On the Possible Myrmecophily of Nemopterinae Larvae (Neuroptera, Nemopteridae) by V.J
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55 On the Possible Myrmecophily of Nemopterinae Larvae (Neuroptera, Nemopteridae) by V.J. Monserrat & M.D. Martinez' ABSTRACf Field and laboratory studies of different species of Iberian ants with the eggs and larvae of Nemoptem bipennis and Lertha so.fiae (Neur optera: Nemopterldae: Nemopterlnae). suggest a previously unknown myrrnecophllous life-style In the larvae of this subfamily. A wide range of potentially edaphic prey was offered to newly hatched larvae. but growth occurred only when ant larvae were used as food. Furthermore. ant workers harvest Its eggs. as though they were seeds. and Introduce them Into their nest. Ant tolerance oflarvae inside the nest Is proved and discussed. and the acquisition of the colony odor or some other appeasement mechanisms against ants Is suggested. SImilarities In the ecological requirements of the Nemopterlnae Ima goes and harvester ants hav,e ,been observed and a coevolutionary process among plants (as seed producers). nemopterlnes (as plant pollinator Imago and ant-predator larva) and ants (as seed harvesters and predator lodgers) Is suggested. KEY WORDS: Myrmecophlly. larval-predation. Neuroptera. Nemopterlnae. coevolution. lNTRODUCfION Among the many myrrnecophllous arthropods deSCribed. which are symbiotic. commensals. or predators of ants. the order Neuroptera Is scarcely represented (Holldobler & Wllson 1990). Only larvae of the tribe Belonopteryglni (Chrysopldae) have been recorded as llvlng In colonies of ants. Other families such as Berothidae. Dllarldae. or Mantispldae are associated with other social Insects. as obligate larval predators oftermUe nymphs or of wasp and bee larvae (Parker & Stange 1965. Johnson & Hagen 1981. Brushweln 1987. Minter 1992). One of the most Interesting of the neuropterous famllies Is the Nemopterldae. which has specialized nectar and pollen eating Ima goes. It Is divided Into two subfamilies with very different morphology and habitats. The biology of the Croclnae subfamlly. with almost 50 species. Is well known Including larval stages. taxonomy. distribution IDepartamento de Biologia Animal I. Facultad de Blo)ogia. Uruversidad Complulense E-28040 Madrid. SPAIN 56 Sociobiology Vol. 26, No.1 , 1995 and phylogeny. This subfamily has been revised recently (Holzel 1975, Mansell 1986). In contrast, the Nemoptertnae contains almost 100 species, includtng some of the biggest and most spectacular of all Neuroptera (Fig. 1). The imagoes are usually abundant, have short emergence periods, have crepuscular and diurnal flying habits, and usually have pronounced endemisms and are restricted to a single habitat. Their taxonomy and systematics need revision, and there is surprisingly a very little data on the biology of most species (1Jeder 1967, Mansell 1973), and to date, there is very little information on the morphology and biology of preimagtnal stages in this subfamily. Eggs, first or last larval stage or pupae are only known on the Mediterranean Nemoptera bipennis (Dufour 1857, Navas 1919, Withycombe 1925, Monserrat 1985), N.coa (Troger 1993), a few references of N.sinuata (Popov 1963, 1973). There are also a few references about the Austra lian Chasmoptera hutti (Mathews 1947) and on the South Mrican Knersvlaktia nigroptera (Picker 1984), Palmipenna aeoleoptera (Picker 1987) and Derhynchia vansoni (Mansell 1973). Nemoptertnae larvae have always been found in the ground, living freely in loose sand, sometimes at a certain depth (l5-25cm) beneath the surface. Attempts to rear them have always falled, only Troger (1993) persuaded last instars to feed on wasp, butterfly and fly larvae and pupae, while some other poSSible prey, such as small arthropods, Tlpulids, Noctulds, or Tenebrionlds have been suggested. Pupation has been observed twice, also in the ground, 5-1 Ocm beneath the surface in the fleld or O.5-lcm beneath the surface in laboratory conditions (Mathews 1947, Mansell 1973, Troger 1993). The supposed predatory behavior of larvae in this subfamily and an edaphic life-style has long been suspected (Wheeler 1929). These have been conflrmed by some of the recent findings, but many other aspects of their biology and behavior remains unknown, such as relationships with other animals, life-cycle time, the number ofins tars and molts, and sources of food in the wild. In this paper, some new data are presented on the imagoes behavior, morphology of eggs, larval instars (reared in laboratory) and cocoon of the Iberian Nemoptera bipennis (Illiger) and Lertha so.fiae Monserrat. These provide new information on the larval biology and behavior of this subfamily, and demonstrate evidences of possible myrmecophily in the Nemoptertnae larvae. Figs. 1-5. 1, Morphology of a Nemopterinae imago,Lerlha sofiae; 2, Micropilar area,L.scfiae egg; 3, Newly hatched and recuperate eight months age larvae ofNemoptera bipennis; 4, Medium third instar larva of N.bipennis. eating an ant larva; 5, Enlargement of a portion of RgA. Monserrat & Martinez · Myrmecophilous Nemopterinae 57 58 Sociobiology Vol. 26, No. 1, 1995 MATERIAL & METHODS Eggs of Nemoptera bipennis were obtained from gravid females collected from different localities in Spaln during the last eight years and eggs of Lertha so.fiae from specimens collected in Spain (Almeria, Balanegra,20.VII.1991). Each female was Isolated in a plastic box of lOx 5 x 5cm, In order for her to oviposit. Some moisture, a few grains of commercial pollen and some fixed flowers were provided in each box. No records were made of temperature during the first years of unsuccessful attempts to rear larvae in the laboratory, but when an adequate feeding method was known, the monthly range of the temperatures of both years, under which the larvae were reared was noted in °c as follow: I: 14-21. II: 10-23, 1Il: 14-25, IV: 16-23, V: 19-32, VI: 15-37, VII:21-41, VIII:22-38, IX: 17-30, X: 14-22, Xl: 17-23, XlI:7-22. The photoperiod was taken to be a natural month, but In dark partial shade, not full light, and a relative humidity of 40-600A>. After birth, the larvae were Individually Isolated into plastic culture boxes of2 x 4.5 x 4.5cm, halffllled with sand. Newly hatched larvae of these species had an obvious predatory appearance (Fig. 3) and their soil dredging behavior confirmed an edaphlc life-style. Consequently soil fauna should constitute the usual diet. Nemopterins usually occur at high densities, so the larval food cannot be unusual or too temporal. However, because of their small size, different soil organisms (prefer ably non-predacious), as well as non-edaphlc soft ones such as aphids, and flies, beetle larvae or butterfly larvae, were buried in the sand, as possible prey for the newly hatched larvae. Food provision was mixed and renewed every 15 days. A wide range of prey was offered separately to different larVae, each kept isolated in an individual culture box. Prey included Nematoda (Rhabditlda: Rhabditldae) and the eggs, nymphs, larvae, pupae, co coon or imagoes of different Arthropoda (Acari: Oribatida; Thysanura: Leplsmatidae; Diplura: Japygidae; Collembola: Poduroidea; Dermaptera: Forflculidae; Embioptera: Emblldae; Isoptera: Kalotermitldae; Psocoptera: Psocomorpha; Homoptera: Aphididae; Coleoptera: Bruchldae, Tenebrionldae, Curculionldae; Diptera: Drosophilldae; lepi doptera: Tineidae, Pyralidae; Hymenoptera: Formicinae and Myrmicinae) (Table 1). Larvae moved and fed freely within the sand, and to study molting, during all stages of development, the sand was carefully sieved every 15 days, to look for possible exuvia. Laboratory experiments of possible interactions between ants and Table 1. List of the different prey offered to newly hatched Nemopterinae larvae, and the time (-) until their death (+) or pupation (PP). ;:: MONTHS 0 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 0 ..~ PREY '"~ ..!!!. NEMATODA (+J ;:: SOIL MITES (+J ..a. SPRING TAILS (+J ..~ SILVERFISH (+J N DIPLURA (+J ;:: EARWIG EGGS (+J '< EMBIOPTERA (+J 3 TERMITES - (+J 8 PSOCIDS (+J ";1: APH IDS 0- (+J ~ BEETLE LARVAE - (+J '"z FLY LARVAE (+J .. FLY IMAGOES (+J B MOTH LARVAE (+J ~ ANT LARVAE (PPJ ~ . ~ ANT PUPAE (+J .. ANT COCOON (+J ANT IMAGOES (+J ifl 60 Sociobiology Vol. 26, NO. I, 1995 eggs or lruvae were made using Chauvin type ant-culture cyllndrtcal boxes (l2cm In diameter x 5cm high), In which ant colonies were maintained and fed with a Bhatkar diet. Field expertments with nemoptertne eggs - lruvae and ants were carded out on different locations within the Murcia and Madrtd provinces, where 7 newly hatched lruvae were released on small plots of sand, Isolated by an open metallic cylinder 50cm long and 30cm In diameter, vertically engraved Into the sand. For hruvestlng expert ments, 10 Nemoptertnae eggs were placed near different ant-nests (In the field) and 5 eggs on the foraging surface of Chauvin ant culture boxes (In the laboratory). The ants used In these expertments are noted In Table 2. and ant lruvae used as food were taken In the field are noted In Table 3. RESULTS The eggs obtained were not adhesive and were Isolated Into small vials to observe their development time. The number of eggs laid was 0-13. x = 6 by L.so.fiae and 0-51, jf = 25 by N.bipennis. Electron microscope studies were made of several (Fig. 2) . A) Laboratory Experiments After 20-24 egg development days, the hatched lruvae rest for some minutes, then burrow head first, vertically Into the sand, to a depth of 5-lOcm, where they remain without further burrowing. When dis turbed, the lruva lay motionless, as If dead, for hours In any posture, Table 2: Ant species used, and time spent by workers, to harvest and to introduce in their nests (+) len (in field) or five (in Chauvin boxes) Nemoplerinae eggs layed near by their nests. (""": granivorous, .": omnivorous, *: flouidophagous ant species). DAYS ANT SPECIES 2 3 4 5 6 7 Messor barbarus"· + Messor stllJCto,·" + Lasius niger·· + + Lasius flavus·· + + Tetramoriumhispanicum ... + + Aphaenogasterseni!is·· + + lridomyrmex humilis·· + + Pheidole pallidula"" + + Tapinoma nigerimun u + + Camponotus Belhiops" + + + CamponotuslateraJis'" + + + Camponotuspilicomis·· + + + + + Plagiolepispygmaea" Monserrat & Martinez - Mynnecophilous Nemopterinae 61 Table 3.