REVIEW Eur.1. Entomol. 102: 317-324, 2005 ISSN 1210-5759

Seasonal adaptations of green lacewings (Neuroptera: Chrysopidae)

MICHEL CANARD

47 chemin Flou de Rious, F-31400 Toulouse, France; e-mail: [email protected]

Key words. Chrysopidae, green lacewing, seasonal adaptation, diapause, voltinism, overwintering, eycle synchronization, wintering chambers

Abstract. Seasonal adaptations of green lacewings (Neuroptera: Chrysopidae) and their role in the control of aphid populations are discussed. The chrysopids of temperate zones face seasonal changes and must escape cyclic adversity. One way is via the number of broods per year. Most green lacewings are facultatively multivoltine, with the succession of generations most often regulated by photomediated diapause. Others are univoltine and some extend their life-cycle to two years in cold or dry environments. Synchroni­ zation is an important feature of seasonality, often starting in spring. In univoltine species, it is sometimes the result of subtle mecha­ nisms, such as double contradictory signals (short plus long day lengths) for reactivation in spring, or a multi-receptivity of the preimaginal instars to photoperiod throughout a year, combined with photo-controlled and synchronized egg laying in late summer. Only one North American species is known to enter a surnumerary food-mediated diapause in summer. Every postembryonic instar may undergo diapause depending on the species. The timing and impact of the spring resumption in aphid consumption depends on their overwintering strategy. As far is known, chrysopids are intolerant of freezing, but their supercooling points are low enough to enable them to endure hard frost. The numbers of overwintering specimens of green lacewings in the field depend on the structure of the as~emblages in the pre­ vious growing season. Three examples are used to show that the overwintering populations are difIerent in the different biotopes and dependent on the way the dominant species overwinter. Artificial chambers proposed for overwintering adults of common green lacewings afford them protection during diapause and enhance their predatory efficiency in spring.

INTRODUCTION any lacewing in the southern hemisphere. The quite well­ studied Westpalaearctic Region harbours about 121 spe­ Organisms living at the higher latitudes are regularly cies of chrysopids (Aspock et aI., 2001), 67 of them occur confronted with seasonal changes in climate (cold/hot or in Europe; in the Nearctic Region, 82 species are dry/wet), which are more or less rigorously adverse and recorded in North America, excluding Mexico (Penny et result in the evolution of strategies for escaping this aI., 1997, 2000). It is mainly by studying these species cyclic adversity. In arthropods, diapause and/or migration that we can understand the mechanisms by which they may offer ways of doing this. As far is known, survive and efficiently colonize the available biotopes Chrysopidae only use diapause. True n1igration (sensu every year. Here their impact on the control of aphid out­ Kennedy, 1975) may occur, but only, as far is known, in breaks will be assessed rather than the physiological Chrysoperla cqrnea (Stephens, 1836), the so-called mechanisms by which this is achieved. "common green lacewing", which obligatorily flies down-wind on the firsttwo nights after emergence, what­ VOLTINISM ever the generation (Duelli, 2001). A con11llonly encountered method of adjusting annua1 WHICH SPECIES OF GREEN LACEWING ARE cycle is the number of broods per year, i.e. univoltinislll INVOLVED? vs multivoltinism, which affects the impact these preda­ tors have on aphids. Responses are variable and not About 1200 species of Chrysopidae are described dependent only on the latitudinal occunence of a species. (Brooks & Barnard, 1990). Most are inhabitants of the For example, Ceraeochrysa placita (Banks, 1908), tropical and equatorial zones and display homodynamic reported from Canada to Mexico, does not enter dor­ development. They do not experience a seasonal alterna­ mancy in order to survive winter in the southern part of tion of favourable and adverse clin1atic and trophic condi­ its range; nevertheless, it is always univoltine (Tauber et tions. This is the case for instance in the Afrotropical aI., 1998). Mallada desjardinsi (Navas, 1911) (Brettell, 1979) and Other species have lllore varied patterns of vo ltinism, the Neotropical Chrysoperla externa (Hagen, 1861) such as the stenotopic Chrysopa phyllochroma Wesmael, (Macedo ct aI., 2003). In Ceraeochrysa cincta 1841 and Chrysopa dasyptera McLachlan, 1872, which (Schneider, 1851), C. cubana (Hagen, 1861) and C. are univoltine in Central Europe according to Zeleny smithi (Navas, 1914), diapause was not observed even at (1965, 1984); but Ch. phyllochroma may have two gen­ 30 0 N in Florida and Texas, nor induced experimentally in erations a year in western Europe (Trouve et aI., 2002) the laboratory (Lopez-Anoyo et aI., 1999). and Ch. dasyptera has two generations a year in the Green lacewings in the Holarctic Region show adapta­ Middle Volga Region in Russia (52-54°N) (Kovrigina, tions to the seasonal changes; diapause is not recorded for

317 1990). In the case of facultative uni/multivoltinism, some Little is known about the physiological mechanism of individuals of a species mostly only show a slight their cold hardiness, but cryoprotection in Neuropterida response depending on their place of origin, as in probably does not differ from that in other insects. In Chrysopa abbreviata Curtis, 1834, in Italy (Pantaleoni, overwintering cocoons of Chlysopa "walkeri McLachlan, 1982). Nevertheless, most green lacewings exhibit facul­ 1893, carbohydrate analysis shows glycogen and treha­ tative multivoltine cycles with the number of broods per lose as the major stored elements. The glycogen level was year a direct function of the climatic and trophic condi­ consistantly higher than that of trehalose, whilst polyol tions. levels were low or undetectable (Sagne et ai., 1986). Some species manifest a tendency to prolong and n1ain­ Overwintering adults of Chrysoperla affinis (Stephens, tain diapause for more than one year and so have a two­ 1836) [Chrysoperla kolthoffi (Navas, 1927)] showed a year cycle. This precaution against unfavourable strong decrease in total lipid content at the beginning and environmental conditions is adopted in northern, cold at the end of winter reproductive diapause; the percentage countries, e.g. by Chrysopa dorsalis Burmeister, 1839, in of phospholipids increased significantly during post­ Russia (Volkovich, 1998), and in xerothermic conditions, diapause, while that of glycerids decreased, especially in e.g. by the Iberian C~hrysopa regalis Navas, 1915 females (Lemesle et aL, 1998). (Canard, 1986a). This particular adaptation involves spe­ WHICH INSTARS OVERWINTER? cies diapausing as prepupa within a cocoon, since this is the only stage able to provide protection against dehydra­ In all species of green lacewings there is one, SOIne­ tion and weight loss (Canard et aI., 1996). times two, developmental stages which are able to survive adverse winter conditions, namely frost and scarcity, if CUES REGULATING VOL TINISM not total lack, of prey. In the family Chrysopidae, When "obligatory" (i.e. always Inanifested in natural depending on the species, all stages except the embryo, conditions) univoltinism is a totally innate function, can overwinter. Thirty nine of th~ 67 species in Europe genetically mediated (Tauber & Tauber, 1981; Tauber et and 17 North American species o'verwinter as a prepupa aI., 1986). On the other hand, as in most arthropods within a cocoon (Table 1). exhibiting facultative multivoltinisIn, photoperiod is the OVERWINTERING OF FIELD POPULATIONS IN main factor regulating the cycle, more or less tnodulated DIFFERENT BIOTOPES by temperature and/or thermoperiod, as in Dichochrysa flav~rrons (Brauer, 1850) (Principi et aI., 1990), Chrysopa Aphid control is often determined early in a growing pallens (Rambur, 1838) (Orlova, 1998) and Dichochrysa season, because if the aphid fundatrices encounter an prasina (Burmeister, 1839) (Volkovich, 1998) in northern abundance of natural enemies when they colonize plants, Russia. the resulting colonies are less numerous and when estab­ lished, less crowded. Early occurrence of predators is a ARE GREEN LACEWINGS FROST TOLERANT? key factor in efficient aphid management. Whether uni- or multivoltine, chrysopids in ten1perate The tiine of resumption of predatory activity by green climates experience low temperature in winter. There is lacewings depends on thei r overwintering strategy, which little information on the ability of green lacewings to determines their impact on aphid abundance (Fig. I). resist cold. The available data indicate a good hardiness - If they overwinter as partly grown larvae as in to frost even if the green lacewings are unbiased frost Dichochrysa spp., they start feeding on prey immediately; intolerant. - if they overwinter as prepupae within a cocoon, the Prepupae of Chrysopa perla (Linnaeus, 1758) on the first contact between the predator and the prey is delayed sixth month of diapause are unable to survive 3 days at until the adults emerge if they are predacious, as in -17°C, but can survive -6°C (Sagne & Canard, 1984). Chlysopa spp.; Overwintering adults of the common green lacewings in - if they overwinter as adults, the impact on prey is NOlih America survived well (97%) 31 weeks at 5°C delayed until reproduction ( ovogenesis, mating) + when in a diapause-inducing photoperiod (Tauber et ai., embryogenesis are complete, as in the common Chrysop­ 1993). This is better than expected, based on their thermal erla spp., thresholds of development, which are estimated to be or even much more longer, if they overwinter as a 11-12 or 8-9°C in Chrysopa perla originating froin prepupa which gives rise to a parental spring generation western Europe (Canard & Principi, 1984) and Central of adults having palyno-glycophagous habits, as is the Russia (Volkovich, 1998), respectively, and about 10°C case in Nineta, Chrysotropia and Cunctochrysa spp. in northeastern European strains of common green lace­ The abundance and stages of green lacewings that wings (Volkovich, 1998). The supercooling point (SCP) resun1e predatory activity in spring in a biotope are a of common green lacewings is -12.6°C in September, function of the structure of the chrysopid populations pre­ -17.3°C in November and -6.5°C in April in France sent the previous year. Three examples of chrysopid (Vannier, 1986, 1987). The diapausing young larvae of assen1blages (Thierry et ai., in press) that differ in the per­ Nineta pallida (Schneider, ] 846) have a SCP of -25°C in centages of species that overwinter as larvae, prepupae first instal' ex-ovo and -17.9°C during winter (Vannier & and adults, which is relevant to their spring occurrence Canard, 1989; Canard & Vannier, 1992). (Table 2).

318 TABLE 1. Overwintering stages of some Holarctic chrysopids. The first biotope is typical of an agro-ecosystem influ­ 1st 2nd/ Pre· Species Pupa Imago enced by the Atlantic. This study was carried out at instar 3rd pupa Loos-en-Gohelle, in the southern French part of the Flan­ European: ders Plain, Pas-de-Calais, France (50 0 27'N, 02°47'E). It No thoeh rys a fulvieeps * is an agricultural area with a long tradition of vegetable Nothoehrysa capitata * and fruit production. The fields are of commercial type, Hypoehrysa elegans * ltalochrysa italiea * all managed using soft cultural techniques, either inte­ Nineta jlava * grated or strictly organic farming methods. Several crops: Nineta vittata * strawberry, potato, witloof, tobacco and kidney-bean and Nineta guadarramensis * adjacent uncultivated biotopes were sampled. Nineta palIida * This agro-environment had the poorest biocenotic rich­ Chrysotropia ciliata * ness (Margalefs index) and low indices of both diversity Chrysopa perla * (Shannon) and equitability (Hurlbert) (Table 2). The Chlysopa walkeri * single dominant species, Chrysoperla afjinis, made up Chrysopa dorsalis * more than 2/3 of the overwintering (and spring?) popula­ Chrysopa regalis * Chrysopa hungariea * tion. In such conditions, a good survival of adults over Chrysopa abbreviata * winter is a key factor. The protection against unfavour­ Ch,:vsopa formosa * able climatic factors, such as humidity and predatory spi­ Chrysopa phyllochroma * ders, can be improved (McEwen & Sengonca, 200 I ). Chlysopa eommata * Adequate food for adults, before and after diapause, is Chrysopa viridana * necessary to initiate diapause satisfactorily and later Chrysopa nigricostata * stilTIulate reproductive activity (Alrouechdi, 1982). What­ Chrysopa pallens * ever help is supplied to the overwintering population of Diehoehrysa jlavifrons * chrysopids, it will only have a slow and late affect on Diehoehrysa pieteti * Diehochrysa iberica * spring aphid colonization. Diehochrysa prasina * The second biotope is a continental mountain, mon­ Dichochrysa zelleri * tane spruce acidophilous forest (Code Natura 2000: Dichoehrysa ventralis * 94.10), subalpine picea zone (Code Natura 2000: 42.21). Diehochrysa clathrata * The site is located in the Transylvanian Alps, near Sinaia, Peyerimhoffina gracilis * about 110 km north-west of Bucharest and 60 km south Chrysoperla carnea * of Brasov, Romania (45°21 'N, 25°33'E), at an altitude of Chrysoperla affinis * 810m, near to two small brooks in the Prahova valley. Chrysoperla agilis * The vegetation comprises an arboreal canopy of Fagus Chrysoperla lucas ina * Chrysoperla sylvatica and the conifers Picea excelsa, Abies alba and mediterranea * Pinus silvestris, associated with diversity of shnlbs such Chrysoperla mutata * as Alnus incana and an herbaceous ground cover typical Rexa lordina * of forest glades. Cunetoehrysa This spontaneous altitudinal forest has the highest bio­ albolineata * cenotic richness, but a moderate diversity (Table 2), due ;.'" Cunetoehrysa baetica * to the strong dominance of the facultatively bivoltine North American: Cunctochrysa albolineata (Killington, 1935), which is Ceraeoehrysa placita * palyno-glycophagous in the adult stage. Mortality of the Chrysopa nigrieornis * diapausing prepupae in cocoons during winter is mainly Chrysopa oeulata * Chrysopa due to predation by small rodents and shrews within the quadripunetata * litter, entomopathogenic fungi and also possibly pro­ Chrysopa slossonae * longed immersion (Sagne & Canard, 1984) in poorly Chrysopa timberlakei * drained soils. The resumption of predation of aphids by Chrysoperla adamsi * chrysopids is expected to be late, but may be marked Chrysoperla downesi * when most of the larvae of the dominant chrysopid spe­ Chrysoperla johnsoni * cies reach the third stage. Chrysoperla mohave * The third example is typical of thermo-Mediterranean Chrysoperla plorabunda * biotope. It is a spontaneous pine forest (Code Natura Meleoma dolicharthra * 2000: 95.40), in the Aleppo pine sub-zone (Code Natura Meleoma emuncta * Meleoma hageni * 2000: 42.84). It is situated at an altitude of about 100 m, Meleoma kennethi * in southwestern France, near Fontcouverte, in the Cor­ Meleoma schwarzi *? bieres, Aude, France (43°10'N, 02°35'E). The soil is cal­ Meleoma 1;!1al~'nrOTT1 * careous, arid and stony. The arboreal vegetation Total 1 10 31 1 12 comprises Pinus halepensis, Quercus ilex and Cupressus % 58 sempervirens, and the shrub layer is composed of Buxus

319 overwintering as

i+:13 ...... L ______'-o I ..... ~

i fj!~ ~ \\\~ ...... I " __ I --- ..... , I ' l~l ~ )\\ ~ I \ I \\ I \ ®i'iJ ~ ~ )\, ...... ,..... time

Fig. 1. Delay in the resu111ption of aphidophagous activity shown by green lacewings as a function of theu' overwintering strategy. sempervirens, Quercus coccifera and Cistus spp. The her­ rikova, 1979) or under the bark of trees; they are often baceous cover is irregular and essentially composed of difficult to detect as they move little and are covered with the Mediterranean indicatory grass Brachypodium ramo­ debris. sum. The cocoons harbouring diapausing prepupae are This arid and dry biotope is the most well-balanced of thought to stay in the litter or remain hidden underground. the three biotopes, and has a high richness, diversity and In the laboratory, all the full-grown third instar larvae of equitability (Table 2). Probably the most common instars Chrysopa perla crawl down into a srnall cavity in a dry overwintering are larvae. Mortality is due to generalist and light substrate before weaving a cocoon; those that insectivores and a lack of suitable refuges. Their obliga­ enter diapause hide themselves more than those that tory need to feed when the temperature reaches the undergo on uninterrupted development (Canard & Pnl­ thermal activity threshold means that starvation may also dent, 1979). There is little information on the overwin­ be a limiting factor. The pressure on live prey in such bio­ tering sites of other species, as cocoons are very rarely topes, experiencing mild winter temperatures, is sel11i­ found in the field. Aggregations of cocoons of Chrysopa permanent and so consistent control of aphids (or other pallens are sOlnetimes observed in the sawdust that accu­ prey) is expected. mulates from pruning branches of Robinia trees in urban areas. OVERWINTERING REFUGES Overwintering by adults is the most usual for the com­ Litle is known about actual overwintering sites of nlonest green lacewings \vhich many people think is the chrysopids. When larvae overwinter, they possibly do so only way of overwintering in the Chrysopidae. Such a on host plants, like the young naked larvae of Nineta pal­ generalisation is possible because of the dominance of !ida (Canard, 1985). But others, such as Dichochrysa common green lacewings in agroecosystems and their spp., remain in low growing herbage or leaf litter (Bab- dependance on man made structures (e.g. Gepp, 1967):

TABLE 2. Number of species and percentage of specimens of chtysopids overwintering in three typical biotopes. Percentages are ------those of the actual structure of relevant lacewing assemblages. number richness diversity equitability No. species overwintering as % specimens ovenvintering as zone and biotope of species index index index larva prepupa tmago larva prepupa Imago atlantic: vegetable crops 5 0.92 0.8 0.4 3 28 71 dominant species Ch. affinis 12 continental: montane forest 17 2.65 1.52 0.49 3 C. albo­ 2 3 82 15 dominant species lineata mediterranean: spontaneous 6 13 1.94 1.95 0.74 5 2 55 5 40 dominant species D. iberica

320 TABLE 3. Ground colour of the body of some Chrysoperla spp. Place species summer colour winter colour Europe q[finis green brown agilis pale green mixed carnea pale green mixed lucasina green mediterranea dark green North America adamsi green mixed downesi dark green johnsoni bright green mohave yellow green yellow plorabunda green brown Middle East and North Africa sillemi pale green mixed for a long time, the best and sale retreats were considered chromo-mimetic adaptation to particular overwintering to be unheated parts of country houses, stables, barns and sites (Duelli, 1992; Henry et aI., 2001). similar structures. Of course, other overwintering sites are YEARL Y SYNCHRONIZATION available in the field, including rolled dead leaves, litter, underside of bark, abandonned wasp nests ... in all cases For insects, synchronization of development with the dry and dark places. After the sibling species of the seasons is important. Although the factors that inhibit carnea complex were recognized, it was demonstrated in development have been the object of many studies, the central France that they each have a different and specific synchronization mechanisms are often neglected (Hodek, overwintering strategy (Thierry et aI., 1994). ChrysoperZa 2002) despite their being the rnain factor determining the affinis is the only species found indoors in winter, but successful termination of diapause. also in bushes at the end of spring. Chrysoperla lucas ina Multivoltine cycle (Lacroix, 1912) shelters in evergreen plants, such as ivy and cherry-laurel bushes, whilst ChrysoperZa carnea The regulation of multivoltinism is relatively simple. sensu stricto is more thigmotactic and prefers dry rolled The primary control is· via photoperiod during develop­ leaves that remain on trees or on the branches of under­ ment. Later, re-activation or deactivation of morpho­ story bushes. genesis is regulated by (low) temperature as in several European Chrysopa spp. (Principi & Castellari, 1970): IS IT POSSIBLE TO PROTECT OVERWINTERING thus, Ch. perla in which low temperature detennines the ADULTS OF CHRYSOPERLA SPP.? timing of the annual cycle and the synchronization of the We know both the sites used by ovenvintering adults sympatric uni- and multivoltine strains (Gepp, 1975). and that the main cause of death is predators and diseases. However, the completion of diapause may sometimes be This is why biocontrol progranlmes try to enhance sur­ spontaneous, so that after a period of thennal quiescence, vival. To the best of our knowledge, the Chinese were the the resumption of development is initiated by temperature first to provide ,artificial shelters for Chrysoperla nippo­ reaching the thennal threshold for activity, as in nensis (Okamoto, 1914) (Wang et aI., 1987). Later, suc­ Chrysopa oculata Say, 1849, (Propp et aI., 1969). In cessively Sengonca, McEwen (see review in McEwen & some cases, more subtle mechanisms may optimize the Sengonca, 2001), <::aldumbide et a1. (2002) and Thierry et spring emergence. Thus, Dichochrysa picteti a1. (2002) provided more infonnation on the Palaearctic (McLachlan, 1880) overwinters as active third or younger comnl0n green lacewings and suggest ways of improving instar larvae, depending on the date on which they hatch the overwintering chambers. These are only attractive to in autumn (Canard et aI., 1992). The photoperiod induces Chrysoperla affinis, the commonest species in the crops a more or less intense slowing down of development: in temperate climates. Supplementary feeding before medium day lengths (early autumn) result in the longest storage and after the temperature rise in spring is crucial diapause, short day lengths (late autumn) the shortest dia­ for initiating diapause (Alrouechdi, 1982) and the pause. The marked variability in the different larval resumption of reproductive activity. stages present in autumn is reduced or even disappears in spring (Canard, 2001). SEASONAL POL VPHENISM: CHANGE IN ADULT COLOUR Univoltine cycle To be univoltine and synchronize one's life cycle is not Colour changes shown by overwintering adults of easy to achieve. Adjusting univoltinism may be easy if Chrysoperla spp. were for a long time considered to be dependent on a single climatic factor. The North­ obligatory, associated with diapause and subject to varia­ American Meleoma signoretti Fitch, 1856, as far is tion (see e.g. MacLeod, 1967; Tauber et aI., 1970; Honek, known, responds to a simple signal: the diapausing pre­ 1973). This now needs to be reappraised bearing in mind pupa is re-activated only by long days (Tauber & Tauber, the diversity of species in this complex, as winter colour 1975). But the annual cycle of other univoltine species may be a Ineans of recognizing sibling species (Table 3). may be synchronized by more complicated cues with pos­ The ground body colour of overwintering adults is a sibly two consecutive periods of diapause development

321 because the photoperiod response is not irreversibly lost desert-inhabiting species, which is surprisingly also pre­ by (a first) diapause completion in multireceptive insects dacious as an adult, unlike (? all) other Chrysoperla spp. (Hodek, 1999). The examples given below attest to such In this green lacewing, as in most of the genus, diapause complexity. in the overwintering adults is induced by photoperiod. At the end of pre imaginal development, the strictly However, it also manifests a facultative reproductive dia­ univoltine American Chrysoperla downesi (Smith, 1932) pause (aestivation) , which is induced when starved under requires a sequence of short day lengths followed by a long day conditions, and terminated when prey become sequence of long day lengths to initiate ovarian matura­ available (Tauber & Tauber, 1973). tion and so avert diapause. In the field, it overwinters as ACKNOWLEDGEMENTS. Deep-felt thanks are due to T. an adult until the natural photoperiod is long enough to Volkovich (St. Petersburg, Russia) for pertinent comments on re-activate reproduction (Tauber & Tauber, 1976). The the manuscript and to both A. Whittington (Edinburgh, larvae of the European Peyerimhoffina gracilis (Schnei­ Scotland, UK) and an anonymous reviewer for improving and der, 1851) are photo-insensitive unlike the pupae and the checking the English. imagos. The same double exposure to short- followed by long day lengths is needed to stimulate reproductive REFERENCES activity. In the field, they enter and remain in diapause ALROUECHDI K. 1982: Bioecologie de Chrysoperla carnea (Ste­ until spring (Grimal, 1988). Peyerimhoffina gracilis is phens) (Neuroptera: Chrysopidae). Son Impact Entomophage commonly univoltine, however, early egg laying in spring en Vergers d'Oliviers. 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323 generic characteristics of larvae, larval descriptions, and life TROUVE C., THIERRY D. & CANARD M. 2002: Preliminary survey cycle. Ann. Entomo!. Soc. Am. 91: 608-618. of the lacewings (Neuroptera: Chrysopidae, Hemerobiidae) in TAUBER M.J. & TAUBER C.A. 1973: Nutritional and photoperi­ agroecosystems in northern France, with phenological notes. odic control of the seasonal reproductive cycle in Chrysopa Acta Zool. Acad. Sci. Hung. (Suppl. 2) 48: 359-369. mohave (Neuroptera). J. Insect Physiol. 19: 729-736. VANNIER G. 1986: Accroissement de la capacite de surfusion TAUBER M.J. & TAUBER C.A. 1975: Natural daylengths regulate chez les adultes de Chrysopeda carnea (Insectes: insect seasonality by two mechanisms. Nature 258: 711---712. Nevropteres) entrant en diapause hivernale. Neurapt. Intern. TAUBER M.J. & TAUBER C.A. 1976: Developmental requirements 4: 71-82. of the univoltine species Chrysopa downesi: photoperiodic VANNIER G. 1987: Diminution de la capacite de surfusion chez stimuli and sensitive stages. 1. Insect Physiol. 22: 331-335. les adultes de Chrysopeda carnea (Insectes: Nevropteres) au TAUBER MJ., TAUBER C.A. & DENYS CJ. 1970: Adult diapause cours de la diapause hivema1e. Neuropt. Intern. 4; 211-219. in Chrysopa carnea: photoperiodic control of duration and VANNIER G. & CANARD M. 1989: Cold hardiness and heat toler­ colour. J. Insect Physiol. 16: 949-955. ance in the early larval instar of Nineta pallida (Schneider) TAUBER MJ., TAUBER C.A. & MASAKI S. 1986: Seasonal Adapta­ (Neuroptera: Chrysopidae) Neuropt. Intern. 5: 231-238. tions of Insects. Oxford University Press, New York, USA, VOLKOVICH T.A. 1998: Environmental control of seasonal cycles 411 pp. in green lacewings (N europtera: Chrysopidae) from the TAUBER M.J., TAUBER C.A. & GARDESCU S. 1993: Prolonged forest-steppe zone of Russia. Acta Zool. Fenn. 209: 263-275. storage of Chrysopeda carnea (Neuroptera: Chrysopidae). WANG R., ZHOU W.R. & QlU S.B. 1987: [Augmentation of Envir. Entoma!. 22: 843~848. Chrysopcrla sinica: storing overwintering adults for early THIERRY D., CLOUPEAU R. & JARRY M. 1994; Variations in the spring release.] Chin. J. Biol. Contr. 3(2): 55-60 (in Chinese, overwintering ecophysiological traits in the common green English abstr.), abstract in Rev. App!. Entomo!' 76: 7526. lacewing West-Palaearctic complex (Neuroptera: Chrysopi­ ZELENY 1. 1965 : Lace-wings (N europtera) in cultural steppe and dae). Acta Gecol. 15: 593--·--606. the population dynamics in the species Chrysopa carnea Ste­ THIERRY D., RAT-MORRIS E. & <;ALOUMBIDE C. 2002: Selective phens and Chrysopa phyllochroma Wesmael. Acta Entomo!. attractivity of artificial overwintering chambers for the Bohemoslov. 62: 177-194. common green lacewing species of the Chrysopeda carnea ZELENY 1. 1984: Chrysopid occurrence in West Palaearctic tem­ (Stephens) complex in Western Europe (Neuroptera: perate forests and derived biotopes. In Canard M., Semeria Y. Chrysopidae). Acta Zool. Acad. Sci. Hung. (Suppl. 2) 48: & New T.R. (eds): Biology ofChlysopidae. Dr W. Junk Pub­ 351-357. lishers, The Hague",The Netherlands, Series Entomologica THIERRY D., DEUTSCH B., PAULIAN M., VILLENAVE 1. & CANARD 27: 152-160. M.: Quantifying biodiversity in eGosystems by green lac~­ wing assemblages. A method of assessment and typifying Received September 9,2004; revised and accepted February 22,2005 ecological landscapes. Agron. Sustain. Devel. (in press).

324 Bibliography of the Neuropterida

Bibliography of the Neuropterida Reference number (r#): 11663

Reference Citation: Canard, M. 2005 [2005.??.??]. Seasonal adaptations of green lacewings (Neuroptera: Chrysopidae). European Journal of Entomology 102:317-324.

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File: File produced for the Bibliography of the Neuropterida (BotN) component of the Lacewing Digital Library (LDL) Project, 2012.