Corresponding author: Mark R. Shaw ( firstname.lastname@example.org )
Academic editor: Gavin Broad
© 2017 Mark R. Shaw.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation: Shaw MR (2017) Further notes on the biology of Pseudavga flavicoxa Tobias, 1964 (Hymenoptera, Braconidae, Rhysipolinae). Journal of Hymenoptera Research 54: 113-128. https://doi.org/10.3897/jhr.54.10789
Pseudavga flavicoxa, a solitary koinobiont ectoparasitoid of Bucculatrix thoracella, attacks host larvae early rather than late in their final instar, subsequent development of the parasitoid then occurring within the host cocoon. This paper supplements an earlier contribution outlining other aspects of its biology and taxonomy. The host is stung repeatedly, both into the thoracic region and elsewhere on its body, causing temporary paralysis and also enabling host-feeding, which preceded oviposition in all observed cases. Stung hosts then intercepted without oviposition occurring recovered and (like parasitized hosts) resumed feeding and then constructed a cocoon, but suffered developmental arrest as a prepupa. The egg is invariably laid onto the arthrodial membrane between the first and second thoracic segments, to which it is glued. This site is first prepared by the female by a to-and-fro motion involving contact by the lower valves of the ovipositor, which are somewhat blade-like and sharp-edged. It is unclear whether dried traces of a ‘glue’, presumably originally liquid, subsequently seen at this site were of host origin resulting from a small wound or arose as a secretion from the female wasp, but the former is suggested. The egg was seen to issue from the extreme base of the ovipositor, at most guided onto the prepared patch by the parted lower valves. Although clearly partly plurivoltine, P. flavicoxa is remarkably long-lived as an adult, both sexes being easily kept alive under semi-natural conditions (Edinburgh, U.K.) during the late summer and autumn, males for 8 weeks and females for up to 20, despite their small size (ca 2.2–2.4 mm long). Dissection of gravid females showed that each of the 4 ovarioles carried just one mature egg at a time, with submature eggs remaining only poorly developed until the mature egg was expended.
Host-feeding, venom effect, developmental arrest, egg placement, ovipositor structure, longevity
Some aspects of the biology of the small rhysipoline braconid Pseudavga flavicoxa Tobias as a koinobiont ectoparasitoid of the bucculatricid moth Bucculatrix thoracella (Thunberg) were outlined by
Larvae of B. thoracella, some parasitized, were collected by Dr Ian Sims at Jealott’s Hill, Berkshire, England as they descended from leaves of Tilia × vulgaris for cocoon formation in the period 9.ix–4.x.2014. The resulting host cocoons were sent to Edinburgh and received on 10.x.2014, where they were immediately placed in a fully shaded and unheated outdoor wooden shed (cf.
After a brief period as a leaf miner, the larva of B. thoracella feeds on the parenchyma of Tilia leaves from the leaf underside, leaving a windowed pattern of damage visible from the upperside. To accomplish its moults, the larva constructs a temporary small and dense silken shelter, in which ecdysis occurs. When fully fed, the larva descends from the leaf on a silken thread, and spins its characteristic ribbed cocoon upon landfall. Following recent range expansion (outlined by
After being fed for at least 25 days on dilute honey, when dissections of others indicated that eggs would certainly be mature, females of P. flavicoxa were introduced singly to an undisturbed final instar B. thoracella larva beside its feeding damage on a cut piece of Tilia leaf trapped by the cork of a 7.5 × 2.5 cm upright glass tube. Because the parasitoids were generally very slow to successfully parasitize the hosts, several tubes were set up to be observed simultaneously (Fig.
Emergence of P. flavicoxa adults from the overwintered cocoons was during the period 6–20.vii.2015. Males (N=42) emerged on average 5.25 days before females (N=32). When provided with dilute honey, both sexes lived for an extraordinary length of time given their small size (ca 2.3 mm long); males routinely for at least eight weeks, and some females for as long as 20 weeks (the last two females were killed by the first frost recorded in the outdoor rearing shed on 1.xii.2015). The adult progeny from the 2015 captive ovipositions emerged in July 2016. This suggests that P. flavicoxa is essentially univoltine, although
No interactions were seen between the parasitoid and penultimate instar hosts, nor hosts in their moulting cocoons. Henceforth ‘host’ refers to the final instar. The female wasps showed only very slight interest in the feeding damage caused by hosts (Fig.
It gradually became clear that hosts late into their final instars were unattractive, and perhaps genuinely unsuitable, which might have accounted for a proportion of the cases in which hosts were completely ignored, and also the failure to obtain ovipositions in the autumn of 2014 (
No host-feeding interactions were seen apart from the concurrent host-feeding that preceded each oviposition. Accepted hosts were stung repeatedly as temporary paralysis ensued, and in all observed cases pierced in both thoracic and abdominal regions, though apparently at random. Although it is possible that venom was administered preferentially into one or other of these sites, no difference in behaviour was noted. During and following the stinging process the wasp made repeated traverses and turns along the long axis of the host (Fig.
While many parasitoid Hymenoptera ovipositing in (or on) exposed hosts are quick to do the deed, instances of extreme patience or slow stalking have been recorded in several other studies (e.g.
The egg, measuring 0.28 × 0.13 mm, was positioned with its long axis transversely along the membrane between the first and second thoracic segments on all 14 hosts on which an egg was laid, as had been the case for all seven hosts with an egg observed in nature in 2014 (
Eggs positioned on the intersegmental membrane between the host’s prothoracic and mesothoracic segments.
Dissections of females in the first weeks after their emergence suggested that eggs were rather slow to mature (with access to dilute honey only), and it was not until they were about 3 weeks old that they were judged all to have fully mature eggs, one in each of the two paired ovarioles making four in all, with subsequent eggs in each ovariole remaining greatly underdeveloped until the mature egg had been laid (Fig.
The temporary paralysis caused to facilitate oviposition wears off after a few tens of minutes, and the host gradually resumes apparently undiminished feeding activity within an hour (exceptionally only after 3 hours). The approximate minimum and maximum extent of this before cocoon construction (after at least 1 and more often 2 or even 3 days) is shown in Figs
Amount of feeding by host following oviposition until cocoon formation 1 and 3 days later respectively (not to same scale).
Host stung but not oviposited on then removed from cocoon, after respectively 11 and 20 days.
This suggests a reason why hosts too late in their final instar are rejected; if the arrest suffered by the host results from a disturbance to the endocrine system, as has been deduced to be caused by Rhysipolis species (
The ovipositor overall has an unusual structure, with a strong but blunt upper valve and the acute lower valves appearing blade-like except in their apical fifth (Figs
A serrated tip (presumably serving to hold the ovipositor in the host while venom is administered) is present on the upper edge of the lower valves (Fig.
Thin sections across ovipositor. 18 just apicad of the broad part of lower valve as it starts to narrow 19 about half way along broad part 20 near origin of sheaths 21 near extreme base. Scale bars 0.04 mm.
In principle the to-and-fro motion of the ovipositor immediately preceding oviposition could have been associated either with host-wounding or with spreading a secretion produced by the wasp. The lower valves of the ovipositor are rather blade-like for most of their length and, although not (on their lower edge) serrated (Fig.
I am grateful to Ian Sims, who first reared P. flavicoxa in Britain and subsequently collected and sent host cocoons containing the parasitoid to enable this study; to Viv Allison (Department of Comparative Physiology, University of Edinburgh) who prepared the ovipositor sections; and to Richard Lyszkowski for taking and processing the stacked photographs of ovipositor dissections. In review Istvan Miko made valuable remarks on the ovipositor.