Identity of the larval specimen

The specimen can be easily identified as a larval representative of neuropteran insects. The overall body organisation (Fig. 3a) with three pairs of walking appendages leaves no doubt that the specimen is an insect. The strongly prognathous mouth parts combined with the arrangement of the mandibles and maxillae into an apparent pair of functional stylets and the distinct sclerotic neck (cervix) are especially strong indications that the specimen is a larval neuropteran.

Fig. 3 Restoration of the fossil mantis lacewing larva and comparative material of different representatives of Mantispidae. a Restoration of the new fossil larva in ventral view. b First larval stage of the extant species Mantispa uhleri; simplified from [5] (their Fig. 4A). c, d. Antenna (c) and labial palp (d) of first larval stage of the extant species Mantispa pulchella; simplified from [14] (their Fig. 15). e Head of Plega melitomae; note the curved mandibles; modified after [15] (his Fig. 42). f Fossil mantis lacewing larva described by Ohl [1]; simplified from [1] (his Fig. 1b) Full size image

The close association with a spider, even clutching the spider leg with the tarsal claws immediately gives a hint that this specimen could be a representative of Mantispidae. Many modern-day first stage mantis lacewing larvae are known to climb on spiders to later on feed on the eggs within the egg sacs of the spider.

Yet what about other characters? The strongly club-shaped elements of antennae and labial palps support the interpretation that the specimen is a first larval stage of a mantis lacewing. While some larval representatives of Hemerobiidae also have similar appearing club-shaped labial palps ([13], his plate 5), the combination of club-shaped elements on antennae and labial palps seems in modern forms only present within Mantispidae ([5], their Fig. 4A, simplified in Fig. 3b; [14], their Fig. 15, partly simplified in Fig. 3c, d). Hence this morphological structure is compatible with such an interpretation of the fossil.

A more difficult character is the structure of the mandibular-maxillary stylets: they are inward curved in the fossil, but straight in most modern forms [5, 8]. Yet there are also some less well-known cases in which modern mantis lacewing larvae possess curved mandibular-maxillary stylets ([15]; simplified in Fig. 3e).

We should furthermore expect the presence of a prominent empodium (extension between the tarsal claws) in the fossil, as this structure is known from mantispids, but also from many other neuropteran larvae (e.g., Hemerobiidae, see [13], his plate 5). However, such structures are not apparent. In the well-preserved leg grasping the spider leg the empodium might be hidden behind the spider leg (see below). The secondary absence of prominent empodia also does not seem unusual within Neuroptera.

In summary, the morphology of the specimen strongly supports an interpretation of the fossil specimen as a stage one larva of a representative of Mantispidae. Further systematic interpretations are more difficult. Curved larval mandibles occur in representatives of Symphrasinae [15]. Yet, according to Liu et al. [16] Symphrasinae is either sister group to all other mantis lacewings or even non-monophyletic. In the latter case, curved larval mandibles may well represent a plesiomorphic character. Our knowledge of larval morphology and biology of most mantis lacewings is still very incomplete [8]. We will need a denser sampling of larvae before being able to resolve character evolution of larval characters.

A case of palaeo-parasitism?

Inferring the interactions between two extinct organisms is not as simple as in extant forms, as direct observation is not possible. Nagler and Haug [17] discussed different types of information that can be used for such an enterprise.

Two different types of indications can be applied in the present case. As always, both depend on our knowledge of the extant forms of Mantispidae. Firstly, phylogenetic inference is a strong indicator here. As argued above, the morphology of the fossil larva is a clear indicator that it is a first larval stage of a mantis lacewing, and extant mantis lacewing larvae have repeatedly been characterised as parasites (see also further below on this point).

Secondly, this interpretation is further supported by the fact that the fossil larva is in direct contact with the fossil spider. Modern forms are also known to board spiders via the legs [4]. The fact that the tarsal claws are in direct contact to the leg and the empodium is not visible, hence most likely behind the leg, makes a strong case that the spider leg was indeed tightly gripped by the larva. As not all modern-day first stage mantis lacewing larvae interact with spiders the second aspect is quite important for the present case.

It therefore seems likely that the fossil behaved in a similar way to modern-day first-stage larvae of Mantispinae, boarding spiders and waiting for eggs to be produced. The only other fossil providing a comparable case was described by Ohl [1] from significantly younger Eocene amber (Fig. 3f). Yet, in this case less morphological details of the larva were available as the head region is deeply concealed between the two body regions of the spider. On the other hand, the position on the spider is more comparable to the known final position in modern larvae. In both cases there should be little doubt that the larva is a first stage of a mantis lacewing intentionally interacting with spiders, just like their modern counterpart.

Still there remains one aspect that makes it still difficult to identify these two fossil finds as cases of palaeo-parasitism. The simple question is: are modern-day larvae of mantis lacewings indeed parasites?

Life habits of modern-day mantis lacewing larvae: The details

Classic categories such as ‘predator’ or ‘parasite’ are in fact often not easily applied to all the variety of life strategies employed by the myriads of different insect species. As possible cases of intermediate feeding strategies many wasps, dipterans or strepsipterans have been addressed as ‘parasitoids’, adult midges as ‘micro-predators’, or better temporary parasites. This demonstrates already that our coarse categories cannot properly reflect the true diversity of ecologies out there.

Consequently, the literature seems to a certain degree “undecided” how to address the feeding habits of first stage mantis lacewing larvae: Some authors call them ‘preying’ or ‘predation’ [1, 4,5,6, 8], in other cases other authors (or even the same ones) refer to ‘parasitism’ [1, 18, 19] or use related expressions such as ‘host’ [1, 8, 18, 19].

Obviously, a differentiated view is necessary here. Already Redborg [4] pointed out that the habit of the larvae to feed on the spider eggs cannot be interpreted as parasitism, but represents a case of predation. Indeed, the egg sac cannot be parasitised (expression for example in [1]), and also the eggs are not only parasitised, but more or less entirely consumed.

However, some aspects are still reminiscent of parasites. The emergence of (pharate) mantis lacewings from spider egg sacs [4, 5] is strongly reminiscent of parasitoid wasps emerging from their hosts. Still the process is quite different. Even more resemblance to “classic” parasitism is present in cases in which the larva mounts the spider before it has produced the egg sac. This attachment behaviour is indeed very reminiscent of the behaviour of many parasites in the strict sense. Yet, such a behaviour could also be interpreted as a kind of phoresy, but two other aspects can apparently be coupled to spider boarding possibly qualifying for parasitism in the strict sense.

Firstly, there are few reports that some larvae do not sit at the area between prosoma and opisthosoma (the pedicel), but enter the book lungs of the spider [4, 5]. Although there is no report of details this will clearly affect the spider negatively while providing positive effects, at least shelter and humidity, for the larva. Such a behaviour is also reminiscent of well-known parasites that live in the gill chambers or lungs of their hosts, such as bopyridean isopods or tongue worms (interestingly we have different types of inferences pointing to parasitic behaviour of early fossil representatives of these groups; [20,21,22,23,24,25,26]).

Secondly, at least some first stage mantis lacewing larvae that board spiders before they have produced egg sacs seem to bridge the time until eggs are available by piercing the spider and feeding on its haemolymph. This last point would definitely qualify for being interpreted as parasitism in the strict sense. Unfortunately, it is not fully clear [4], but is also based on not entirely direct observation. Still it seems quite likely that some first stage mantis lacewing larvae that perform spider boarding also feed on the spider’s haemolymph, and hence are parasites in the strict sense. We can only assume that both fossils, as they boarded spiders that do not yet seem to already carry egg sacs, would also have employed this strategy and indeed represent parasites. In summary, they both represent very likely cases of palaeo-parasitism.

A case of hypermetaboly?

As pointed out above, modern-day first stage larvae of mantis lacewings feeding on spider eggs develop through a quite unusual developmental pattern: The first stage larva in fact resembles the later adult more than the two following stages. This first stage larvae, as the adults, are mobile and active, while stage two and three larvae are largely immobile. They also lack sclerotisation. The grub-like body form is most likely of advantage for gaining size. From stage two to stage three, they can increase their size by more than 300% [5], which is quite drastic for a single moult. This is at least a possible functional explanation for the grub-like morphology: there is no selective pressure for any mobility, the morphology can therefore be “adjusted” to the main function of the larva – eat and grow.

First stage larvae largely resemble the larval stages of other neuropteran insects, especially those of Berothidae, but also those of certain representatives of Hemerobiidae or Chrysopidae. Therefore, we can assume that the mobile, campodeiform appearance of the first stage larvae is an ancestral character, the grub-like morphology is a derived one.

The grub-like morphology of the stage two and three larvae could most likely only evolve after the strategy of entering egg sacs had evolved as otherwise selective pressures would probably have acted for preserving the plesiomorphic type of morphology in these stages. We therefore assume that the earliest representatives of mantis lacewings that had evolved larvae that would enter egg sacs in the first stage would not yet have possessed grub-like larval stages two and three. Only later in this lineage could this type of morphology have evolved.

In consequence, we suggest that the presence of first stage larvae that board spiders is not necessarily a direct indication of highly specialised grub-like larvae, especially as the curved mandibles in the fossil may indicate that it still lacks some of the derived characters. We therefore disagree with Ohl [1] that hypermetaboly was necessarily present already in the stem-species of Mantispinae; it might well have evolved later, within the group. Hence, we cannot be sure about the developmental pattern of the two fossil larvae.