Caribbean Journal of Science, Vol. 40, No. 1, 52-61, 2004 Copyright 2004 College of Arts and Sciences University of Puerto Rico, Mayagu¨ez

Review of the Biology of acasta (Walker) (: ) and Additions on Development and Sex Ratio of the Species

JORGE M. GONZÁLEZ1,JORGE B. TERÁN2 AND ROBERT W. MATTHEWS1

1University of Georgia, Department of Entomology, Athens, Georgia 30602, USA 2Universidad Central de Venezuela, Facultad de Agronomı´a, Instituto de Zoologı´a Agrı´cola, Apdo. 4579, Maracay, Aragua, Venezuela. Corresponding author: [email protected]

ABSTRACT.—A list of known hosts of Melittobia acasta and different biological aspects presented in previous literature are summarized and clarified. Development, sex ratio, and offspring production, on wild, facultative, and factitious hosts, and size of stages at different temperatures are shown. In general, devel- opment time is equivalent and similar to that of other Melittobia species; however, as temperature rises development time decreases. Sex ratio oscillates between 96 to 98% female depending on the host, falling into the expected percentage for most species in the . Total offspring numbers were similar to those produced by other Melittobia species using the same hosts.

KEYWORDS.—development, sex ratio, offspring production

INTRODUCTION bus, and honeybees (Apis mellifera), some re- search has targeted control aspects (Alford Melittobia are gregarious ectopara- 1975; Dahms 1984b; Doroshina 1990; Erick- sitoids of wasps and bees especially of son & Medenwald 1979; Farkas & Szalay those that build mud nests. Before Dahms’ 1985; Fye 1965; Herting 1977; Holm 1960; (1984a) revision, the genus consisted of one Holm & Skou 1972; Husband & Brown species native to Europe (M. acasta), two 1976; Jelinski & Wojtowski 1984; Kalinin & native to North America (M. chalybii and M. Molchanov 1987; MacFarlane & Donovan megachilis), and a few others from Australia 1989; MacFarlane & Griffin 1994; MacFar- and eastern Asia. After this revision the lane & Palma 1987; MacFarlane et al. 1994; number of species increased to 14 world- Maeta 1978, 1985, 1999; Packard 1864; Pou- wide. Although M. acasta remained the vreau 1973; Santis 1981; Schmid-Hempel only European species, Dahms also re- 1998, 2001; Smith 1853; Stolvov & Palevich corded it from Canada, Japan, New Zeal- 1988; Thompson 1946; Torchio 1963; and, and South America. For North Valkeila 1959; Wael et al. 1993, 1995; Zerova America, species increased to eight, includ- et al. 1986). ing M. acasta. Other studies emphasized, evolutionary, Prior to Dahms’ work, for U.S. species morphological, biological and behavioral the name mostly used in the literature was aspects, especially those related to court- M. chalybii, but these identifications were ship, with M. acasta serving as a model or often erroneous, and as many as 4 species compared with other species (Altson 1920; were confused as one (Gonza´lez and Mat- Assem 1975, 1976a, 1976b, 1985; Assem & thews 2002). Likewise, some confusion ex- Maeta 1978; Assem et al. 1982; Balfour- ists for records of M. acasta. Browne 1922; Borgia 1980; Dahms 1984b; Melittobia acasta is reported as a parasite Doroshina 1989; Gonza´lez 1994a, 1994b; or hyperparasite of members of various or- Gonza´lez & Matthews 2002; Gonza´lez & ders, including Hymenoptera, Diptera, Tera´n 2001; Gonza´lez et al. 1996, 1999, 2004; and Coleoptera (Table 1). Be- Klunker & Fabritius 1992; Lapp 1994; Lith cause it sometimes also attacks bees used 1955; Malyshev 1968; Nong & Sailer 1986; for crop pollination such as , Bom- Parker & Thompson 1928; Picard 1922, 52 MELITTOBIA ACASTA (HYMENOPTERA) 53

TABLE 1. Reported hosts of Melittobia acasta (Walker)

Host group Countries Reference Social Bees (Bombus spp.; Apis Great Britain; New Zealand Alford 1975; Balfour-Browne 1922; spp.) Erickson & Medenwald 1979; Hobbs & Krunic 1971; MacFarlane & Donovan 1989; MacFarlane et al. 1994; Valkeila 1959; Wael et al. 1993, 1995 Parasitic Bees (Psythirus spp., Great Britain; Germany Alford 1975; Wolff & Krausse 1922 Stelis spp.) Solitary Bees (Anthophora spp., Great Britain; Russia; USA; New Balfour-Browne 1922; Doroshina Chalicodoma sp., Heriades spp.; Zealand; Japan; Finland 1989, 1990; Farkas & Szalay Anthidium sp.; Megachile spp.; 1985; Herting 1977; Holm & Osmia spp.) Skou 1972; MacFarlane & Donovan 1989; Maeta 1985; Smith 1853; Thompson 1950a; Valkeila 1959 wasps (Trypoxylon Great Britain; Cuba; Venezuela; Balfour-Browne 1922; Dahms spp., spp.) Japan 1984b; Gonza´lez 1994a, 1994b; Gonza´lez & Tera´n 1996; Gonza´lez et al 2004; Maeta 1985 Parasitic wasps (Alysia Great Britain; Japan; New Altson 1920; Balfour-Browne 1922; manducator; Monodontomerus Zealand; Germany Dahms 1984b; Donovan 1989; spp.; Sinophorus turionus; Maeta & Yamane 1974; Wolff & Sphecophaga vesparum, Chrysis Krausse 1921, 1922; Husain & spp.) Khan 1986; Thompson 1950a Other solitary wasps Germany; Finland Herting 1977; Lith 1955; Wolff & (Ancistrocerus spp., Odynerus Krausse 1922; Malyshev 1911, spp. 1968 Social wasps Great Britain; Japan Bouc˘ek 1959; Maeta 1985; Maeta & Yamane 1974 and parasitic flies (Musca Great Britain; Japan Dahms 1984b; Graham-Smith spp.; Neobellieria spp.; 1916, 1919; Herting 1978; Maeta Sarcophaga spp.; Calliphora & Yamane 1974; Waterston 1917 spp.; Anthrax spp.; Metagonistylum minense; Paratheresia claripalpis) Lepidoptera Great Britain Herting 1975; Morley & Rai; Thompson 1950b Coleoptera Czechoslovakia Bouc˘ek 1959

1923; Schmid-Hempel 1998, 2001; Ranger ing species identity in Melittobia. Results 1996). will help to promote nomenclatural stabil- Lists of synonymies of M. acasta are in ity and thereby facilitate future work on Boucˇek & Graham (1978a, 1978b); Dalla this interesting genus. Here we focus on the Torre (1898); Dahms (1984a); Domenichini widespread M. acasta. (1966); Hansson (1991); Holm (1960); Kalina (1989); Kostjukov (1978); La Salle (1993); Peck (1963); and Schmiedeknecht (1909). MATERIALS AND METHODS Through careful reading of the older pri- mary literature coupled with study of mu- In order to compare the status, distribu- seum voucher materials and controlled tion, and other aspects related to the biol- laboratory studies, we are attempting to ogy of M. acasta, a thorough literature re- untangle some of the confusion surround- view was done. Laboratory studies were 54 J. M. GONZA´ LEZ, ET AL. initiated using M. acasta originally collected All experiments using S. fistularium as in Venezuela (Assays 1-4) or California, hosts were conducted in climatically con- U.S.A. (Assay 4). Unless otherwise noted, trolled chambers at Instituto de Zoolog´ıa cultures were established in 2-dram vials Agr´ıcola, Universidad Central de Venezu- and maintained at 25°C and 70% RH. ela, Maracay, Venezuela. Experiments with Assay 1: In order to see if hosts [Sceliph- other hosts (assay 4) were done in incuba- ron fistularium (Hymenoptera: )] tors at University of Georgia, Athens, Geor- could survive and develop if gia, U.S.A. were removed, individual mated females of M. acasta were allowed to lay about 100 eggs/host (n=100). Females were then re- RESULTS moved and a few days later developing third instar M. acasta larvae were removed Although some authors (Eickwort 1971, from every host. 1973; Hobbs & Krunic 1971; Holm 1960; Assay 2: To assess whether temperature Husband & Brown 1976; MacFarlane & had any influence on size, regular cultures Pengelly 1977; Maeta & Yamane 1974; were established on S. fistularium at differ- Newport 1849a, 1849b, 1852a, 1852b, 1853; ent temperatures (15°,20°,25°,30°, and Packard 1864; Spradbery 1973; Thomson 35°C) and 70% RH. Length and width of 1878; Wolff & Krausse 1921) mentioned eggs, all larval instars, and pupae were Melittobia or related species in their work, measured of a sample from the whole off- after careful analysis of those works and spring produced (Brood size approxi- available voucher specimens we conclude mately 400-500 individuals per host; that they were often working on (or found) Sample size: n=39 for each stage and tem- M. acasta (Dahms 1984a; Gonza´lez & Mat- perature). Egg widths were measured at thews 2002). two places (small and large width) because When females of M. acasta are presented of their “pear like” shape. Larval width was with a suitable host (i.e., Sceliphron spp., measured at the mid part of the body, and Trypoxylon spp.), they wander around it, pupae were measured at the junction of the and after some time spent (1-48 h) “assess- thorax and abdomen. Measurements were ing” the host, they puncture the host’s exo- taken using a stereoscope adapted with an cuticle with their ovipositor. After a few ocular micrometer. seconds, hemolymph starts to ooze from Assay 3: To study duration of each life the wound, upon which the female then stage and instar of M. acasta, parasitized S. feeds. fistularium hosts were maintained at vari- Females become distinctly physogastric ous temperatures (15°,20°,25°,30°, and 12-48 hours after first feeding. Beginning 12 35°C) and 70% RH (n=20/ each tempera- to 24 hours after feeding, most females start ture). Observations were made every 12 laying eggs (Table 2). Eggs are coated with hours and the developmental stage was re- a sticky substance that allows them to ad- corded. Sample individuals were removed here to the host and to other eggs. Eggs are (see assay 2) for measurements and to de- normally laid in batches of 4 to 12, however termine if they had passed to the next in- lower egg numbers or individually depos- star. Assay 4: In order to compare develop- TABLE 2. Life history development of Melittobia ment time and sex ratio of M. acasta on dif- acasta on different hosts at 25°C. (S.f. n = 90, 50% RH; ferent hosts, cultures of the were other hosts n = 40, 50% RH) made using as hosts: S. fistularium (n=90), Trypoxylon politum Megachile rotun- Eggs Larvae Pupae Total (n=40), Host (days) (days) (days) (days) data (n=40), Neobellieria bullata (n=40). One female of M. acasta was placed per host. Sceliphron fistularium 1-3 14-16 3-5 18-24 Life history was followed to determine du- Trypoxylon politum 2-4 9-15 6-8 17-27 ration of each developmental stage. Off- Megachile rotundata 2-5 8-14 5-8 15-27 Neobellieria bullata 2-7 8-12 5-9 15-28 spring were counted to determine sex ratio. MELITTOBIA ACASTA (HYMENOPTERA) 55 ited eggs are not rare. The female initially the temperature (Table 4). Fourth instar lar- lays eggs on the ventral region of the host, vae have a slower development, and they but eventually covers other areas of the take on the color of the host they are feed- host body. ing on. All larvae are vermiform and the Two female morphs (brachypterous and main difference between instars is their size macropterous) exist (Gonza´lez & Tera´n (Table 5). At 15°C, second instar larvae en- 1996; Gonza´lez et al. 1996), and although tered diapause; after 10 months, these dia- they differ in some particular behaviors pausing larvae were placed at 25°C, and (courtship, migration tendencies), their egg most resumed normal development and laying behavior was basically identical. The became adults. main difference is that brachypterous fe- Pupae appear 10 to 15 days after the eggs males deposit eggs immediately upon are laid (Tables 2). They are exaerete and emergence and mating. measure about 1.5 mm long and 0.5 mm After removing all the M. acasta larvae wide, regardless of temperature (Table 5). from 100 parasitized S. fistularium prepu- Pupae are creamy-white and darken as pae (Assay 1), 14 hosts were found to have they mature. Males are brownish, and have black spots or darkened wound marks, pre- red “dots” where the eyes should be. Fe- sumably caused by the female’s ovipositor. male eyes become pink and later red, while None of these hosts developed, while the the body gets dark brown-black. Males be- others did. Out of the 100 hosts, 73 became come shiny dark brown, females shiny apparently normal adult S. fistularium, with black when close to emerging as adults. the other 13 succumbing to fungi. Males are the first adults to emerge, a Eggs hatched between 1-3, 2-4, and 2-7 group of brachypterous females emerges days in S. fistularium, T. politum, and N. bul- after that, and macropterous females lata respectively (Table 2). Larval and pupal emerge last. Some males were observed development also varied with host type fighting, and in most cases the first to (Table 2). Offspring numbers and sex ratio emerge killed some male pupae that were varied among the hosts (Table 3). almost ready to become adults. Eggs hatch between 12 to 48 hours, de- pending on the temperature (Table 4), and DISCUSSION have an average length of 0.21 mm (Table 5). The large egg width averages 0.06 mm Melittobia acasta appears to be the only and the smaller width averages 0.04 mm Melittobia species present in Europe (in- regardless of temperature (Table 5). First cluding Russia) but it is also found in Ar- instar larvae are easily recognized by the gentina, Canada, Costa Rica, Cuba, India, apparent body segmentation and they are Japan, New Zealand, Australia, U.S.A., and similar in length to the eggs (Table 5). The Venezuela (Table 1). Torchio (1963); Hobbs second and third instars are recognized not & Krunic (1971); and Husband & Brown only by the difference in size, but because (1976) mention that they found M. chalybii just after molting the last larval “skin” is attacking Megachile rotundata in some areas attached to the distal end of the body. They of USA and Canada. However, according also molt at different times depending on to descriptions and places mentioned it is likely that they were actually dealing with TABLE 3. Offspring production and sex ratio of M. acasta. Moreover, MacFarlane & Griffin Melittobia acasta on different hosts at 25°C(S.f. n = 90, (1994) mention that “according to Mat- 50% RH; other hosts n = 40, 50% RH) thews” Husband & Brown (1976) actually found M. acasta. Holm (1960) mentions M. Sex chalybii Bombus Host Males Females ratio attacking colonies in Den- mark. Because of this location, we suspect Sceliphron fistularium 14 ± 1.2 460 ± 26.3 3:97 that they actually found M. acasta, which Trypoxylon politum 13 ± 6.3 552 ± 53.2 2:98 the same author and a collaborator found Megachile rotundata 1.8 ± 1.4 38 ± 22.1 4:96 later attacking Megachile species (Holm & Neobellieria bullata 2.7 ± 1.5 87.2 ± 42.2 3:97 Skou 1972). 56 J. M. GONZA´ LEZ, ET AL.

TABLE 4. Time ranges (hours) for each developmental stage in Melittobia acasta (Walker) developing on S. fistularium at different temperatures (n = 20 hosts/temperature).

Temperature First instar 2nd instar 3rd instar 4th instar °C Egg (larvae) (larvae) (larvae) (larvae) Pupae Total 15 36-60 36-60 ** 20 12-36 36-60 60-84 60-84 216-264 96-144 480-672 25 12-36 12-36 36-60 36-60 216-264 72-120 384-576 30 8-20 6-20 6-18 36-60 192-240 72-120 320-478 35 8-20 6-20 6-18 12-36 12-36 72-120 116-250

TABLE 5. Size of different stages of Melittobia acasta (Walker) on Sceliphron fistularium (Dahlbom) at different temperatures. (X ± SD; n = 39 larvae measured/temperature). Relative Humidity: 70%)

Development Stages Temp. Larvae Larvae Larvae Larvae °C Eggs 1st instar 2nd instar 3rd instar 4th instar Pupae 15 Length .21 ± .004 .21 ± .000 .47 ± .01 ** Width* .06 ± .000 .06 ± .003 .14 ± .003 Width 2 .04 ± .000 20 Length .21 ± .003 .21 ± .003 .47 ± .01 .92 ± .093 1.33 ± .11 1.5 ± .006 Width* .06 ± .001 .06 ± .001 .13 ± .063 .42 ± .067 .48 ± .061 .5 ± .005 Width 2 .04 ± .000 25 Length .21 ± .028 .21 ± .003 .47 ± .001 .99 ± .09 1.34 ± .18 1.6 ± .007 Width* .06 ± .001 .06 ± .001 .13 ± .007 .33 ± .03 .44 ± .07 .5 ± .005 Width 2 .04 ± .000 30 Length 21 ± .003 .21 ± .003 .47 ± .01 .94 ± .09 1.31 ± .11 1.5 ± .004 Width* .06 ± .001 .06 ± .001 .13 ± .006 .38 ± .032 .48 ± .061 .5 ± .004 Width 2 .04 ± .000 35 Length .21 ± .002 .21 ± .002 .47 ± .011 .89 ± .099 .128 ± .11 1.5 ± .004 Width* .06 ± .001 .06 ± .001 .13 ± .006 .42 ± .033 .48 ± .047 .5 ± .003 Width 2 .04 ± .000 *: Two widths were measured in eggs. The first refers to the larger one; In larvae and it refers to the only one measured. **: 2nd instar larvae remained in diapause at 15°C.

Melittobia acasta is clearly capable of trations; however, this was done in our parasitising a wide variety of be- laboratory with M. digitata and M. australica longing to different orders (Table 1), al- (L.Deyrup pers. comm.). Host feeding by though it seems unlikely that this broad female Melittobia acasta is very similar to range of hosts attacked would be noticed that observed in other Melittobia species as under field conditions. The fact that several reported by different authors (Balfour- species of pollinators are apparently regu- Browne 1922; Coˆnsoli and Vinson 2001; larly attacked by M. acasta should be of con- Dahms 1984b; Malyshev 1968; Maeta & Ya- cern, especially where populations of these mane 1974; Schmieder 1933). After punc- pollinators are artificially manipulated. The turing the host cuticle with her sting, fe- importance of M. acasta in these situations males of M. acasta feed on the oozing merits further study, because populations hemolymph, as do most idiobionts. Ac- can build to high levels in a relatively short cording to Doutt (1959) host fluids provide time due to the rapid development time of the proteins necessary to stimulate egg de- this gregarious parasitoid. velopment. However, while host feeding is Parker & Thompson (1928) could not common among macropterous females, it is stimulate females of M. acasta to feed on not for the brachypterous females. The lat- honey or sugar water at different concen- ter emerge with a large load of eggs and MELITTOBIA ACASTA (HYMENOPTERA) 57 start laying them immediately after mating, occurs widely under a broad range of en- similar to M. digitata (Coˆnsoli and Vinson vironmental conditions from tropical to 2001). temperate regions, the cues involved in dia- Maeta and Yamane (1974) reported dark- pause merit further study. Even though the ening of hosts wounds made while feeding total development increases when tempera- by the ovipositor of M. japonica (=M. acasta). ture increases (Table 4) the size of the dif- In our experiments only 14, out of 100 ferent stages of M. acasta remain the same hosts, S. fistularium prepupae’s sting marks (Table 5). were darkened, and none of these were Two female morphs are commonly able to pupate and develop into normal found in all Melittobia species (Consoˆli & adults. This sting mark also was found in Vinson 2002a, 2002b; Gonza´lez & Tera´n Tenebrio molitor pupae attacked by M. digi- 1996; Gonza´lez et al. 1996; Schmieder 1933). tata, and such hosts seldom developed into Lith (1955) reported the presence of 1% of adults (Deyrup et al. 2003). Trypoxylon poli- brachypterous females and termed them “a tum prepupae did not show evidence of genetical anomaly.” Morphological and be- melanization at sting sites. Since the last havioral characteristics of males and the larval skin surrounds Neobellieria bullata pu- two female morphs of M. acasta and M. aus- pae, we do not know whether this occurs in tralica were described by Gonza´lez & Tera´n this host. The striking thing is that, except (1996). Gonza´lez et al. (1996) compared for mortality due to fungi, all 73 out of 100 courtship behavior among morphs of M. parasitized prepupae of S. fistularium that acasta and other Melittobia species. Brachy- did not show sting mark evidence were pterous females represent about 1-2% of subsequently able to pupate and develop the total females produced by M. acasta on into apparently normal adults. S. fistularium, T. politum and M. rotundata When stinging their host, M. acasta fe- hosts. No brachypterous females were pro- males could also inject fluids whose effect duced on Neobellieria bullata. is to diminish body movements, stop host Development time varied slightly de- development, or both, as Malyshev (1968) pending on the host (Table 2). The same can suggested. Buckell (1928) observed a simi- be said about the total clutch size and sex lar situation working with M. chalybii (=M. ratio and it seems directly related with the digitata), a species that is closely related to size of the host (Table 3). Similar results M. acasta (Assem et al. 1982; Dahms 1984b). have also been found for other Melittobia It appears that substances injected during species (Gonza´lez & Matthews 2002). The host stinging by M. acasta vary in their ef- general tendency is that larger hosts result fects on host physiology and development in slightly shorter development time and a and that further study of the venom and slightly less female-biased sex ratio accessory gland materials would be re- (Gonza´lez & Matthews 2002). Overall, warding. ranges of development times and sex ratio When temperature is controlled, hatch- of M. acasta produced on the four hosts ing time and total development time can be used in these experiments fall into the ex- artificially modified. At 15°C (70% RH), pected numbers for the genus (Gonza´lez & eggs hatch about 48 hours after being laid, Matthews 2002). but as temperature increases, hatching time diminishes to about 12 hours (Table 4). The Acknowledgements.—Thanks to Michael same trend is found for every developmen- Schmid (Wurzburg University), J. van den tal stage of M. acasta, resulting in a faster Assem (Rijjksuniversiteit Leiden), and the total development time with higher tem- personnel of the Interlibrary Loan depart- perature (Table 4). However, at 15°C (70% ment (University of Georgia) who helped RH), after entering the second instar, larvae to locate obscure papers on Melittobia of M. acasta remained in diapause, and ter- acasta. Part of the research was based on the minated only when the temperature was Ph.D. thesis of the senior author and was increased. Diapause regulation in M. acasta partially supported by CONICIT- is wholly unstudied, but since this species Venezuela, and CDCH of Universidad 58 J. M. GONZA´ LEZ, ET AL.

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