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M O D E S of D E F E N S E in N E M a T I N E Sawfly Larvae

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M O D E S of D E F E N S E in N E M a T I N E Sawfly Larvae Journal of Chemical Ecology. Vol. II. No. 8. 1985 MODES OF DEFENSE IN NEMATINE SAWFLY LARVAE Efficiency Against Ants and Birds JEAN-LUC BOEVÉ and JACQUES M. PASTEELS Laboratoire de Biologie animale et cellulaire \ Univer.'iité libre de Bruxelles 50, av. F.D. Rooseveit 1050 Bruxelles, Belgium (Received March 12, 1984; accepted November 29, 1984). Abstract—Ventral glands are common in nematine larvae (Hymenoptera: Symphyla), but they show various degrees of development and are functional for défense only in some species. In those species, volatile irritants are pro­ duced which are effective against ants. Alternative or complementary mech­ anisms against ants are the pubescence of Trichiocampus spp., the foam pil­ . lars constructed by Stauronema compressicornis, various movements of the abdomen, which occur independently of the glandular sécrétion in several species, immobility of the flat larvae of Nematinus luleus, and burrowing within plant tissues in gallicolous larvae or miners. Glandular development is r not clearly related to the appearancc of the larvae, either cryptic or apose­ matic. The sécrétion, even when it is produced in large amounts by species with well­developed glands, is only moderately efficient against great tits. Bright colors are f'ound in gregarious larvae; thèse were accepted only with reluctance by great tits and sometimes rejected, even species in which the ventral glands are reduced. We suggest that the various volatile irritants se­ creted by ventral glands are aimed primarily against insects (e.g., ants) and only secondarily against birds. Key Words—Sawfly larvae, Nematinae, Hymenoptera, Tenthredinidae, dé­ fensive sécrétion, ventral glands,mechanical défense, crypsis, aposematism, gregariousness, prédation, ants, birds. INTRODUCTION The soft bodied sawfly caterpillars are potentially easy prey for predators and parastoids. Indeed, Benson (1950) gives an impressive list of their potential 1019 0O98-O331/O8OO-lO19$O4..')O/O lO 1985 Plénum Publi.shing Coiporaluin 1020 BOEVÉ AND PASTEELS enemies, among them birds, ants, and parastoids. It is thus not surprising that diverse and elaborate défensive mechanisms are reported in this group (Benson, 1950); however, the évidence for thèse défenses is often anecdotal and detailed studies are few. Chemical défense has been thoroughly studied only in Neodiprion sertifer (Diprionidae) (Eisner et al., 1974), and in Perga affinis (Pergidae) (Morrow et al., 1976). Both species sequester host plant terpenes in, respectively, two and one pouches of the foregut, and they regurgitate thèse compounds when the larvae are disturbed. Recently, a toxic octapeptide was found in the Australian larva Lophyrotoma interrupta (Pergidae) (Williams et al., 1982). Herbivorous vertebrates are frequently poisoned by ingestion of thèse larvae. Nematine sawflies (Tenthredinidae) possess medioventral glands which can be everted when the larvae are alarmed. They release a fluid which, in some cases, is odorous (Yussa, 1922; Benson, 1950; Maxwell,1955; Alsop, 1970; Smith, 1970). The composition of the sécrétion has been studied for nine species in the gênera Nematus, Nematinus, Croesus, Pontania, and Pristiphora. The sécrétions contain one or more volatile compounds, such as benzaldehydes, monoterpenes, aliphatic aldéhydes, or acétates (Boevé et al., 1984; Bergstrôm et al., 1984). Thèse or similar compounds are commonly found in défensive sécrétions of insects and were classified by Eisner (1970) as nonspecific toxicants acting as irritants. Unidentified volatile compounds were also detected in Pla- tycampus luridiventris and in additional Nematus, Nematinus and Pristiphora species (unpublished). In this paper we study the interspecific variation in gland development and attempt to correlate it with larval appearance and with the efficiency of défense against two sorts of important predators: ants and birds. For convenience, the term aposematism will be used throughout the text, although this probable func- tion of the bright colors will be documented later in the paper. METHODS AND MATERIALS Larvae of 28 species were studied. They were ail collected in the field in Belgium and maintained in the laboratory on their natural host plant. Both sawfly and host-plant species are listed in Table 1. Lorenz and Kraus (1957) and Nigitz (1974) were used to identify the larvae, and Benson (1951, 1952, 1958) for the adults. Morphological studies were conducted on larvae fixed in Dubosq-Brasil and embedded in Paramat. The 7-/xm sections were stained with ferrie trioxy- hematein-phloxin-light green. Gland size was evaluated by measuring the area of the gland, colored with hemalum and mounted in Canada balsam. For each species, one to four last-instar larvae were dissected. The surface measured is in point of fact the surface of the glandular tissue as observed, for example, in DEFENSE IN SAWFLY LARVAE 1021 TABLE 1. APPEARANCE AND FEEDING HABITS OF SPECIES STUDIED" Appearance Distribution Host plants Investigations Croesus septentrionalis (L.) A G Alnus, Betula 1,2,3 C. vams (ViU.) C G-S Alnus 1,2,3 Hemichroa australis (Lepel.) C S Alnus, Betula 1,2,3 H. crocea (Geoffr.) A G Alnus, Betula 1,2,3 Mesoneura opaca (Kl.) C S Quercus 1 Nematinus luteus (Pz.) C S Alnus 1, 2, 3 Nematus bipartitus (Lepel.) C s Populus 1, 2,3 A^. hypoxanthus (Fôrst.) C s Populus, Salix 1 N. melanaspis (Hg.) A G Populus, Salix 1,2,3 N. melanocephala (Hg.) A G Salix 1,2,3 N. miliaris (Pz.) A G Salix 1,2,3 A'^ pavidus (Lepel.) A G Salix 1,3 N. salicis (L.) A G Salix 1,2 N. spiraeae (Zadd.) C Ag Aruncus 1,3 N. tibialis Newm. C S Robinia 1,2,3 Pachynematus scutellatus (Hg.) C S Picea 1,3 Platycampus luridiventris (Fall.) c S Alnus 1 Pontania vimimlis (L.) 9 7 Salix 1,3 Pristiphora aquilegiae (Voll.) c Ag Aquilegia 1 P. compressa (Hg.) c S Picea 1.3 P. conjugata (Dahlb.) A 6 Populus l P. erichsonii (Hg.) A G Larix 1 P. palHpes Lepel. C Ag Ribes 1, 2, 3 P. saxesenii (Hg.) C S Picea 1, 3 P. testacea (Jur) A G Betula 1,2,3 Stauronema compressicornis (Fabr.) C S Populus 1,2,3 Trichiocampus ulmi (L.) C S Ulmus 1, 2 T. vimimlis (L.) A G Populus 1,2,3 "A: aposematic, C: cryptic. G: gregarious, S: solitary, Ag: aggregated (see text), 1 : glandular morphol- ogy, 2: tests with ants, 3: test with great tits. Figures 1A-C, and which represents half the total glandular surface (see Figure ID). This measure was used as a rough approximation of thèse glands' défensive investment. Measurement of the volume of sécrétion would have been impossible in those species with reduced glands, and for which no détectable amount of sécrétion may be collected. Défensive efficiency against ants was observed by placing a larva wifh 20 Myrmica rubra workers in a square container (side: 10 cm). Two minutes were allowed for the ants to discover the larva. During the next 3 min, the number of ants attacking or surrounding the larva was counted every 20 sec on a video- recording of the experiments. This quantifies the interest of the ants for the larvae as prey and is considered to be inversely related to the larvae's défensive 1022 BOEVÉ AND PASTEELS ability. Depending on the availability of the sawfly species, one to six répétitions were made with separate larvae. For some species, additional observations were made with larvae on their host plant. A twig of the plant bearing a larva was then placed in the foraging area of a laboratory nest of Myrmica rubra. To test the efficiency of défense against birds, larvae were ofFered to two caged great tits (Parus major, one maie, one female) collected as adults in the field. In each session, a bird received in succession a mealworm, three full- grown sawfly larvae of the same species, and again a mealworm. Acceptance or rejection was recorded. The limited supply of biological material excludes a précise quantification of the différent larvae's palatability, and thèse tests were only carried out to show up possible trends in the birds' reactions. No bird was ever tested with more than three différent species per day, in order to avoid satiation. No bird ever refused a mealworm. Statistical tests are described in Siegel (1956). RESULTS Crypsis and Aposematism. Nematine caterpillars oflFer some of the best examples of both crypsis and aposematism. Two extremely cryptic species are illustrated in Figure 1 (A and B). The larva of Platycampus luridiventris (Figure lA) is green, flat, with latéral expansions, and is tightly appressed to the leaf surface. Thèse larvae are solitary and located on the underside of the leaf, often along the major veins when not feeding. Nematinus luteus larvae (Figure IB) are semicylindrical in shape. They are green with small white dots, mimicking the texture of the leaf The latéral margins are light, counteracting the shadow effect. They are solitary and live on the upper surface of the leaves. Brightly colored larvae are illustrated in Figure 1 (C and D). Larvae of Hemichroa crocea (Figure IC) feed in groups along the leaf-edge. They are light brown with black longitudinal Unes on each side. They usually curl the extremity of their abdomen ventrally. The larvae of Croesus septentrionalis are yellowish with black dots and a black head. They also feed in groups at the edges of the leaves. When disturbed, they raise their abdomens in a typical défensive posture (Figure ID). The appearance, cryptic or aposematic, and the feeding habits, gregarious or solitary, of the difl'erent species studied are given in Table 1. Gregarious habit is significantly correlated with bright coloration and crypsis with solitary habit (x^, P < 0.001). Solitary species, if not extremely cryptic as described above, are at least the same color as the leaf There is no association between type of appearance and taxonomic position; cryptic and aposematic larvae are often found within the same genus.
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