Systematic Entomology (1996) 21, 343-352

A new brachypterous species from Costa Rica, with comments on the evolution of flightlessness in brown lacewings (: )

J 0 H N D . 0 S WA L D Department of Entomology, Texas A&M University, College Station, Texas, U.S.A.

Abstract. A new flightless hemerobiid species, Nusalala brachyptera, collected at high elevation in Costa Rica, is described and illustrated, and a variety of data relevant to the evolution of flightlessness in the family Hemerobiidae are reviewed. Flightlessness due to brachyptery has evolved independently in at least five monophyletic [= holophyletic] lineages of the family Hemerobiidae (brown lacewings). Volant hemerobiids are primarily foliage foraging arboreal predators [presumed ancestral condition], while flightless species are predominantly associated with terricolous-type microhabitats (e.g. ground-litter, epiphytic mosses) [presumed derived condition]. These differences suggest a significant habitat shift for flightless hemerobiid species, and that the parallel evolution of flightlessness and brachyptery in hemerobiids are shared responses to the conditions of a terricolous existence. The restriction of most flightless hemerobiid species to insular andlor montanelalpine land areas may be related to the typically depauperate nature of the faunas of such areas. This faunal characteristic may facilitate ttansitions from arboreality to terricolousness by presenting ancestrally arboreal predators such as hemerobiids with novel ecological opportunities in terricolous microhabitats.

Introduction Helicoconis aptera Messner and H.hirtinewis Tjeder; see Meinander, 1972), Hemerobiidae (see below), Ithonidae (an Macroptery and the ability to fly are plesiomorphic within the undescribed species from Mexico; E. G. MacLeod, personal superorder Neuropterida - orders Neuroptera (lacewings communication, specimen seen), and Nemopteridae and allies), Megaloptera (alderflies and fishflies) and (Stenorrhachus walkeri (McLachlan); Stange, personal Raphidioptera (snakeflies) - and flightless taxa are rare within communication, specimen seen). In the families Berothidae, this group of largely predatory . Only one record of a Coniopterygidae, Ithonidae and Nemopteridae flightlessness flightless megalopteran has been traced - a micropterous female has been reported only in females. In these families, species corydalid probably belonging to the genus Platychauliodes with flightless females are known or suspected to be sexually [possibly an aberration; see Barnard (1940)l. Flightlessness is dimorphic, with fully macropterous volant males. Only within not definitely known in the order Raphidioptera, although the family Hemerobiidae are species presently known that are doubts have been expressed about the flight abilities of the flightless in both sexes. females of two inocelliid species based on their relatively small This paper describes a new brachypterous species of the wings (i.e. Inocellia fulvostigmata Aspock & Aspock, see hemerobiid genus Nusalala and reviews the phenomena of Aspock et al., 1991, and Indianoinocellia mayana Aspock, wing reduction and flightlessness in the family Hemerobiidae. Aspock & Rausch, see Aspock et al., 1992:175). Within the Four topics related to the latter theme are discussed. First, the order Neuroptera, taxa inferred to be flightless on the basis of taxonomic and phylogenetic positions of flightless hemerobiids brachypterous, micropterous or apterous wing states are known are surveyed. Second, the morphological evidence for in the families Berothidae (i.e. Trichoma gracilipenne Tillyard; flightlessness in hemerobiids is examined. Third, the available see Aspock & Aspock, 1985), Coniopterygidae (e.g. data on habitat preferences of flightless hemerobiids is reviewed. Finally, factors that may have contributed to the Correspondence: Dr John D. Oswald, Department of Entomology, evolution of flightlessness in hemerobiids are considered and Texas A&M University, College Station, TX 77843-2475, U.S.A. discussed.

O 1996 Blackwell Science Ltd 343 344 John D. Oswald

Figs 1-7. Nusalala brachyptera, n.sp. [holotype]. 1, Left forewing (converted to right dorsal view). 2, Left hindwing (converted to right dorsal view). 3, 9th tergite and ectoproct, lateral. 4, parabaculum and laterobacula, dorsal. 5, same, lateral. 6, gonarcus complex, dorsal. 7, same, lateral (arrow points into compressed space separating neo- and extrahemigonarcus). Abbreviations: 9t, 9th tergite; ect, ectoproct; egpp, extragonopontal process; ehgp, extrahemigonarcal process; ehgs, extrahemigonarcus; igs, intragonarcus; ltb, laterobaculum; med, mediuncus; ngps, neogonopons; nhgs, neohemigonarcus; pa, parabacular apophysis; tl, terminal lobe.

Nusalala brachyptera sp.n. (Figs 1-7) Forewing (Fig. 1). Brachypterous, 3.54.5 mm long (tegula to apex), oval and coriaceous; coloration variable, mostly Diagnosis. Differentiated from other Nusalala species by testaceous with scattered darker markings, e.g. some crossveins the following combination of characters: (i) Forewings and along wing margin; venation reduced and slightly irregular; coriaceous and brachypterous (Fig. 1); (ii) hindwings costal space narrow, with or without a few (1-3) crossveins micropterous and scale-like, venation vestigial (Fig. 2); (iii) (not veinlets) present, pterostigma absent; subcostal space with male ectoproct with a prominent posteroventral spine (Fig. 3). crossveins irregular in number and position; radius with 4-6 The first two characters will differentiate brachyptera from all 'prestigmal' oblique radial branches; radial space with 34 described species of Nusalala except andina Penny & Sturm. irregular gradate series; bases of media and radius fused; These two brachypterous species are easily separated by the M3 + 4 not always (e.g. paratypes) fused to Cu as in other presence of a distinct posteroventral male ectoproct spine in Nusalala species. Hindwing (Fig. 2): micropterous, apex brachyptera (absent in andina). The detailed conformations of truncate, venation vestigial. the extragonarcal processes (extrahemigonarcal, extragono- pontal and mediuncus) and laterobacula of brachyptera are also diagnostic (Figs 4-7). Male terminalia (holotype). 9th tergite (Fig. 3, 9t): divided sagittally into a pair of hemitergites; apodemes of Description. (Holotype and paratype males; morphological proximoventral hemitergite angles prominent. Ectoprocts terminology after Oswald, 1993a.) (Fig. 3, ect): indistinguishably fused to ipsilateral 9th

O 1996 Blackwell Science Ltd, Systematic Entomology, 21, 343-352 Flightlessness in brown lacewings 345 hemitergites ventrally, but free dorsally; posteroventral spine on Cerro de la Muerte, 7.vi.1992, 2750 m [9000'], ex. litter, short but prominent. Gonarcus (Figs 6-7): intragonarcus (igs) M. L. Jameson (CAS, in alcohol). extensive, narrowed dorsally and extending on to neogonarcus, ventral margin with a rounded indentation, no clear Other Material (1 9). COSTA RICA: Cartago Prov.: 1 9 3 differentiation between intragonopons and intrahemigonarcus; mi. [5 km] S. Empalme, 10.vii.1974, 2620 m [86007],O'Brien, extragonarcus highly modified; each extrahemigonarcus (ehgs) O'Brien & Marshall (CAS, pinned). Because this specimen produced posterodorsally as a stout glabrous processes (ehgp) was not collected in association with an identifiable male it is and posteroventrally as a rounded lobe, margins of specifically excluded from the type series and is only extrahemigonarcus inwardly revolute below posterodorsal provisionally placed with this species. processes; extragonopons composed of a pair of slender acuminate processes (egpp) laterally and a median mediuncus Etymology. From Greek brachys, short, and pteron, feather (med); bases of extragonopontal processes connected medially or wing, in reference to the species' abbreviated wings. by a tenuous sclerotized strap; mediuncus attached to distal margin of strap by a transverse membranous articulation; Discussion. The genus Nusalala (Navis, 1913) currently neogonarcus present; neogonopontal region (ngps) narrowed contains ;= 20 valid species and is endemic to South and and articulated sagittally in dorsal view, projectigg Central America and the West Indies (Monserrat, 1990). The conspicuously over base of extragonopons in lateral view; genus is in need of a comprehensive revision, and the discovery neohemigonarcus (nhgs) present but inconspicuous, adpressed of additional new species is expected. Flightlessness and to proximodorsal surfaces of extrahemigonarcus. Parabaculum brachyptery was first noted in Nusalala by Penny & Sturm (Figs 4-5): parabacular apophysis (pa) a well-developed, (1984) in the Colombian species andina. Nusalala brachyptera arcuate, vertical plate; terminal lobe (tl) apices splayed, is the second flightless species to be described in this genus. principal sclerotization of lobes on medial faces, lateral faces The single female specimen cited above was collected ;= 20- largely membranous, lobe surfaces adjacent to laterobacula 30 km WNW of the two male specimens. Its tentative forming a longitudinal v-shaped channel. Laterobacula (Figs 4- identification as brachyptera is supported by its similar wing 5; ltb): glabrous, apices revolute, each with a small process or modifications, high elevation collection site in the Cordillera lobe at distal end of articulation with parabaculum. Hypandrium de Talamanca, geographical proximity to the two known males internurn: present. Variation: One of the paratypes differs of this species, and the absence of other known flightless somewhat from the holotype in the following features: (i) Nusalala species in Costa Rica. extrahemigonarcal processes more robust, particularly basally; (ii) each extrahemigonarcus with a small but distinct cusp on posterior margin below posterodorsal spine at point ventrally where extrahemigonarcus ceases to be inwardly revolute (these Survey of flightless hemerobiids cusps absent in holotype); (iii) sclerotized bridge linking bases of extragonopontal processes incomplete medially. Eleven hemerobiid species are currently presumed to be flightless (Table 1). These species belong to four genera Distribution. Currently known only from Costa Rica in the assigned to three monophyletic (= holophyletic) subfamilies Cordillera de Talamanca near Cerro de la Muerte. (Fig. 8). Notiobiellinae: . The genus Psectra contains = 25 valid species. It is exclusively Old World (sub-Saharan Africa, Biology. Both the holotype and paratypes were collected at India, China, South East Asia, Australia, Oceania), except for high elevation (2750-3350 m). One paratype was collected its single flightless species, Psectra diptera Burmeister, which from ground litter. is Holarctic (Europe, eastern Russia, Japan, Canada, northern U.S.A.). Klimaszewski & Kevan (1992:442) suggested that Holotype. 6 (CAS, pinned). Label data (bracketed data this species was probably introduced into North America from added): 'Costa Rica, S[an]. J[osC].,/29mi. N. San Isidroldel Europe. Although this is possible based on its known occurrence General [S.I.d.G. = 9"22'N, 83"42'W], 3350m [11000']1 in Europe, primarily north-eastern distribution in the United 23.vi.1974' [white rectangular label], 'L. & C. W. O'Brienl States and south-eastern distribution in Canada, I have seen & G. B. Marshall' [white rectangle], 'Holotype/Nusalalal specimens from as far west as north central Montana (J. D. brachyptera Oswald/J. D. Oswald 1993' [red rectangle]. Oswald, unpublished). Such a westerly record for an eastern- Condition: good, complete. Right midleg and part of right introduced flightless species seems anomalous unless one antenna glued to a paper point, balance of body (except postulates further human-aided range expansion. The species terminalia) in a gelatin capsule on same pin. Terminalia cleared, may, alternatively, prove to be native to North America. stained with Chlorazol Black, and placed in a glycerin-filled Drepanacrinae: Conchopterella. The Neotropical genus microvial pinned below specimen. Conchopterella contains four valid species in southern continental South America (Argentina and Chile, two spp., Paratypes (26 6). COSTA RICA: Cartago Prov.: 16 Villa including one undescribed) and the offshore Juan Fernandez Mills, km 97.5 Inter-American Hwy, 23.v.1968, 3096 m, R. K. Islands (two spp.). The two continental species are Colwell (MacLeod, pinned);?Cartago Prov.: 18, Rt. 2, krn 97 macropterous and volant, while the two insular species (kuscheli

0 1996 Blackwell Science Ltd, Sjsremaric Entomologj~,21, 343-352 346 John D. Oswald

Table 1. Synoptic data on flightless brown lacewings.

Subfamily Genus Elevation Taxonomic species Distribution Habitat (m) Forewing Hindwing sources*

Notiobiellinae Psectra diptera Holarctic ground, low vegetation 0-? brachypterous polymorphic 1, 2, 5

Drepanacrinae Conchopterella kuscheli Juan Fernandez Is. low vegetation 250-500 subcircular brachypterous 3 maculata Juan Fernandez Is. low vegetation 250-550 subcircular brachypterous 3

Microminae Nusalala andina Colombia grass tufts 3800 brachypterous micropterous 7 brachyptera Costa Rica ground litter 2620-3350 brachypterous micropterous this paper acutipennis Zaire 'humus-dwelling' 2720-3000 stenopterous stenopterous 4 cookeorum Maui shrubs? 2950 brachypterous micropterous 10-1 1 vulcanius Maui - 1520 brachypterous absent 6, 8-9, 11 lobipennis Maui shrubs?, mosses, tree trunks 1520-2150 brachypterous micropterous 8, 9, 11 swezeyi Kauai 'rain forest floor' - brachypterous micropterous 9, 11 usingeri Hawaii shrubs? - brachypterous micropterous 9, 11

* Taxonomic Sources: (1) Aspock et al. 1980; (2) Burmeister, 1839; (3) Handschin, 1955; (4) Kimmins, 1956; (5) Klimaszewski & Kevan, 1992; (6) Monserrat, 1993; (7) Penny & Sturm, 1984; (8) Perkins, 1899; (9) Zimmerman, 1940; (10) Zimmerman, 1946; (11) Zimmerman, 1957.

Handschin and maculata Handschin) are brachypterous and ofgn endemic radiation of the genus Micromus on the Hawaiian flightless. Islands. Although the phylogenetic relationships among the : Nusalala. The genus Nusalala contains about = 25 species of Hawaiian Micromus have not yet been critically 20 valid species distributed throughout the Neotropical Region studied, most of these species (perhaps excluding the from southern Mexico to central Argentina. Two flightless widespread Micromus timidus Hagen [= navigatorum Brauer]) species are known: andina Penny & Sturm, from Colombia, will probably be found collectively to constitute a monophyletic and brachyptera n. sp., from Costa Rica. The allopatry and group and radiation endemic to the Hawaiian Islands. The high-elevation collection sites (Table 1) of these species suggest number of times that flightlessness has evolved within this that they evolved flightlessness independently; however, assemblage cannot presently be determined. However, the phylogenetic relationships within this genus are too poorly observations that (i) each flightless species is endemic to a known to corroborate or refute this hypothesis. single island (see Table I), (ii) the species are collectively Microminae: Micromus. The nearly cosmopolitan genus endemic to three different islands, and (iii) the species have Micromus contains = 100 species distributed throughout the been collected (where known) only at relatively high elevations, New and Old Worlds, except for South America, where previous suggest that flightlessness has evolved independently in several records of this genus appear to apply to the genus Nusalala. Hawaiian Micromus lineages. Fightlessness has developed independently in at least two, but The inference that the two preceding lineages, at least, probably more, lineages of Micromus. represent the repeated evolution of flightlessness within Micromus is strongly supported by the allopatry of the flightless Lineage 1. Micromus acutipennis Kimmins. This continental species belonging to these lineages, and by the allopatry of the African species is a member of the informal 'variegatus larger groups of volant species to which they belong, i.e. the species group'. This group is a distinctive aggregate of small, Old World M.variegatus group (acutipennis) and the Hawaiian exclusively Old World, Micromus species, e.g. M.berzosai Micromus complex (cookeorum, vulcanius, lobipennis, swezeyi Monserrat, multipunctatus Matsumura, oblongus Kimmins, and usingeri). parallelus (Navis), and variegatus (Fabricius), which are united on the basis of the hindwing M3 + 4 being fused to the cubitus and on male terminalic characters. Inference of flightlessness

Lineage 2. Micromus cookeorum (Zirnmerman), lobipennis Direct behavioural observations of the capacity for wing motion (Perkins), swezeyi (Zimmerman), usingeri (Zimmerman) and and flight are lacking for all putatively flightless hemerobiids vulcanius Monserrat. These five species are flightless members except Psectra diptera, a species with reduced forewings and

O 1996 Blackwell Science Ltd, Systematic Entomology, 21, 343-352 Flightlessness in brown lacewings 347

Psectra Zachobiella Austrornegalomus Noius Megalomina Fl 8:O 2:O 3:O 3:O I Anapsectra

# flightless species

Notiobiellinae

Carobiinae Sympherobiinae Notiobiellinae Megalorninae Microminae 1 :9 3:60 4:70 1 :40 4:125 Adelphohemembiinae 1 1 Psychobiellinae 1 Drepanacrinae I Drepanepteryginae I ,1:l 5200 1 :2 3:lO 3:40 / r # genera: # species

Fig. 8. Phylogenetic distribution of flightlessness within the family Hemerobiidae. Cladograms after Oswald (1993a.b; 1994). (Below) Subfamilial cladogram of the Hemerobiidae. Areas of solid triangles are approximately proportional to the number of species in each subfamily. Species numbers are approximate. (Above) Intergeneric cladograms of the three hemerobiid subfamilies that contain flightless species. Note the multiple independent origins of flightlessness (boxed genera). Species numbers are approximate. polymorphic hindwings. New (1966) attempted to elicit flight Edelsten, 1940; Fraser, 1946; Killington, 1946; New, 1966) behaviour in this species by suspending two 'macropterous' has confirmed a flight capacity for this species. individuals (i.e. specimens with relatively well-developed fore- The inference of flightlessness in all other presumably and hindwings) in the air by means of thread tethers attached flightless hemerobiid species is based upon the presence of to their mesonota. His tests produced 'only a few feeble wing various structural modifications of the wings, summarized 'beats' ', and he concluded that sustained flight was not possible below, which reduce their apparent viability as flight organs. in this species. New's results are consistent with Killington's (1946) report of repeated and consistently unsuccessful attempts Forewing modiJications (Table 1). Forewing modifications to induce flight in this species. Authors who have maintained include alterations in wing size, shape, venation, ornamentation, that at least some macropters of Psectra diptera may be capable and texture. Nearly all flightless hemerobiids exhibit some of flight have based their conclusions on indirect evidence, degree of forewing brachyptery, although the forewings are such as (i) the discovery of specimens in elevated locations never as strongly reduced as the hindwings and in most species near lights, e.g. upper story windows (MacLeod, 1960) or are only slightly shortened. Micromus acutipennis is unusual in elevated light traps (Throne, 1961) - which, alternatively, may having the forewings narrowed rather than shortened (Kimmins, have been reached by gressorial means, and (ii) evidence for 1956:116, Fig. 2; Monserrat, 1992:135, Fig. 28). In Micromus rapid wing motion (Fraser, 1946) -without actual observation swezeyi the forewings have developed a falcate outline of flight. Thus, although doubts persist about the possibility (Zimmerman, 1940:509, Fig. 2, 1957:75, Fig. 39). In the two for flight in at least some individuals of Psectra diptera, none flightless species of Conchopterella the costal space is greatly of the published accounts of live observations (i.e. Fryer & enlarged, which, together with the shortening of the forewing,

0 1996 Blackwell Science Ltd, Systematic Entomology, 21, 343-352 348 John D. Oswald combines to create a nearly circular wing outline (Handschin, Habitat preferences 1955:19, Figs i-n). All other flightless species exhibit the subelliptical forewing outline typical of most volant The microhabitat preferences of flightless hemerobiids are of hemerobiid species. interest for making evolutionary inferences about the origin of All flightless species possess well-developed, often flightlessness in brown lacewings. Unfortunately, such data are somewhat irregular, forewing venation. Several species, e.g. scarce. Presented below is a review the data available in the Micromus cookeorum, M.swezeyi, Conchopterella maculata, published literature, from specimen labels, and from have developed supernumerary crossveins between the correspondence with several collectors who have encountered longitudinal veins, which in some cases are numerous enough flightless hemerobiids in the field. These data are summarized to obscure the true courses of the longitudinal veins. The in Table 1. macrotrichia on the outer surfaces of the longitudinal veins are also modified in several species. These modifications include both reduction in setal size, which may be extreme in some Psectra species, e.g. Micromus vulcanius, lobipennis, and thickening and pedicelation of setae, i.e. Micromus cookeorum. The Holarctic species Psectra diptera is the only flightless A feature common to most flightless hemerobiid species is hemerobiid for which relatively detailed biological information a secondary thickening of the forewing membrane, giving it a is available. Observations on live adults have been published & coriaceous texture. This development eliminates or restricts by Fryer Edelsten (1940), Fraser (1946), Killington (1946; still the best biological reference for this species) and New bending along several of the wing's longitudinal flexion lines, (1966). Because of its relative rarity and intriguing wing strongly suggesting that such wings no longer function for polymorphism, a considerable literature of short 'collection flight. The development of a coriaceous wing texture is also reports' and other papers exists for this species. Typical correlated with the development of a distinctly concavo-convex, collecting sites reported for adults of Psectra diptera include: rather than planar, wing form. In retracted position, such wings 'sedge refuse in ... Fen' (Donisthorpe, 1935); 'grass of prairies' form a biconvex chamber around the abdomen, into which one (Fitch, 1855); sweeping 'meadow grass' and 'sedge' (Fraser, or more pairs of legs are capable of being withdrawn. An 1946); 'under cut grass' (Fryer & Edelsten, 1940); 'beating ... extreme development of this condition occurs in Conchopterella grass' (Hagen, 1886); 'under cut grass', 'at grass roots in a kuscheli and maculata. In these species the expansive damp, uncut field' (Killington, 1946); 'taken off a hazelbush', development of the costal space (Oswald, 1993a:236, Fig. 132), 'beaten from amongst bushes' (Kimmins, 1935); 'grass or especially proximally, extends the wing-chamber sedke of an improved pasture', 'ground in mountain meadow' anteroventrally, providing a laterally enclosed space within (MacLeod, 1960); 'sweeping ...the banks of the Nith' which the entire head and prothorax (and their appendages) (McGowan, 1903); 'am Rand eines kleinen Wassergrabens auf can be retracted. By providing a strengthened retreat for einer kiirzlich abgemahten Wiese' (Messner, 1971); '[on] an the appendages and relatively weakly sclerotized abdomen, oak whose low drooping branches touched ...the rough growth coriaceous concavo-convex wings may provide some degree below' (Morton, 1936); 'seaward side of ...permanent sand- of physical protection against predation, or, alternatively, may dunes. ..amongst.. .roots of Marram grass.. .and...on bare, loose act to camouflage the normal body outline. No investigations sand' (New, 1966); 'light trap ...hung from a clothes line' of the musculature of the fore- or hindwings of flightless (Throne, 1961); and 'cultivated bog' (Tjeder, 1946). Although hemerobiids are present in the literature; however, the fact that Killington (1946) managed to rear the larvae of this species wing motions have been observed in Psectra diptera (e.g. from eggs laid by a captive female, the only published record Fraser, 1946; Killington, 1946; New, 1966) suggests that at of wild-caught larvae is apparently that of New (1968), who least remnant forewing musculature exists in this species. captured two specimens in pitfall traps on beach dunes in eastern England. In combination, these and other records portray Psectra diptera as a ground-dwelling species that is Hindwing modifications (Table 1). Modifications to the usually associated with damp, although not fully aquatic, hindwings include variations in wing size, shape, and venational microhabitats. Under this interpretation, the sporadic and development. The variations in size range from slight scattered collection records of adults from standing low brachyptery with full venation, e.g. Conchopterella (see vegetation are attributable to the occasional vertical dispersal Oswald, 1993a:236, Fig. 133), through microptery with of adults into such vegetation, where they are then subject to vestigial venation, e.g. Nusalala (Fig. 2) and most Micromus, capture by sweeping or beating. to complete aptery, i.e. Micromus vulcanius. Psectra diptera is unusual in that it is characterized by a polymorphism in hindwing size (see MacLeod, 1960 and references cited therein). Conchopterella Variations in shape include length reduction, resulting in broadly oval wings (e.g. Conchopterella), width reduction, The habitat preferences of this genus are poorly known. resulting in lanceolate wings (i.e. Micromus acutipennis), and, C. W. O'Brien (pers. comm.) reported collecting flightless in highly reduced species, small, scale-like, terminally rounded Conchopterella adults on Mas a Tierra Island by beating low or truncate flaps. scrubby vegetation (including Gunnera sp. and 'bush ferns')

O 1996 Blackwell Science Ltd, Systematic Entomology, 21, 343-352 Flightlessness in brown lacewings 349 growing under a closed canopy forest. Many specimens were of rainforest trees (J. K. Liebherr, pers. comm.). Other Hawaiian taken beating at night, and the species appears to be reasonably species have been reported from mosses on the rainforest floor abundant. Larvae of this genus are unknown. These data, (swezeyi; see Howarth & Mull, 1992), from grasslands, and although inconclusive, suggest that flightless Conchopterella from the forest canopy (F. G. Howarth, pers. comm.). Given species are ground or scrub inhabiting species that forage, at these cryptic habits, the published collection records of least as adults, in low vegetation. flightless Hawaiian hemerobiids from elevated plant surfaces may be attributable (as for some Psectra diptera records) to individuals that dispersed by chance into vegetation adjacent Nusalala to their preferred microhabitats. The cryptic shape and coloration and apparent nocturnality of the Hawaiian species A total of six adult specimens are known of the two flightless (definitely known for lobipennis; F. G. Howarth, pers. comrn.), Nusalala species: four of brachyptera and two of andina. The as well as their association with relatively poorly collected larvae of these species are unknown. Nusalala andina was microhabitats (ground litter, epiphytic plants, under bark), collected from cut-off tufts of the grass Calamagrostis effusa probably contributes significantly to their seeming rarity, growing in a moist to marshy paramo region at 3800 m (above although other factors such as restricted habitat distributions, timberline) in the Colombian Andes (Penny & Sturm, 1984). predatory lifestyles, and possible competitive exclusion by No observations were made on the live adults. The type locality introduced ants, may also play a role. No data is available of brachyptera was a pygmy cloud forest, characterized by an on the immature stages of any of the flightless Hawaiian upper open canopy of short (= 2-6 m tall), widely dispersed, Micromus species. trees and a lower dense scrub vegetation containing thick- leaved evergreen plants and a bamboo-like grass (C.W. O'Brien, pers. comm.). The type specimen was probably collected by Evolution of flightlessness beating the scrub vegetation. Label data associated with one paratype of brachyptera indicates that it was collected from Two major propositions relative to the evolution of ground litter. These data clearly place flightless Nusalala flightlessness in hemerobiids are supported by the data compiled species in microhabitats at or near the ground surface. here. First, the repeated evolution of flightlessness in brown- lacewings is closely associated with parallel shifts from ancestrally arboreal to derived terricolous or terricolous-like Micromus , habitats; and, second, the parallel, derived, modifications in wing morphology observed in flightless hemerobiids are the Five specimens of the African species acutipennis are adaptive consequence of living on the ground, or in ground- recorded in the literature (Kimmins, 1956; Monserrat, 1992). like habitats. The first proposition is based on three central The three specimens originally described by Kimmins were premises: (i) that flightless hemerobiids collectively represent stated to be 'humus-dwelling' by their collector, clearly a polyphyletic aggregation of taxa, (ii) that hemerobiids are suggesting a ground microhabitat association for this species. ancestrally arboreal, and (iii) that loss of flight ability in The microhabitat associations of the several Hawaiian species, hemerobiids is positively correlated with the occupation of however, are more difficult to establish with certainty. The ground or ground-like habitats. The second proposition rests published plant-association records for these species are as on the additional premise that the altered morphological features follows: Micromus cookeorum (ex. Dubautia sp.); M. lobipennis of flightless hemerobiids can be reasonably interpreted as (ex. Cyanea, Metrosideros, Myrsine, ferns, mosses on trees), adaptive in terricolous or temcolous-like habitats. Support for and M. usingeri (ex. Sophora). Most of the Hawaiian species these premises is given below. of these plant genera are shrubs or small trees, and it seems probable that most of the hemerobiid specimens were collected from them by beating or sweeping. However, the limited (genus-level) identifications of these plants, and the absence of more precise plant-position data for the collections, makes The collective polyphyly of flightless hemerobiids can be interpretation of the significance of these records difficult. Of clearly demonstrated by mapping the taxonomic distribution the five flightless Hawaiian species, lobipennis is the most of flightless taxa on to an estimate (cladogram) of the higher common, least modified morphologically, and best known phylogeny of the Hemerobiidae. Such a mapping (Fig. 8) biologically. Adults of this species are known to be active clearly shows that the 11 known flightless hemerobiid species nocturnal predators that patrol the trunks and branches of trees belong to four genera placed in three different monophyletic in mature, high elevation, rainforest habitats, where they subfamilies. probably prey on endemic psocids and other small (Howarth & Mull, 1992; F. G. Howarth, pers. comm.). During daylight hours this species retreats under bark (F. G. Howarth, Ancestral arboreality pers. comm.) or amongst epiphytic plant growth. Several individuals of this species have been collected in recent years Arboreality is inferred to be ancestral relative to by sifting epiphytic mosses pulled from the trunks and branches tenicolousness within the family Hemerobiidae. This polarity

0 1996 Blackwell Science Ltd, Systematic Entomology, 21, 343-352 350 John D. Oswald is based upon the habitat preferences shown by species (i) abbreviation of the forewing length, (ii) thickening of the belonging to the sister-groups of the hemerobiid clade that forewing membrane, (iii) development of a concavo-convex contains all flightless taxa, i.e, the Notiobiellinae + forewing shape, and (iv) significant areal reduction of the Drepanacrinae + Megalominae + Drepanepteryginae + Micro- hindwing. All of these modifications can plausibly be minae (Fig. 8). Two of these sister-groups, subfamilies interpreted as adaptations to terricolous-type environments. Hemerobiinae and Sympherobiinae, contain a number of genera with species that are relatively well-characterized biologically, Forewing abbreviation. In hemerobiids, as in most i.e. in the genera , Sympherobius and . neuropteran taxa, the tips of the forewings in resting position These species are overwhelmingly arboreal, although a few extend beyond the end of the abdomen. Shortening the are also known to occur in lower shrubby vegetation (Aspock forewings reduces overall body length, and thus may facilitate et al. 1980; Killington, 1936, 1937). Biological information increased mobility in the confined spaces of terricolous habits on members of the other three sister-groups, subfamilies by decreasing the minimum turning radius of the body. Adelphohemerobiinae, Carobiinae and Psychobiellinae, is Forewing membrane thickening. The thickening of the lacking or is too anecdotal to provide meaningful information forewing 'membrane' to form a coriaceous wing texture on habitat preferences. Although detailed biological information may serve multiple functions in terricolous hemerobiids. It for most species is lacking, arboreality also appears to be the undoubtedly increases the wing's resistance to abrasion and predominant lifestyle mode of the biologically known species tearing, which is further aided in some species by the appearance of the clade containing all flightless species. of numerous adventitious crossveins. It may also function as a form of 'armor' to protect the relatively soft and vulnerable abdomen, thus reducing susceptibility to predation. This latter Correlation of Jlightlessness and terricolousness function may partially offset the loss of the capacity to escape predators by flight. The increased rigidity of the coriaceous As shown in Table 1, flightlessness appears to be strongly forewing may also reduce the incidence of wing-membrane1 positively correlated with tenicolousness in brown lacewings. substrate adhesion that might be caused by wing surface Five of the 11 known flightless species have unambiguous wetting (given water's high surface tension) in moist, high ground habitat associations (Psectra diptera, Nusalala andina, humidity, terricolous environments. N.brachyptera, Micromus acutipennis, and M. swezeyi). A second group of five species (Conchopterella kuscheli, Forewing concavo-convexity. An interesting feature of most C.maculata, Micromus cookeorum, M.lobipennis, and flightless hemerobiids is the tendency for the forewings to lose M.usingeri) are known from low vegetation, but are likely to their planar structure and become bowed out around the be normal inhabitants of more temcolous-type habitats, e.g. abdomen. This 'wrap-around' wing form probably produces a M.lobipennis, whose rainforest tree-trunk habitat often includes more compact body form that also adds to increased mobility dense epiphytic mosses that might be considered extensions of in confined spaces. As suggested above under Inference of the adjacent forest floor. The habitat association of the eleventh jlightlessness: forewing modz$cations, the space formed species, M.vulcanius, is unknown. between these wings may additionally function as a protected cavity within which the appendages (antennae, legs and abdomen) may be sequestered when the is threatened. Flightlessness and adaptation Hindwing areal reduction. Vestigialization of the hindwings Assessment of whether or not the loss of flight capacity in in flightless hemerobiids is probably attributable to the non- flightless hemerobiids can be considered adaptive is largely functionality of the hindwings following the loss of flight. restricted, given the limited available data, to a subjective Unlike the forewings, no secondary function for this pair of evaluation of the functional significance of the wing remnants, wings has apparently been developed. Under such i.e. do these remnants perform significant alternative functions circumstances, minimization of energy expenditure on in flightless species? That the forewings continue to play an hindwing development would be expected. Observed important function in the body plan of flightless hemerobiids differences in the degree of hindwing reduction suggest that is supported in a general way by the observation that the fore- different hemerobiid lineages are at different stages in the and hindwings are usually differentially reduced (Table 1). development of flightlessness. It is tempting to assume that taxa Hindwings are often reduced to small 'scales' (micropterous), showing more highly reduced wings, particularly hindwings, while the forewings are never reduced to the extent that any represent older origins of flightlessness; however, because there of the abdomen is left exposed in lateral view. If both pairs of are no data to suggest that wing reduction proceeds at similar wings were equally non-functional following the loss of flight rates in different hemerobiid lineages, such an assumption is capabilities, they would be expected to exhibit similar degrees currently without foundation. of reduction. Another type of data relevant to the question of wing- General discussion remnant function is the existence of interspecific commonalities in forewing and hindwing morphology. Four basic modifications Because of the functional and evolutionary importance of of wing structure are shared by nearly all flightless hemerobiids: wings in the diversification of insects, explanations for the

O 1996 Blackwell Science Ltd, Systematic Entomology, 21, 343-352 Flightlessness in brown lacewings 351 secondary reduction and/or loss of alar structures have been depauperate relative to lowland or continental areas. This fertile topics for speculation and investigation. The most widely condition, in turn, suggests the existence of decreased faunal accepted general explanation for flight loss in insects associates competition and/or the presence of open ecological niches in such losses with the occupation of stable environments, i.e. insular and montane habitats. These latter factors may facilitate environments where favourable biotic and abiotic conditions transitions from arboreality to temcolousness by presenting (e.g. space, food, mates, temperature, humidity) are sufficient novel ecological opportunities in temcolous microhabitats to to support the long-term persistence of populations without the any ancestrally arboreal predators that are able to reach them need for substantial dispersal (Roff, 1990; Wagner & Liebherr, (for oceanic islands) or are able to adapt to their more extreme 1992). Under these conditions, individuals (and their physical environmental conditions (for high-elevation areas). aggregates - taxa) that are able to reduce the biological costs In the case of at least some flightless Hawaiian hemerobiids, associated with maintaining the flight apparatus (e.g. wings, the novel ecological opportunity may have been the ability to musculature, coordination, behaviour) are likely to be selected, exploit new food resources, such as the speciose Hawaiian whereas individualsltaxa characteristic of more heterogeneous radiations of trunk- and branch-inhabiting psocids, which may, environments cannot typically shed these costs because of their thus, have provided the initial link in the chain leading to dependence upon the flight apparatus for dispersal to new flightlessness (F. G. Howarth, pers. comm.). habitat patches. In the final analysis, however, the data available for The evolution of flightlessness in brown lacewings is broadly hemerobiids are inadequate to point to a specific model that consistent with the habitat stability model. The terricolous and best accounts for the evolution of flightlessness in this group. temcolous-type microhabitats occupied, as argued above, by Additional data are needed, particularly regarding biology and most flightless hemerobiids would appear to be relatively stable habitat attributes, before a more complete picture of the habitats (i.e. spatially extensive and temporally persistent) with evolution of flightlessness in the Hemerobiidae can be favourable abiotic environmental conditions (e.g. high humidity constructed. and moderated temperatures). The hemerobiids that occupy these habitats are flightless in both sexes. They must therefore live, feed, and breed in close proximity as dispersal is limited Acknowledgements to gressorial means. A second hypothesis that might explain the occurrence of I thank Norman D. Penny of the California Academy of flightlessness in hemerobiids is the 'habitat dimensionality' Sciences (CAS), San Francisco, and Ellis G. MacLeod for the hypothesis. This hypothesis suggests that taxa that occupy , loan of the material described here as Nusalala brachyptera. high dimensional (e.g. arboreal) habitats will exhibit a lower Francis G. Howarth, Steve Marshall, Gordon M. Nishida and frequency of flightlessness than those found in lower Charles W. O'Brien, provided unpublished field observations dimensional (e.g. terricolous) habitats. This hypothesis is based and/or other information regarding flightless hemerobiids. I on the idea that the capacity for flight is a more valuable asset thank each of them for their answers to my inquires. Oliver S. to arboreal species, which'must move efficiently among habitat Flint, Ron McGinley, Gary Miller and Kady Tauber kindly substrates in three dimensions, than it is for ground-dwelling reviewed earlier drafts of this paper. species, which move primarily in two dimensions. The twin observations that flightless hemerobiids have been derived from volant ancestors, and that the transition from volantry to References flightlessness was paralleled by an ecological shift from arboreal to terricolous habitats, are strikingly concordant with the central concept of this hypothesis. Aspock, H., Aspock, U. & Holzel, H. (1980) Die Neuropteren Europas. Because of the general terms in which these models are 2 vols. Goecke and Evers, Krefeld, West Germany. 495 and 355 pp. Aspock, H., Aspock, U. & Rausch, H. (1991) Die Raphidiopteren der couched, they are useful for constructing frameworks within Erde. 2 vols. Goecke and Evers, Krefeld, Germany. 730 and 550 pp. which the general evolution of flightless can be viewed. But, Aspock, U. & Aspock, H. (1985) Die Berothiden Australiens (und they are not too helpful for identifying the specific selective Neuseelands) 11: Die Genera Trichoma Tillyard, Trichoberotha pressure(s) that may have provided the specific impetus(es) for Handschin, Protobiella Tillyard und Austroberothella n. g. the evolution of flightlessness in hemerobiids. The models are, (Neuropteroidea. Planipennia. Berothidae). Zeitschrift der also, not mutually exclusive, and elements of both may be Arbeitsgemeinschafr Osterreichischer Entomologen, 36 (1984), applicable to the evolution of flightlessness in hemerobiids. 65-85. 'Why' questions are notoriously difficult to answer with Aspock, U., Aspock, H. & Rausch, H. (1992) Rezente Siidgrenzen certainty in biology; however, some clues to the ultimate der Ordnung Raphidioptera in Amerika (Insecta: Neuropteroidea). causation of the ecological shift from arboreality to Entomologia Generalis, 17, 169-184. Barnard, K.H. (1940) Additional records, and descriptions of new temcolousness, and hence flightlessness, in hemerobiids may species, of South African alder-flies (Megaloptera), may-flies be contained in the observation, noted by Penny & Sturm (Ephemeroptera), caddis-flies (Trichoptera), stone-flies (Perlaria), (1984), that most (10 of 11) known species of flightless and dragon-flies (Odonata). Annals of the South African Museum, hemerobiids are characteristic of insular and/or montanelalpine 32, 609-66 1. environments. This correlation may ultimately be attributable Burmeister. H.C.C. (1839) Handbuch der Entomologie. Band 2, Abt. to the fact that insular and high-elevation faunas are typically 2. Enslin, Berlin. (pp. xii + [397]-1050 + [4]).

O 1996 Blackwell Science Ltd, Systematic Entomology, 21, 343-352 352 John D.Oswald

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Bibliography of the Neuropterida Reference number (r#): 8705

Reference Citation: Oswald, J. D. 1996 [1997.01.??]. A new brachypterous Nusalala species from Costa Rica, with comments on the evolution of flightlessness in brown lacewings (Neuroptera: Hemerobiidae). Systematic Entomology 21:343-352.

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File: File produced for the Bibliography of the Neuropterida (BotN) component of the Global Lacewing Digital Library (GLDL) Project, 2007.