoc/oplls but if so, it seems from these obscryations that it is walks over A. wben i/a cocoons but does not independent of the host's response to em 'ironmental oviposit. The silk llla" be too dense to permit inser­ conditions. tion of the ovipositor. In comparison. T. galoc/opus parasitizes A. glom era/Its either through the In Europe. 1'. golo c/oplls is widel\' d istributed primary host or after the free-lh'ing cocoon is form­ over the range of A. glo /n eratlls. parasitizing o,'er ed but before pupation of the primary parasite. All 50 % of the avail able la rvae at some times of the individuals in a cluster are not necessarily a ttacked. year (Mook a nd Haeck 196.5 : Ri chards 1940). The re J. E:->TmIOI.. So c. BHIT. COl.{ ' ~ I H I A 80 ( 1983) . D EC, 31. 1983 27

90 a. (/) W -: 80 -l + <>: U ~ 70 W ltl LL * + en 60

* 50

40 b. ~ (f) 30 • BBY r-- [J UBC (f) « IT 20 « 0..

0;:,R, 10

0 ~

May J une J uly Au g S ept O ct

T. ga l ac topus C . A. r ubecula

P . rapae

Fig. 1. Phenology of Tetrastichus galactopus at two locat ions in British Colu mbia during 1982 (BEY. Burnab\: U BC ·U ni \"t~ rs it' · of British Colu mbia). a) Pe r ce nt female T .galactopus at EEY . b) Per cent parasitism of A. rubccula (ex IV·instar P .rapac + cocoons on"') b,' T .galactopus a t BEY a nd UBC. e) Seasonal act i"it,' schedule for adult P.ra pae. A.ruhecula and T.galactopus in the Vancou" er a rea. a re a fe\\' estimates for A. rtliJeclila from :\o rth consistent \\'ith 1'. galartoptls find ing the isolated America . \Vhen 1\. I'IIhl'(,lIla was released in cohorts a t UBC: but the evidence is circumsta ntial. Missou ri , h"perparasitism b,' T. galactuptts rangerl The occurence of T. [!, alac/optls in the earliest col· from 36 .6 °{, to 72.~ '7c (Parker et al. 1( 71 ). At BB Y. lections a t BBY make it a rguable that the h",)cr. h'-perparasitism of A. rtliJrclila reached 62 '''< in parasites a re highh' synchroni zed \\'ith the first 198 1 and 4 1 '7c in HlIl2. Comparable len ,ls wcre generation of the p rima n ' parasite a nd that the ap· obser\'ed at UBC in 1982. Except for the relati" e'" parent ti me lag is due to pre" ious local ex tinctio ns in late start of the UBC population. th e same seasonal that area. pattern \\'as e" ident at both stue'" sit es (Fi g I b). It is d ifficult to ascerta in the effects of h'per· Parasites often lag behind their hosts in spring ap· parasitism on populations of either A. glomeratlls or pea rance (compare P. rapac a nd A, miJrclila in A. rtlbectlla. Blunck (19.57) states that fl\ per. Figure Ie). In the case of T . ga iactoplis. the lag mm' parasites in Germam' "diminish the useful effect of be due to a sustained diapausl' throllgh the sp rin g or A. glumerattls" but offers no d ata. Parker ct al. a high \\'inter mort al it,· and perhaps frequent local (197 1) d id not thi nk the "sizeable loss of A. rtliJc(,t tia extinction \\'ith subsequent slo\\' recolonization of to l'l"perparasites th rougho ll t the scason" affected Its the sample areas ..\1 00k a nd I-I aeck (196.5 ) thought role in suppress ion of P. rap(/c populations. But it is dispersal of T. gaiactoplis was rapid . an impression true that A. rtliJ ectlla has fai led to become establish· 28 J. E:\Tmlol.. Socl3nlT CULl I\I BIA 80 (198.3). DE c:. .3 1. 198.3 ed at their release sites in Missollri where hvper. ACK;\IOWLEDGEMENTS parasitism bv T. ga/artapus was common. However All lahoraton' work was carri ed out at the Van· A. rtlbectl/a:~ persistence in VanCOU\Tr des pite ap· couver Resea rch Station. Agriculture Canada. I preciable hyperparasitism by T. g% ~~ctopu s argues thank B. D. Frazer for r es ear ~h space and review of against hyperparasitism as a predominant limita· the manusc ript, and A. T . S. Wilkinson for ad\·ice. tion to establishing A. miJccu/a in North America. C. Yoshimoto of the Bios\'stematics Research In· stitute. Ottawa conf irm e~1 m\' determination of Tetrastichus ga/a ctopus.

REFERENCES Blunck. H. 1957. Picris rapae (L .). its parasites and predators in Canada and the United States. J. Econ. Entomo!' 50:8.35·8.36. Bouletreau. M. 197 1. 'vI dabolisme rcspiratoire dc Pteromalus puparum (Ihm. Chalc. ) au cours du devcloppement et influence de la densit e de population la rvaire. Ann. Zoo!. Eco!. Anim . .3: 195·207. Delucchi. V. HJ50. Note morfologichc su Tetrastichus rapo Walker .Chalcididc parassit a di Imenotteri utili all'agricoltura. Redia .35:4 41 ·4.50. Ferriere, C. and J. C. Faure. 1925. Contribution a l' &tudc des C halcidiens parasites de I' Apanteles glomeratus, L. Ann. Epiph\·tes 11 :221 ·2.34. Gautier, C . and S. Bonnamour. 1924. Recherches sur Tetrastichus rapo. (][,-m. C halcid idae). Rey. Path. Veg. & Ent. Agric. 11:246·25.3 . Krombien, K. B. , P. D . Hurd, Jr., D . R. Sm ith and B. D. Bllrks. 1979. Catalog of HnTIenoptera in America North of Mexico. Vo!' I Sm ithsonian Institution Press. \Vashington. D .c:. 11 9Hpp. Mook, J. H. and J. !-laeck. 1965. Dispersal of Pieris hrassicae L. (: Pi c ridae) a nd of its priman' and secondary hvmenopterous parasites in a newl\· reclainled pl oder of the fonner zuiderzec. Ar· chiv . :\ecrlandaises de Zoologic 16:29.3·.312. Parker, F. D. , F. R. La\\'son and R. E. Pinnell. I D7 1. Suppression of Pieris rapac usin g a 11e\\ control S\'stem: mass releases of both the pes t and its parasit es . J. Econ. Entomol. 6·1:721·7.3.5. Picard, F 1921. Sur la biologic du Tetrastichus rapo Walk. (Il ,- rn. C halcididae). Bull . Soc. Ent . Fr. 9:206·208. Hichards. O . W. 194 0. The biolog\' of the small \\·hite bntterfh (Pieris rapae). \\'ith special reference to fac· tors controlling its abundance. J. Anim . Ecol. 9:2-! .3·28S. Wilkinson. A. T. S. 1966. Apantelcs rubeeula Yl arsh and other parasites of Pie ris rapac in British Columbia. J. Econ. Entomol. ·59:10 12· 1013.