Trends in Entomology Vol. 12, 2016

The feeding biology of adult lacewings (): a review

Dušan Devetak* and Vesna Klokočovnik Department of Biology and Institute of Biology, Ecology and Nature Conservation, Faculty of Natural Sciences and Mathematics, Koroška cesta 160, 2000 Maribor, Slovenia.

ABSTRACT Theoretical and practical aspects of Neuroptera, especially the green lacewings within (green lacewings), which are one of the largest this , are generally considered as major lacewing families, have been well studied in the components of beneficial entomofauna in context of their use in crop protection [6, 7]. Some agroecosystems. A review of the knowledge on neuropteran adults have glycophagous diets that the feeding habits of adults in the order Neuroptera include sugar-rich foods such as , plant is presented, based on data from the literature. Of fluids and honeydew. the 16 neuropteran families, feeding habits in the Microscopic analysis of the intestinal contents in adults have been documented for 13. A diversity adult lacewings revealed six types of feeding of feeding habits influences the functional strategies (Table 1): morphology of the mouthparts and the structure of the digestive tract. A list of relevant literature is - Carnivorous: (only one also provided. investigated!), , , and most Myrmeleontidae; KEYWORDS: lacewings, Neuroptera, integrated - Omnivorous: , , most management, feeding, predator, , , and some Chrysopidae (at least , phylloxerids, some species of the );

INTRODUCTION - Carnivorous-glycophagous: ; The lacewings (order Neuroptera) are one of the - Glycophagous (sometimes called smaller orders of holometabolous , containing glycinophagous): most Chrysopidae; about 6,000 known species distributed among - Palyno-glycophagous (sometimes called sixteen families (Table 1). Adults and larvae of pollino-glycinophagous): some Chrysopidae most families are predaceous. Within Neuroptera, (genus and three predaceous families, namely Chrysopidae, prasinus), and Crocidae; Hemerobiidae and Coniopterygidae are potentially - Palynophagous (sometimes called the most important in integrated pest management pollinophagous): some Berothidae (Nyrma and and organic farming [1, 2, 3, 4]. Dusty wings Berothimerobius), a few Myrmeleontidae (e.g. (Coniopterygidae) are indeed important predators yavapai) and some Chrysopidae but usually overlooked because of their small size (the Nothochrysinae ). [5]. Brown lacewings (Hemerobiidae) are used in pest management in several parts of the world. The aim of this paper is to provide a review of the feeding strategies in adult lacewings and to encourage further study and manipulation of this *Corresponding author: [email protected] order in future from a holistic perspective.

30 Dušan Devetak & Vesna Klokočovnik

Table 1. Feeding habits in adults in the extant families of Neuroptera. Suborder/ Feeding habit Key references/reviews

Suborder Nevrorthiformia

Family unknown (fungal spores?) [14]

Suborder Family Ithonidae carnivorous [17] Family Osmylidae omnivorous [19, 45] glycophagous; palyno-glycophagous; Family Chrysopidae [4, 19, 29, 32] palynophagous; omnivorous Family Hemerobiidae omnivorous [4, 19] Family Sisyridae carnivorous-glycophagous [14, 19, 45] Family Coniopterygidae carnivorous [4, 19] Family unknown [53] Family Mantispidae carnivorous [55, 56] Family Berothidae omnivorous; palynophagous [61] Suborder

Family unknown (carnivorous?) [63, 64]

Family Nemopteridae palyno-glycophagous [67]

Family Crocidae palyno-glycophagous [69, 70]

Family carnivorous [72] Family Myrmeleontidae carnivorous; palynophagous [8, 75] Family Ascalaphidae carnivorous [19]

Additionally, we present a few original findings digestive tract of adult Osmylus fulvicephalus of the diet in some species. algae, lepidopteran scales and scattered pollen grains are occasionally observed. A possible explanation A review of the methods for studying intestinal for this observation could be that Osmylus adults contents probably scrape off honeydew spread on twigs A simple method for studying intestinal contents and plant surfaces [10] and swallow the in adult Neuroptera is dissection and mounting of honeydew along with small particles, which may the alimentary tract on glass slides and microscopic get stuck on the sticky plant surface. inspection of food remains. An alternative method Various molecular methods have been developed for studying intestinal contents is inspection of in recent decades for gut analysis of Neuroptera. feces [8]. Sometimes insect bristles are found in A technique using PCR (polymerase chain the digestive tract, which are derived from the reaction) for identifying a definite prey species insect’s own integument as a result of grooming. (Ips typographus) was used in green lacewing larvae Insect bristles or even antennal fragments are [11]. This method seemed to be very helpful in sometimes found in the gut of adult green lacewings the detection of Bremisia tabaci remains even in sensu lato that are not the guts of adult green lacewing predators, when a predators. This finding can be interpreted as the sequence-characterized amplified region marker result of self-grooming by the insect [9]. In the was used [12].

Feeding biology of adult lacewings 31

Feeding habits in adults Family: Chrysopidae, green lacewings Suborder: Nevrorthiformia More information has been published on Chrysopidae than on any other family of Neuroptera, thanks to Family: Nevrorthidae their role as predators of pest . Principi Malicky [13] often observed adult nevrorthids on [23, 24] was one of the first to have studied the sticky and assumed that they fed on feeding habits of adult green lacewings by honeydew. Monserrat [14] reported the presence microscopic analysis of the intestinal contents in of a significant quantity of fungal spores in the dissected insects. In the seventies, Hagen et al. digestive tract of two nevrorthid species, Nevrorthus [25] prepared the first comprehensive list of apatelios H. Aspöck, U. Aspöck & Hölzel, 1977 chrysopid species with information on adult and Nipponeurorthus fasciatus Nakahara, 1958. feeding habits. Later, knowledge on the adult Randolf et al. [15] described in details the feeding strategies in Chrysopidae further improved mouthpart morphology in Nevrorthus apatelios, [e.g. 4, 19, 26, 27, 28, 29, 30]. The association of showing strongly sclerotized asymmetrical adult green lacewings with certain plant substrate mandibles. Additional work is needed to establish species is evident [31] when they prey on a more complete picture of the feeding habits in phytophagous insects and when they feed on Nevrorthidae. sweet plant products, honeydew and pollen.

Suborder: Hemerobiiformia Most adult green lacewings have a glycophagous feeding strategy. This includes sugar-rich foods Family: Ithonidae, lacewings such as products of plant origin (e.g. nectar, plant Two formerly recognized families, Rapismatidae fluids) and insect honeydew. In some green and Polystoechotidae, were recently included in lacewings, e.g. in Chrysoperla and Pseudomallada the family Ithonidae sensu Winterton and prasinus, this feeding regime is combined with a Makarkin [16]. De Jong [17] studied the biology palynophagous strategy, and thus classified as a of an American species punctatus palyno-glycophagous habit [e.g. 4, 19, 28, 29, 30, 32]. (Fabricius, 1793). Based on observations of Species of the Chrysoperla carnea complex feed dissected individuals of this single species, a on pollen from a variety of plants. In western carnivorous habit was established. Besides France, for example, adults consumed pollen from fragments, several pollen grains were 28 different plant families, and females consumed found in the foregut [17]. Adaptation to such a more pollen than males [30, 32]. diet could include the asymmetrical mandibles Some adult green lacewings feed on insects (genera described in this species. Anomalochrysa, Atlantochrysa and Chrysopa). Family: Osmylidae The species of the genus Chrysopa consume mites, small insects like aphids, pollen, and In the past, adult Osmylidae have generally been presumed to feed on food of origin [18]. spores of fungi; thus, these green lacewings are In the gut of the European species Osmylus designated as omnivorous [4, 19, 33, 29]. Bozsik fulvicephalus , besides insect fragments, algae, [29] demonstrated that species of the genus fungi, honeydew, pollen and plant fragments were Chrysopa differ on account of the proportions of food items consumed. Some omnivorous species found [10, 19, 20]. This species feeds on small arthropods and does in fact, actively feed on require proteins of animal origin to reproduce, pollen as well [10]. In the gut of Australian even if they are able to survive and maintain their Kempyninae, a subfamily of Osmylidae, New potential with sweet liquids [27]. [21] recorded fungal hyphae, spores, pollen, Only a few green lacewings, belonging to the fragments of bark and foliage and a lesser amount subfamily Nothochrysinae (genera Hypochrysa, of insect fragments. In the past, Osmylus was Kimochrysa, Pamochrysa, Pimachrysa) feed designated as a carnivorous-glycophagous insect exclusively on pollen – a palynophagous habit [4]. [19]; however, based on actual findings on their According to its morphological and physiological feeding habits, osmylids are classified as omnivorous, characteristics, Hypochrysa elegans is well adapted having asymmetrical mandibles [22]. to the digestion of pollen. This species has strong

32 Dušan Devetak & Vesna Klokočovnik

adapted to the non-carnivorous diet, with smaller, symmetrical mandibles without any incisor, and with spoon-like lacinia for consumption of honeydew [4, 33], while other species (omnivorous) have larger, asymmetrical mandibles and a strong incisor on the left side for capturing and holding prey [27].

Family: Hemerobiidae, brown lacewings

It has been known for a long time that adult

brown lacewings feed on aphids and honeydew, including certain species important as biological control agents [1, 4, 19, 35, 36, 37, 38, 39]. The association of adult brown lacewings with certain

plant substrate species is evident, as they prey on

phytophagous arthropods [40]. The first microscopic inspection of gut contents in hemerobiids dates back to 1936, when Killington [41] detected well-chewed fragments of aphids and lepidopteran scales. The gut contents of all the brown lacewing species that were analyzed included fragments [4]. Stelzl & Gepp [42] and Stelzl [19, 37] provided a thorough list that

Figure 1. A part of the digestive tract with tracheal include 22 brown lacewing species and detailed trunks in the wall of the crop (esophageal diverticulum) their feeding habits. Adult brown lacewings not of an adult green lacewing: A - in palyno-glycophagous only feed on Homoptera (aphids, phylloxerids species Pseudomallada prasinus, and B - in omnivorous etc.), but also on other arthropods. mites Chrysopa walkeri (Modified from Canard et al. 1990). (Tetranychidae) are prey for at least nine Abbreviations: cr - crop (diverticulum), e - esophagus, hemerobiid species [4], and dipterans were found mg - midgut. in the gut of nine species [37]. Honeydew is regularly consumed by brown lacewings [19, 37]. mandibles, almost no ventilation of the foregut In certain species, such as Wesmaelius quadrifasciatus and no symbionts in the gut [27]. (Reuter, 1894), Hemerobius nitidulus Fabricius, 1777, H. lutescens Fabricius, 1793 and Micromus In relation to different diets in chrysopid species, Hagen et al. [25], Principi and Canard [26] and lanosus (Zelený, 1962), pollen grains were actively Canard et al. [27] provided information on the ingested [19, 37]. Based on the present data, size of tracheal trunks and the size and shape of brown lacewings are characterized as omnivorous. mandibles. Non-carnivorous species, in contrast With respect to their omnivorous diet, hemerobiid to carnivorous (or omnivorous) species, exhibit mouthparts are well adapted, with asymmetrical larger tracheal trunks in the distal part of the mandibles and sharp spoon-like lacinia for esophagus and a strongly muscular diverticulum honeydew take-up. The labium and maxillary palps (crop), which provide oxygenation to the crop have a similar structure, with special sensory (Figure 1). In non-carnivorous species, this part of organs called rhinaria for palpating the plant the crop also contains yeasts, which participate in surface and searching for food (insect prey or the digestion of saccharides, enabling them to be honeydew) [33]. assimilated [34]. Yeasts could act also as symbionts, providing the essential amino acid valine, which Family: Sisyridae, spongillaflies is absent in a honeydew and pollen diet [26]. The first documented observation of carnivorous In non-carnivorous species, the mouthparts are habits in spongillaflies dates back to 1944, when

Feeding biology of adult lacewings 33

Tjeder published a comment on a male nigra as an indication of honeydew feeding, as long as (reported as S. fuscata) feeding on the of an the number of pollen grains is small [9, 19, 45]. alderfly Sialis lutaria [43]. The crop and gut Mites (Acarina) (Figure 2A) seem to represent an contents were examined in seven Sisyra and two important part of the food for spongillaflies. species (Table 2). Field-collected adult Prostigmated mites of the family Tarsonemidae spongillaflies have been reported to feed on were found in the alimentary tract of the South honeydew and small arthropods like mites and American Sisyra elongata [14], and mites of the aphids [14, 19, 44, 45, 46, 47]. group Eriophyoidea (e.g. family Eriophyidae) Additionally, lepidopteran scales, pollen grains (Figure 2A) occurred in high numbers in the gut and fungal spores, all in low quantities, were also of two European species S. nigra and S. terminalis found. Large amounts of pollen in the digestive [19, 45]. tract were noted only in one species Climacia The feeding regime of sisyrids is classified as desordenata [14]. Small particles such as pollen carnivorous-glycophagous. Adaptations to such grains and lepidopteran scales transported by diets are reflected in the mouthparts, specifically wind can also get trapped in the honeydew and in the spoon-like lacinia, which functions for the later consumed by the adult. The presence of a consumption of honeydew, while the asymmetrical low quantity of pollen grains in gut is considered mandibles and very specialized maxillae, with a

Table 2. Food remains from the digestive tract of spongillaflies (Sisyridae).

Species/geographic origin Algae Pollen Acarina fragments Honeydew

Lepidoptera: scales Homoptera: aphids Fungi (spores, hyphae) Fungi (spores, Unidentified arthropod Climacia areolaris (Hagen, 1861) [46, [14] [14] [14] [44] 14]

Climacia desordenata (Monserrat, 2005) [46, [14] South America 14] (Banks, 1908) [46] [46] [46] South America Sisyra elongata (Penny & Rafael, 1982) [14] [14] [14] [14] South America (Retzius, 1783) [19] [19] [19] [19] [19] [19] [19] Europe Sisyra pedderensis (Smithers, 2008) [47] [47] Australia (Tasmania) Sisyra rufostigma (Tillyard, 1916) [14] [14] [14] Australia Sisyra terminalis (Curtis, 1854) [45] [45] [45] [45] [45] [45] [45] Europe

Sisyra vicaria (Walker, 1853) [46] [46] [46] [46] North America 34 Dušan Devetak & Vesna Klokočovnik

Figure 2. Food remains from the digestive tract and mouthparts in Neuroptera. A - three Eriophyid mites and pollen in Sisyra terminalis; B - lacinia covered with bristles in sinuata; C - pollen grains, mostly of family, in the gut of N. sinuata; D - corneal lenses of the insect compound eye in the antlion, Gymnocnemia variegata ; E - remains of an aphid in the owlfly, Libelloides macaronius; F - tarsus of a dipteran in L. macaronius: the claws, empodium and pulvilli can be identified.

groove surrounded by strong setae on the last dustywing species are specifically associated with segment of the palp, serve for catching small certain substrate plants, whereas others are found arthropod prey [33]. on a wide range of plants [48]. Coniopterygidae are predators, feeding on mites (Tetranychidae Family: Coniopterygidae, dustywings and Eriophyoidea), phylloxerids, aphids and scale Adult dustywings are tiny insects, feeding on insects [4, 19, 49]. However, honeydew seems to slow-moving, soft-bodied arthropods. Stenotopic be an additional food source in adults [19, 50].

Feeding biology of adult lacewings 35

Adult coniopterygids have asymmetrical mandibles because of loss of the incisor on the left mandible. The mouthparts evolved a special adaptation for seeking prey, especially tiny mites and scale insects. Lacinia is modified into a sharp tooth with strong setae. The last segment of maxillary palps possesses groove with long setae and also the labial palps are extended into a wide area with hooked setae and bearing distinct area of sensory hairs. All the above-mentioned mouthparts are adaptations for searching (palpating) prey, which is caught in grooves of the maxillary palps [33, 51].

Family: Dilaridae, pleasing lacewings

The adult diet in pleasing lacewings is mostly unknown, but reduced mouthparts suggest a short life span and little ability to feed, if not complete starvation in the adults [52, 53]. Family: Mantispidae, mantidflies Mantispids are sit-and-wait and stalking predators, which feed on live prey (mostly small insects). Their vision is specialized toward hunting [54]. Figure 3. Raptorial forelegs: (A) in a mantidfly Mantispa Once prey is within reach, mantidflies strike aphavexelte; (B) in an antlion, libelluloides. rapidly to grasp the prey with their spiked Legend: cx - coxa, tr - trochanter, fe - femur, ti - tibia, raptorial fore legs. Adult mantispids have an ta - tarsus. elongated prothorax, with a freely movable head and prominent eyes. The forelegs are raptorial, Suborder Myrmeleontiformia composed of an elongated coxa and a spined femur, which fits against the tibia to immobilize Family: Psychopsidae, silky lacewings prey (Figure 3A) [55, 56]. Tjeder [63] and New [64] noted that the abdomen Family: Berothidae, beaded lacewings of female psychopsids contained bark scrapings, rarely also algal spores and fungal hyphae, and Adults in the Berothidae family have been reported occasionally soil or sand grains. Findings of chitin to ingest mites, insects, pollen, fungal spores and fragments in the gut of African species indicate a hyphae [57, 58, 59, 60, 61]. Whilst most berothids carnivorous feeding strategy [63]. The mandibles are omnivorous, at least two species – Nyrma kervillea and Berothimerobius reticulatus – seem are well developed for carnivorous feeding, and to be palynophagous, consuming large amounts of are somewhat asymmetrical, acutely pointed and pollen (Table 3). In Berothimerobius adults, the with a large internal tooth on each mandible. The mouthparts are well adapted for the palynophagous last segment of the labial palps exhibits a sensory area [63]. However, from these preliminary diet: the lancelolate mandibles are without apical denticles, and the galea is flat and very hairy [61]. findings it is impossible to speculate on the However, mites (: Eriophyoidea) of the feeding habits of adult silky lacewings. family Rhyncaphytoptidae have been observed in Family: Nemopteridae, spoon-winged lacewings or the gut of three species of Podallea [61]. ribbon-winged lacewings Forelegs in adults in the berothid subfamily Nemopteridae have specialized, non-biting Rhachiberothinae are raptorial, resembling the mouthparts for feeding exclusively on nectar and grasping apparatus in mantidflies [62]. pollen (palynophagy) (Figures 2B, 4) [65, 66, 67]. 36 Dušan Devetak & Vesna Klokočovnik

Table 3. Food remains from the digestive tract of beaded lacewings (Berothidae). Legend: x - present; x! - large quantity of pollen; (x) - only a few pollen grains.

Subfamily/species Reference Pollen Acarina Plant material Plant material

Insect fragments hyphae) Fungi (spores, Subfamily Rhachiberothinae Mucroberotha sp. x x [58]

Subfamily Cyrenoberothinae

Cyrenoberotha penai (MacLeod & Adams, 1967) x [57]

Subfamily Berothinae

Isoscelipteron glaserellum (U. Aspöck, H. Aspöck (x) [61] & Hölzel, 1979)

Podallea vaseana (Navás, 1910) x (x) x x [61]

Podallea sashilana (Navás, 1931) x x x [61]

Podallea exarmata (Tjeder, 1959) x x x x [61] Podallea manselli (U. Aspöck & H. Aspöck, 1988) x x x x [61] Nodalla saharica (Esben-Petersen, 1920) x x! x [61] Subfamily Nosybinae Nosybus nobilis (Navás, 1910) x x [61] Subfamily Nyrminae

Nyrma kervillea (Navás, 1933) x! x [59, 60, 61]

Subfamily Berothimerobiinae

Berothimerobius reticulatus (Monserrat & x! [61] Deretsky, 1999)

The most thoroughly studied are the mouthparts capturing insect prey (Figure 4) [67, 68, 69]. Adult of the Balkan-Anatolian species nemopterids play a role as pollinators of plants. Olivier, 1811 [67]. The weak mandibles are elongated Family: Crocidae, thread-winged lacewings and without dentation. The maxillae are the main part for food uptake. The lacinia, galea and maxillary Until recently, thread-winged lacewings (Crocidae) palps form a functional unit that can be extended were included as a subfamily in the Nemopteridae and function for food uptake. The lacinia and family. Adults feed on nectar and pollen, which galea are covered with long bristles (Figure 2B), has been confirmed by examining the gut contents and during feeding, pollen grains stick to these. in the species Necrophylus arenarius Roux, 1833 The mouthparts of adult nemopterids therefore (=Pterocroce capillaris) [69, 70]. Adults have seem to be too highly modified and weak for similar adaptation of the mouthparts as in the

Feeding biology of adult lacewings 37

Figure 4. Non-biting mouthparts in Nemoptera sinuata are adapted for consuming pollen. Abbreviations: la - lacinia, lb - labium, li - ligula, md - mandible, mx - maxilla, pl - labial palp, pm - maxillary palp.

species of the Nemopteridae family, with an a few individuals, where fragments of elongated head and non-biting mouthparts [71]. also occurred. The plant tissue probably originated from the intestinal contents of the caterpillars [8]. Family: Nymphidae, split-footed lacewings Examination of the intestinal contents in four Very little information is available on the biology additional species (belonging to the genera , of nymphids. New [72] mentioned that the adults Gymnocnemia, Megistopus and Palpares) confirmed are predators. their carnivorous feeding habits [73, 74, this Family: Myrmeleontidae, paper]. New [72] believed that adult antlions Prey-catching behavior in larval antlions has been without tibial spurs (such as Gymnocnemia) do not feed on winged insects but prey on sedentary known for a long period. However, the knowledge of the feeding habits in adult antlions remains aphids. Inspection of the intestinal contents of insufficient. Most species that have been studied Gymnocnemia variegata revealed that the species does feed on winged insects (Table 4, Figure 2D). have been classified as carnivorous. During the investigation of feeding habits in adults of four The active ingestion of pollen is known in some European antlion species, Stelzl & Gepp [8] North American species of the antlion tribe (eg. Brachynemurus yavapai examined the feces excreted by adults shortly after capture (Table 4). In the excrement of all Currie, 1903 [75]; their feeding habits can thus be four species, insect fragments were found. These described as palynophagous. In some species of antlions had fed on aphids, dipterans, coleopterans, the tribe, the loss of tibial spurs appears to be heteropterans, lacewings and lepidopteran larvae correlated with a specialized diet of aphids. (caterpillars). In some individuals, only a few Adult antlions, which feed on well sclerotized pollen grains were recorded. Smaller quantities of arthropods, have mandibles with double incisors pollen, lodged between the setae of prey insects, (Figure 5). This kind of mandible is also an could have been consumed indirectly [8]. However, adaptation for capturing and holding of fast-flying in two species, Myrmecaelurus trigrammus and insects [33]. Raptorial forelegs in some species Nohoveus punctulatus, larger quantities of pollen are equipped with bristles and are used in taking a were noted. Some plant tissues were present in firm grip on prey (Figure 3B).

38 Dušan Devetak & Vesna Klokočovnik

Table 4. Food remains from the digestive tract or feces of antli ons (Myrmeleontidae). Legend: x - present; x! - large quantity of pollen; (x) - only a few pollen grains.

Species/food Pollen Nectar Aranea remains Diptera Reference

Psylloidea Coleoptera Plant tissue Aphidoidea Aphidoidea Heteroptera Hymenoptera : Noctuidae

Lepidoptera: caterpillars Neuroptera: Chrysopidae Lepidoptera: unidentified Unidentified insect fragments

Lepidoptera: Microlepidoptera

Brachynemurus yavapai x! [75] (Currie, 1903) Brachynemurus - x x x x x x x x [75] other species plumbeus (x) x x x x x x [8] (Olivier, 1811) Distoleon This tetragrammicus (x) x paper (Fabricius, 1798) Gnopholeon spp. x x x [75] Gymnocnemia This variegata x paper (Schneider, 1845) Macronemurus appendiculatus x! x x x [74] (Latreille, 1807) Maracandula apicalis x [75] (Banks, 1901) Megistopus This flavicornis x x paper (Rossi, 1790) Menkeleon bellula x [75] (Banks, 1901) Myrmecaelurus trigrammus x! x x x x x x x [8] (Pallas, 1771) nemausiensis (x) x [8] (Borkhausen, 1791) Feeding biology of adult lacewings 39

Table 4 continued.. Nohoveus punctulatus x! x x x x x [8] (Steven in Fischer v. Waldheim, 1822) Palpares libelluloides x x x [73] (Linnaeus, 1764) Tyttholeon puerilis x [75] (Adams, 1957)

Figure 5. Mouthparts in an antlion Palpares libelluloides. Abbreviations: ga - galea, la - lacinia, lb - labium, md - mandible, mx - maxilla, pl - labial palp, pm - maxillary palp. 40 Dušan Devetak & Vesna Klokočovnik

Family: Ascalaphidae, owlflies other arthropods, and are candidates for biological control agents. The predatory, i.e. carnivorous feeding habits of owlflies have been known for a long time. Adult owlflies are active aerial predators [76]. Diurnal ACKNOWLEDGEMENTS species can be seen at a certain altitude above the We are grateful to Víctor J. Monserrat (Complutense ground, hovering and darting at high velocities University of Madrid) for critical reading of an in pursuit of small flying insects. In the owlfly earlier version of the manuscript. We are grateful subfamily , compound eyes are to Michelle Gadpaille (Department for English divided and evolved from undivided eyes [77]. and American Studies, University of Maribor) for Diurnal owlflies of the subfamily Ascalaphinae her help with linguistic improvements of the detect their prey as contrasting dark spots against manuscript. the sky with the large dorso-frontal part of their CONFLICT OF INTEREST STATEMENT compound eyes, which are sensitive in the UV range [78, 79]. The properties of the visual system The authors certify that they have no affiliations are optimal for detecting small insects as with or involvement in any organization or entity contrasting spots against both clear and cloudy with any financial interest, or non-financial interest skies [79]. in the subject matter or materials discussed in this Intestinal contents have been examined in only manuscript.

a few owlfly species [19, 80, 81]. In (Denis & Schiffermüller, 1775), L. lacteus REFERENCES (Brullé, 1832) and L. macaronius (Scopoli, 1763), 1. New, T. R. 1988, Aphids, their Biology, remains of mites, aphids, cockroaches, heteropterans, Natural Enemies and Control, A. K. Minks thysanopterans, dipterans, hymenopterans, and P. Harrewijn (Eds.), Elsevier, Amsterdam, lepidopterans and coleopterans have been found 249. (Figures 2E, F) [19, 80, 81]. The diversity of 2. Stelzl, M. and Devetak, D. 1999, Agric. arthropod prey indicated that owlflies presumably Ecosyst. Environ., 74, 305. feed not only during flight but also while resting 3. Tauber, M. J., Tauber, C. A., Daane, K. M. on plant stems. In some individuals even honeydew and Hagen, K. S. 2000, Am. Entomol., 46, and fungal spores occurred [19]. 26. 4. Canard, M. 2001, Lacewings in the Crop Adult owl- are active predators, with strong, well developed asymmetrical mandibles, with a Environment, P. K. McEwen, T. R. New and A. E. Whittington (Eds.), Cambridge double incisor split into two spikes, which is an University Press, Cambridge, 116. adaptation for catching fast-flying, sclerotized 5. New, T. R. 2001, Lacewings in the Crop prey [33, 81]. Environment, P. K. McEwen, T. R. New

and A. E. Whittington (Eds.), Cambridge CONCLUSION University Press, Cambridge, 380. Adult lacewings exhibit six different feeding 6. Canard, M., Séméria, Y. and New, T. R. habits; however, most lacewings feed on small (Eds.), 1984, Biology of Chrysopidae, W. arthropods. Adults of several neuropteran families Junk, The Hague. pollinate plants. The association of lacewings with 7. McEwen, P. K., New, T. R. and certain plant substrate species is also evident: it is Whittington, A. E. (Eds.) 2001, Lacewings indirect when they are preying on phytophagous in the Crop Environment. Cambridge arthropods, and direct when they feed on University Press, Cambridge. honeydew, pollen and sweet plant products. The 8. Stelzl, M. and Gepp, J. 1990, Proceedings of association was demonstrated in Chrysopidae, the Third International Symposium on Coniopterygidae and Hemerobiidae. Because of Neuropterology, M. W. Mansell and H. their carnivorous habit, larvae and adults of many Aspöck (Eds.), South African Department of families have an impact on the populations of Agricultural Development, Pretoria, 205.

Feeding biology of adult lacewings 41

9. Sheldon, J. K. and MacLeod, E. G. 1971, 30. Villenave, J., Thierry, D., Al Mamun, A., Psyche, 78, 197. Lodé, T. and Rat-Morris, E. 2005, Eur. J. 10. Kokubu, H. and Duelli, P. 1986, Proceedings Entomol., 102, 547. of the 2nd International Symposium on 31. Monserrat, V. J. and Marín, F. 1994, Acta Neuropterology, J. Gepp, H. Aspöck and H. Oecol., 15, 119. Hölzel (Eds.), Privately printed, Graz, 151. 32. Villenave, J., Deutsch, B., Lodé, T. and Rat- 11. Meinzer, F. and Gruppe, A. 2011, Proceedings Morris, E. 2006, Eur. J. Entomol., 103, 771. of the Eleventh International Symposium on 33. Stelzl, M. 1992, Current Research in Neuropterology, Book of Abstracts, A. M. Neuropterology, M. Canard, H. Aspöck and Frias Martins and M. Anunciação Mateus M. W. Mansell (Eds.), Sacco, Toulouse, 341. Ventura (Eds.), Ponta Delgada, Portugal, 34. 34. Hagen, K. S. and Tassan, R. L. 1972, Insect 12. Zhang, G. F., Lu, Z. C. and Wan, F. H. and Mites Nutrition, J. G. Rodriguez (Ed.), 2007, Entomol. Exp. Appl., 123, 81. North-Holland, Amsterdam, 323. 13. Malicky, H. 1984, Arch. Hydrobiol., 101, 35. Withycombe, C. L. 1923, Trans. Roy. Entomol. 231. Soc. London, 70, 501. 14. Monserrat, V. J. 2005, Heteropterus Rev. 36. New, T. R. 1975, Trans. Roy. Entomol. Soc. Entomol., 5, 1. London, 127, 115. 15. Randolf, S., Zimmermann, D. and Aspöck, 37. Stelzl, M. 1990, Mitt. Dtsch. Ges. Allg. U. 2014, Arthropod Syst. Phylog., 72(2), 111. Ang. Entomol., 7, 670. 16. Winterton, S. L. and Makarkin, V. N. 2010, 38. Stelzl, M. and Hassan, S. A. 1992, J. Appl. Ann. Entomol. Soc. Am., 103(4), 511. Entomol., 114, 32. 17. De Jong, G. D. 2011, Proc. Entomol. Soc. 39. Stelzl, M., Hassan, S. A. and Gepp, J. 1992, Wash., 113(3), 291. Mitt. Dtsch. Ges. Allg. Ang. Entomol., 8, 18. Killington, F. J. 1932, J. Entomol. Soc. 187. South Engl., 1, 33. 40. Monserrat, V. J. and Marín, F. 1996, J. Nat. 19. Stelzl, M. 1991, J. Appl. Entomol., 111, 469. Hist., 30, 775. 20. Devetak, D. and Duelli, P. 2007, Ann. Ser. 41. Killington, F. J. 1936, A Monograph of the Hist. Nat., 17, 93. British Neuroptera, Vol. 1, Ray Society, 21. New, T. R. 1983, Aust. Entomol. Mag., 10, London. 45. 42. Stelzl, M. and Gepp, J. 1987, Mitt. 22. Beutel, R. G., Zimmermann, D., Krauß, M., Naturwiss. Ver. Steiermark, 117, 185. Randolf, S. and Wipfler, B. 2010, Organisms 43. Tjeder, B. 1944, Entomol. Tidskr., 65, 203. Divers Evol., 10, 311. 44. Brown, H. P. 1952, Am. Midl. Nat., 47(1), 23. Principi, M. M. 1940, Boll. Ist. Entomol. 130. Univ. Studi Bologna, 12, 63. 45. Kokubu, H. and Duelli, P. 1983, Neuroptera 24. Principi, M. M. 1956, Boll. Ist. Entomol. Int., 2, 157. Univ. Studi Bologna, 21, 319. 46. Pupedis, R. J. 1987, Ann. Entomol. Soc. 25. Hagen, K. S., Tassan, R. L. and Sawall, E. Am., 80, 758. F. Jr. 1970, Boll. Lab. Entomol. Agrar. 47. Forteath, G. N. R. and Osborn, A. W. 2012, Filippo Silvestri Portici, 28, 113. Pap. Proc. Roy. Soc. Tasman., 146, 25. 26. Principi, M. M. and Canard, M. 1984, 48. Monserrat, V. J. and Marín, F. 1992, Current Biology of Chrysopidae, M. Canard, Y. Research in Neuropterology, M. Canard, H. Séméria and T. R. New (Eds.), Dr. W. Junk Aspöck and M. W. Mansell (Eds.), Privately Publishers, 76. Printed, Toulouse, 279. 27. Canard, M., Kokubu, H. and Duelli, P. 1990, 49. Henry, T. J. 1976, Proc. Entomol. Soc. Advances in Neuropterology, M. W. Mansell Wash., 78, 195. and H. Aspöck (Eds.), Pretoria, R.S.A., 277. 50. Lacroix, J. L. 1924, Société d’Étude des 28. Bozsik, A. 1992, Acta Phytopathol. Entomol. Sciences Naturelles d’Elbeuf, 42, 53. Hung., 27, 141. 51. Zimmermann, D., Klepal, W. and Aspöck, 29. Bozsik, A. 2000, Beitr. Entomol., 50, 237. U. 2009, Eur. J. Entomol., 106, 651.

42 Dušan Devetak & Vesna Klokočovnik

52. Monserrat, V. J. 1988, EOS Rev. Esp. 67. Krenn, H. W., Gereben-Krenn, B. A., Entomol., 64, 175. Steinwender, B. M. and Popov, A. 2008, 53. Monserrat, V. J. 2014, Heteropterus Rev. Eur. J. Entomol., 105, 267. Entomol., 14(2), 187. 68. Hölzel, H. 1999, Stapfia, 60, 129. 54. Kral, K. 2013, Physiol. Entomol., 38, 1. 69. Monserrat, V. J., Tiviño, V. and Acevedo, F. 55. Redborg, K. E. 1998, Annu Rev. Entomol., 2012, Heteropterus Rev. Entomol., 12(2), 43, 175. 231. 56. Tauber, C. A., Tauber, M. J. and 70. Monserrat, V. J. 1983, Neuroptera Int., Albuquerque, G. S. 2003, Encyclopedia of 11(3), 109. Insects. V. H. Resh and R. T. Cardé (Eds), 71. Tjeder, B. 1967, South Afr. Anim. Life, 13, Amsterdam, Academic Press, 785. 290. 57. MacLeod, E. G. and Adams, P. A. 1967, 72. New, T. R. 1986, Neuroptera Int., Supplemental Psyche, 74(3), 237. Series 1, 1. 58. Tjeder, B. 1968, Entomol. Tidskr., 89, 3. 73. Devetak, D. 1996, Annales, Ann. Istrian 59. Aspöck, U. and Aspöck, H. 1980, Z. Mediterr. Studies, 9, 211. Arbgem. Österr. Entomol., 31(3-4), 92. 74. Devetak, D. 1997, Annales, Ann. Istrian 60. Aspöck, U. 1989, Advances in Neuropterology, Mediterr. Studies, 11, 203. M. W. Mansell and H. Aspöck (Eds.), 75. Stange, L. A. 1970, Univ. Calif. Publ. Pretoria, 101. Entomol., 55, 1. 61. Monserrat, V. J. 2006, Heteropterus Rev. 76. Henry, C. S. 1977, Ann. Entomol. Soc. Am., Entomol., 6, 173. 70, 179-195. 62. New, T. R. 1989, Planipennia, Lacewings. 77. Fischer, K., Hölzel, H. and Kral, K. 2006, Handbuch der Zoologie, Vol. 4 (Arthropoda: J. Zool. Syst. Evol. Res., 44, 285. Insecta), Part 30. Walter de Gruyter, Berlin, 1. 78. Gogala, M. 1967, Z. Vergl. Physiol., 57, 63. Tjeder, B. 1960, South Afr. Anim. Life, 7, 232. 164. 79. Belušič, G., Pirih, P. and Stavenga, D. G. 64. New, T. R. 1988b, Invertebr. Taxon., 2, 841. 2013, J. Exp. Biol., 216, 2081. 65. Picker, M. D. 1984, J. Entomol. Soc. Sth 80. Devetak, D. 1998, Entomol. Croat., 3(1-2), Afr., 47, 259. 45. 66. Popov, A. 2002, Acta Zool. Acad. Sci. 81. Devetak, D., Pirš, P. and Janžekovič, F. Hung., 48(Suppl. 2), 293. 2002, Ann. Ser. Hist. Nat., 17, 219.