The Agrotis exclamationis larvae collected in Aldbury in October 2012 were exposed to O. luteus females; during the period of observation, from about 20:00-22:00. Ophion luteus females paid no attention to the Agrotis larvae, even when walking over them. In light of the subsequent parasitoid emergence, they could already have been parasitized, or oviposition may have subsequently occurred in the dark, when they were not under observation. It proved difficult to overwinter the A. exclamationis larvae, which bury themselves in soil but are periodically restless. Most larvae succumbed to fungi but one survived the winter. On 19.iv.2013, it was found that a large parasitoid larva had emerged from this, probably prepupal, caterpillar and had begun to spin a cocoon below the host remains. Cocoon formation took about seven days, with the cocoon initially composed of loose, white silken threads (Fig. 3a) but gradually darkening and taking on the characteristic appearance of an Ophion cocoon, dark brown, slightly paler centrally (Fig. 3b). An adult female O. luteus emerged in the night of 2-3.ix.2013 (specimen deposited in BMNH). At around this time, O. luteus were regularly caught in GRB’s light trap.
At about the same time as this specimen was pupating, MRS identified a female O. luteus reared from a fully grown Agrotis ?vestigialis (Hufnagel) larva, or prepupa, collected from under moss at Braunton Burrows, North Devon (SS4437) on 8.v.2007 (coll. B.P. Henwood) (specimen in NMS). The exact dates of cocoon formation and emergence of the adult parasitoid are not recorded, but were later in 2007.
HS also reported his previously unpublished rearing records from 1976–1992, when he reared 43 O. luteus from both Agrotis exclamationis and A. segetum field-collected larvae in Germany (Table 1) (12 reared O. luteus specimens deposited in HSC). Unlike GRB’s rearing, the O. luteus larvae in HS’s rearings all emerged from their host larvae in the year of collection, although it should be noted that these emergences took place under unnatural light conditions, as detailed in Materials and Methods. HS also found some Ophion cocoons in the soil in November; however, emergence of these O. luteus adults was almost invariably between July and early September in the following calendar year, except for two that emerged in May. The phenology of both hosts and O. luteus may differ in Germany, at least in particularly warm years (such as 1977) but in Britain, A. exclamationis usually overwinters as a prepupa in the soil, pupating the following spring.
Host records for O. luteus in the literature cover a very wide range of Lepidoptera across ten families, including many noctuids, and even a tenthredinid sawfly (Yu et al. 2012). Most can be dismissed out of hand, especially as in the past almost any large yellowish ichneumonid was liable to be referred to O. luteus. However, Meyer’s (1927) and Győrfi’s (1943, 1944) references to, respectively, Agrotis segetum and A. vestigialis as hosts are, in retrospect, entirely plausible.
Almost all O. luteus records from GRB’s Nocturnal Ichneumonoidea Recording Scheme are from August and September (and into early October) (Fig. 2), which is when large larvae of A. exclamationis and some other Agrotis species are available. However, as discussed by Brock (1982), there is a distinct, though rarely collected, cohort of apparent O. luteus on the wing in May. These specimens are typically smaller than normal O. luteus, with fewer antennal flagellomeres and more buccate heads (there is a distinct ocellar-ocular space and the temples are long in dorsal view). These have informally been referred to as the ‘distans’ morph. The taxonomy of this morph is rather complex; the lectotype of Ophion distans Thomson, 1888 is very similar to that of Ophion luteus (Linnaeus, 1758) (Brock 1982) so, although this spring generation is informally called the ‘distans’ morph, if there were found to be two species (spring and autumn-flying) then the ‘distans’ morph would actually take the name Ophion luteus, with the autumn generation taking the next available name, Ophion slaviceki Kriechbaumer, 1892 (Brock 1982). However, Schwarzfeld et al. (submitted) have found that all British specimens of O. luteus sequenced for Cytochrome Oxidase I, including two ‘distans’ specimens collected in May, cluster together as apparently one monophyletic species.
Brock (1982) reports that O. luteus of the ‘distans’ form have been reared from Ochropleura praecox (Linnaeus) (Noctuidae: Noctuinae) on sand dunes, based on specimens in Claude Morley’s collection, but the location of these specimens is now unknown. Four specimens in BMNH, reared by Claude Morley but with no host names given, seem to be ‘distans’ although three of these have atypical mandibles, having the acute internal angle between the teeth that is a feature of most Ophion species other than O. luteus. The lectotype of Ophion luteus, and other ‘distans’ specimens, have mandibles typical of the common and widespread form of O. luteus.
Agrotis exclamationis can have a small second brood (as occurred in 2013 in southern England), and it is plausible that the early-flying ‘distans’ form results from late summer or autumn-pupating host individuals, with the parasitoid’s early cocoon formation triggered by hormonal changes in the host. These could give rise to adult O. luteus emerging in the late spring. However’s HS’s autumn-cocooning O. luteus are of the usual, autumn-flying morphology, including the two specimens that emerged in May (possibly as a result of unnatural rearing conditions). There are also, perhaps more pertinently, closely related dune-inhabiting noctuid species with this different phenology. Both factors mean that alternative hosts may be available in some areas for an early summer brood of O. luteus.
There are no reliable rearing records of O. luteus from any Xestia species. Xestia spp. and O. luteus have non-synchronous life cycles in Britain, with fully-grown Xestia larvae unavailable at the time for oviposition by O. luteus. The available evidence is that O. luteus is a parasitoid of Agrotis larvae, contrary to Várkonyi et al. (2002). Várkonyi et al.’s (2002) population modelling of boreal Xestia species implicitly assumes that O. luteus is a parasitoid attacking early instar host larvae, switching between two cohorts of Xestia spp. (which have a two year life history at high latitudes), because Xestia are not fully grown in Finland when O. luteus is on the wing. Várkonyi et al. (2002) also report O. luteus rearings from Euxoa species, which over-winter as small larvae, and use this as evidence for O. luteus ovipositing in small larvae of Xestia spp. This is contrary to our findings, as O. luteus adults are only on the wing when their Agrotis hosts are well-grown, and oviposition in young larvae would be unique within the genus. MRS has experience of rearing at least ten British Ophion species, always from Lepidoptera larvae collected as late (probably final) instars and never from larvae collected young, which he collects as often as possible for the sake of rearing Microgastrinae and Rogadinae (Braconidae) that kill hosts young. Furthermore, common Xestia species are easily collected as larvae in Britain, and have repeatedly been reared in large enough numbers for it to be implausible for regular parasitism by O. luteus to have been overlooked in Britain. There is a possibility that the Scandinavian and British specimens identified as O. luteus represent separate species (G. Várkonyi pers. comm.) although there has been no published evidence to support this. Three specimens of Ophion reared from Euxoa in Scandinavia have been identified as O. luteus by J.P. Brock (Brock, pers. comm.), which again raises the question of whether O. luteus as currently defined actually conceals more than one species, assuming that the host identification as Euxoa is correct (these specimens were not available to us). Despite these outstanding questions, we can now say that the common European species that we call Ophion luteus is most likely a frequent parasitoid of the noctuid Agrotis exclamationis and congeners and the hosts of any cryptic species within this complex should be found within noctuid larvae that are almost certainly late instars at the time the Ophion species is/are on the wing.
Identification of Ophion luteus
As with many species of Ophion, O. luteus is predominantly testaceous/pale orange and many Ophion in collections (and online images) are misidentified as O. luteus, which has generally been used as a catch-all name. However, Brock (1982) clarified the identification of O. luteus in his comprehensive key to the British Ophion species. This key can be difficult to use (because they are on the whole difficult species to identify), but O. luteus is usually relatively straightforward to identify. With the exception of very aberrant specimens, such as those reared by Morley (see above), O. luteus (including all specimens of the “ordinary” form and most of the “distans” form) can be identified by the combination of the long hind trochantellus (Fig. 4) and the usually characteristic mandibles (Fig. 5), which have simply tapered internal edges to the mandibular teeth, lacking internal angles at the base of the teeth (compare with the mandible of Ophion crassicornis Brock in Fig. 6), and often show considerable wear. Very occasionally, Ophion crassicornis may have very worn mandibles too, when the internal angles of the teeth are then not visible. Additional useful recognition features for O. luteus are the strongly sinuous fore wing vein Rs and the very short ramellus on fore wing vein 1m-cu (Fig. 7), together with the sparsely punctate mesopleuron (densely punctate in O. crassicornis) and very weak median longitudinal carinae on the propodeum (strong centrally in O. crassicornis). The mandibular teeth of O. luteus are frequently granulose in sculpture and the teeth may be worn down; the range of mandibular abrasion is shown in Fig. 5. Presumably the mandibles are abraded when the Ophion adults emerge from the soil, as this is seen in males as well as females and the mandibles of our reared specimens are unabraded and shiny. Some females have particularly strongly abraded mandibles (Fig. 5c), which still requires explanation – perhaps the soil that the adults need to tunnel through from their subterranean cocoons can become very strongly compacted and hard following a dry summer period, but males in general do not exhibit such extreme wear. Agrotis larvae are found above the soil surface at night, when they are presumably attacked by O. luteus, and O. luteus does not exhibit any modifications typically seen in ichneumonoids parasitising soil-inhabiting Lepidoptera, such as robust legs and short antenna.