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Proceedings of the Tenth International Symposium on Neuropterology. Piran, Slovenia, 2008. Devetak, D., Lipovšek, S. & Arnett, A.E. (eds). Maribor, Slovenia, 2010. Pp. 153–158.

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Habitat and larvae of the enigmatic genus Kimochrysa Tjeder (: ) in South Africa

Peter Duelli1, Herbert Hölzel2 & Mervyn W. Mansell3 1Swiss Federal Research Institute WSL, Zürcherstr. 111, CH-8903 Birmensdorf/Zürich, Switzerland; E-mail: [email protected] 2Eppersdorf 1, A-9371 Brückl, Austria 3Dept. of Zoology and Entomology, University of Pretoria, Pretoria, South Africa

Abstract. Very few specimens of the three known Kimochrysa species endemic to the Western Cape Province of South Africa have been collected. Larvae and their habitats were unknown. We present photographs of the second and third instars of Kimochrysa africana (Kimmins), the host plants of their prey and the pollen-feeding adult. Relationships with the closest relatives among the subfamily Nothochrysinae are discussed. We postulate that the first chrysopid lacewings were small pollen feeders, followed by the much larger honeydew feeding genera of the Nothochrysinae.

Key words: Neuroptera, Chrysopidae, Nothochrysinae, pollen-feeders, relict distribution, rarity, isolation, South Africa

 Our dear colleague, Prof. Herbert Hölzel, passed away shortly before the Neuropterological Symposium in Piran.

Introduction

The genus Kimochrysa Tjeder comprises three species and is restricted to the Western Cape Province of South Africa (Tjeder, 1966; Mansell, 2005). It belongs to the subfamily Nothochrysinae, the oldest extant subfamily of the family Chrysopidae (Neuroptera). Bo Tjeder, who revised the genus Kimochrysa in 1966, wrote that all known fossil chrysopids were Nothochrysinae, or Dictyochrysinae as he called them at that time. Later, however, fossil species of the subfamily Chrysopinae were described from early Miocene Dominican amber (Engel & Grimaldi, 2007).

Todays world distribution of the subfamily Nothochrysinae is indeed relictual: Every continent has a few, mostly rare and very restricted species (Adams, 1967). In Africa, two genera have been found so far, completely isolated from the rest of the subfamily: Pamochrysa Tjeder and Kimochrysa, both restricted to small areas in South Africa. Only a few specimens of both sexes of Pamochrysa stellata Tjeder, from the type locality in the eastern Drakensberg area of KwaZulu-Natal are known. The larval stages of this monotypic genus are unknown.

Three species of Kimochrysa have been described, all from the Western Cape Province. Here also, the larval stages were unknown. Kimochrysa raphidioides Tjeder is known only from the female type specimen, collected around 1830 in the Cape area. Kimochrysa africana was described by Kimmins in 1937, based on two females collected in August north of Cape Town. Further specimens of this species were collected on flowers in the Cedarberg area in recent years (Mansell, unpubl.). The third species, K. impar Tjeder, is very special among chrysopids by having several subcostal crossveinlets in the proximal part of the wings, instead of one, as in all other extant chrysopid species (Tjeder, 1966). This species is known from two localities, one north and one southeast of Cape Town and only very few adult specimens have been collected, in March and April. So, finding the habitat of Kimochrysa was indeed a challenge.

ISBN 978-961-6657-16-7 © 2010 Faculty of Natural Sciences and Mathematics UM

Material and methods

The collecting trip lasted two weeks, from 26 September to 9 October 2004. We covered the northwestern part of the Western Cape Province, focussing on the Cedarberg area, from where the most recent observations of adult Kimochrysa, collected on yellow flowers, had been reported some 15 years ago. After checking numerous flowers for adult lacewings without success, larvae were eventually discovered by sweeping and beating the lower parts of Asteraceae. The larvae were kept singly in plastic vials and fed with aphids and other small, soft- bodied . Most larvae were close to pupation. Some pharate adults were placed in 99% Ethanol for genetic analysis. Photographs were taken of the food plants of the aphid prey. Based on these pictures, Peter Linder (Zürich, Switzerland), a specialist on the Cape flora, tentatively identified the plants to species level.

Results

Numerous larvae were collected on the first and second of October in just one area: Hoek-se-Berg Pass (S 32;07;04.9 / E 19; 10; 29.7; Fig. 1), at 650 metres altitude. They preyed on black aphids (unfortunately not collected) on yellow-flowering Asteraceae. Most larvae were found on Arctotis revoluta, along the roadside (Fig. 2). Further from the road, Euryops thunbergi and E. tenuissimus also harboured Kimochrysa larvae. The habitat is on a mountain pass that descends into the Biedou Valley. It lies in the Succulent Karoo Biome, in a vegetation unit classified as “Agter Sederberg Shrubland” (SKv3) by Rutherford & Mucina (2006). Vegetation and landscape features comprise low mountains and deeply incised valleys supporting tall shrublands composed of a mixture of non-succulent (Berkheya, Felicia, Pteronia) and succulent (Crassula, Euphorbia, Ruschia, Tylecodon) shrubs (Rutherford & Mucina, 2006). The host plants were mainly pioneer species, growing along the disturbed roadside.

The L2-larvae are pale green with some reddish traces. The L3-larvae (Fig. 3) turn greener with age and before pupation some of them are emerald green. The larvae are very similar to those of European Hypochrysa elegans (Burmeister), but they lack the conspicuous black median stripe on the head of the H. elegans larvae (Fig. 4).

The cocoon is not round as in most chrysopids, but has the shape of a barrel (Fig.5). It is greenish-grey, with a dark hoop around the middle. Interestingly, the cocoons of the genus Brinckochrysa appear very similar. At that time we did not know whether we had found Kimochrysa or not, so there was some concern that we had found the larvae of just another Brinkochrysa species.

Half of the resulting 18 cocoons were kept at room temperature and under a long day light-regime (L:D 16:8). The other half was changed after a month from warm (long day) to cold (short day) and a month later back to room temperature. But no emergence occurred for months. In the Cape area it was early spring when the larvae had been collected. The parent adults most probably flew in August, the month when the first K. africana adults had been collected more than half a century ago. The main flowering seasons in the Western Cape is from August to October, but there is a second one in March and April, when the type specimen of K. impar was found. So, would the adults from our cocoons emerge in the South African spring (after a year), or in autumn (after 6 months)?

The first adult emerged after 5 months (Fig. 6), and it was a female K. africana! Soon after that, most of the pupae started to emerge from the cocoon, but mostly failed during emergence or later in the mobile pharate stage. The final moult from the pupal exoskeleton turned out to be the crucial event, probably because the humidity during the long period of pupation or during eclosion was not adequate. But it is clear from the length of the pre-emergence period that the simulated winter conditions that we provided for half of the cocoons did not affect the rate of development leading to the emergence from the cocoon.

The single surviving adult readily fed on pollen of commercial yellow Asteraceae and lived for five weeks. After the two female type specimens of this species this is the third female, so the male of K. africana is still undescribed. Most larvae and the single adult are stored in the collection of P. Duelli, two larvae are in the collection of C. Tauber.

Discussion

From the fact that all adults at least tried to emerge after five months we assume that the species is bivoltine, i.e. having two generations per year. That makes sense, since there are two flowering seasons for Asteraceae in the Western Cape area, albeit not always very reliable. The observation that there was no significant difference in the pupation period between the cocoons kept under different light and temperature regimes either suggests that

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Fig. 1. Habitat of Kimochrysa africana at Hoek-se-Berg Pass, Cedarberg, Western Cape Province. Fig. 2. Arctotis revoluta (Asteraceae), food plant of the aphids Kimochrysa larvae prey on. Fig. 3. Third instar of Kimochrysa africana. Fig. 4. Third instar of Hypochrysa elegans (Sicily, Italy). Fig. 5. Barrel-shaped cocoon of Kimochrysa africana. Fig. 6. Female of Kimochrysa africana feeding on pollen.

it is, in strictly scientific terms, not a diapause but an obligatory dormancy (Danilevskii, 1965; Tauber et al., 1986) lasting about five months - or that the diapause-influencing environmental conditions are still unknown. Kimochrysa impar had been collected in March and April (Tjeder, 1966), which is the season when our K. africana emerged. We assume that K. impar also is bivoltine, but that by chance the two species had been collected in the two different flowering seasons.

With very rare and localized species there is always the question how they managed to survive for so long. Or have they been overlooked so far and are in fact more widespread and abundant? The closest relatives of the three apparently very rare and isolated Kimochrysa species among the pollen-feeding Nothochrysinae are also mostly very rare and isolated species, with the exception of the European Hypochrysa elegans (Burmeister).

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Fig. 7 shows the wings of the closest relatives of the three Kimochrysa species. Geographically the closest is Pamochrysa stellata in the Drakensberg area of KwaZulu-Natal, 1200 km northeast of the Kimochrysa habitats. But the wing venation pattern of Kimochrysa is much more similar to that of the European Hypochrysa, or even of the rare and locally occurring species of Pimachrysa in southwestern USA and Mexico (Adams, 1967). After the revisions of the Nothochrysinae by Tjeder (1966) and Adams (1967), another small pollen-feeding lacewing was found in northern Argentina and neighbouring Brasil (Adams & Penny, 1992). Asthenochrysa viridula was first described by Adams (1978) as Hypochrysa, because the wing venations are so similar.

Fig. 7. Wing shape and venation of Hypochrysa elegans (Europe), Kimochrysa africana (South Africa, WCP), Pamochrysa stellata (South Africa, KwaZulu Natal) and Pimachrysa sp. (Southwestern USA). Wing pictures copied from Brooks & Barnard (1990).

While closely resembling each other, these small nothochrysine pollen-feeders appear quite different from the rest of the Nothochrysinae. Furthermore, the rather large and Dictyochrysa species are mainly honeydew-feeders.

Some of the unsuccessful pharate adults of Kimochrysa africana from Hoek-se-Berg were placed in absolute alcohol before dying and processed for genetic analyses (Haruyama et al., 2008). The position of Kimochrysa africana, shown at the top in the phylogram (Fig. 8), is separated from all other genera of Chrysopidae, analysed on the basis of three nuclear genes. In this first genetic attempt to place Kimochrysa in the chrysopid phylogeny, the larger Nothochrysinae such as Nothochrysa appear to be more closely related to the subfamily Apochrysinae than to Kimochrysa africana. Adams (1967), in his revision of the Mesochrysinae (fossil) and Nothochrysinae, found several wing venation characters that suggest the genus Nothochrysa to be closer to the Apochrysinae and Chrysopinae than the small pollen-feeding nothochrysine species.

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Fig. 8. Part of the genetic phylogram for the family Chrysopidae, adapted from Haruyama et al. (2008). Only the subfamilies considered the most ancient are shown, leaving out the bulk of chrysopid lacewings of the specious tribe Chrysopini. The diagram highlights the isolated position of Kimochrysa africana within the family Chrysopidae.

In spite of very preliminary genetic evidence, but in accordance with the difference in the wing pattern, size, and feeding habits, we tentatively consider the small pollen-feeding nothochrysine species as a very particular guild, probably the most ancient chrysopid group of lacewings in the world. This would imply that pollen feeding might have been the original feeding habit of the first Chrysopidae. The females searched for flowers with pollen and by doing this deposited their eggs in places with a fair probability for aphid infestations. Later, the more advanced Nothochrysinae started to feed on the honeydew of aphids and other homopteran . The smell or taste of honeydew is a much more reliable clue for the presence of aphids, and so the female lacewings advanced to depositing their eggs in the vicinity of sources of honeydew (Hagen et al., 1976; Duelli, 1987). However, the old habit of pollen feeding is still present in Nothochrysa californica Banks, which according to Toschi (1965) will not mate until after feeding on oak pollen.

The disjunct and very local distribution of relict species is world-wide a strong argument for their conservation. In industrialized countries many butterfly and beetle species are put on the national red lists of rare and threatened species, although they are still abundant in neighbouring countries or may have close relatives which are not threatened at all. Compared to those species, the isolated pollen-feeding relictual Nothochrysinae deserve a special level of attention and protection.

Acknowledgements. We thank Tony Brinkman for his help with field-work and Peter Linder for the identification of photographed Asteraceae. Cape Nature is thanked for providing collecting permits, issued in the name of the third author. Catherine Tauber, as a reviewer, gave valuable suggestions to improve the manuscript.

References

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Adams, P.A. & Penny, N.D. 1992. New genera of Nothochrysinae from South America. Pan-Pacific Entomologist, 68 (3): 216–221.

Brooks, S.J. & Barnard, P.C. 1990. The green lacewings of the world: A generic review (Neuroptera: Chrysopidae). Bulletin of the British Museum of Natural History (Entomology), 59(2): 117–286.

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Bibliography of the Neuropterida

Bibliography of the Neuropterida Reference number (r#): 13644

Reference Citation: Duelli, P.; Hölzel, H.; Mansell, M. W. 2010 [2010.11.25]. Habitat and larvae of the enigmatic genus Kimochrysa Tjeder (Neuroptera: Chrysopidae) in South Africa. Pp. 153- 158 in Devetak, D.; Lipovšek, S.; Arnett, A. E. (eds.). Proceedings of the 10th International Symposium on Neuropterology (22-25 June 2008, Piran, Slovenia). University of Maribor, Maribor, Slovenia. 307 pp.

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