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Functional Morphology of the Larval Mouthparts of Panorpodidae Compared with Bittacidae and Panorpidae (Insecta: Mecoptera)

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Functional Morphology of the Larval Mouthparts of Panorpodidae Compared with Bittacidae and Panorpidae (Insecta: Mecoptera) Org Divers Evol (2015) 15:671–679 DOI 10.1007/s13127-015-0225-7 ORIGINAL ARTICLE Functional morphology of the larval mouthparts of Panorpodidae compared with Bittacidae and Panorpidae (Insecta: Mecoptera) Lu Jiang1 & Bao-Zhen Hua1 Received: 10 February 2015 /Accepted: 15 June 2015 /Published online: 27 June 2015 # Gesellschaft für Biologische Systematik 2015 Abstract In Mecoptera, the larvae of Bittacidae and morphological and biological diversity (Byers and Thornhill Panorpidae are saprophagous, but the feeding habit of larval 1983; Byers 1987, 1991; Grimaldi and Engel 2005;Maetal. Panorpodidae remains largely unknown. Here, we compare 2009, 2012). The feeding habits of adult Mecoptera vary the ultramorphology of the mouthparts of the larvae among among families (Palmer 2010): predacious in Bittacidae (Tan the hangingfly Bittacus planus Cheng, 1949, the scorpionfly and Hua 2006;Maetal.2014b), phytophagous in Boreidae Panorpa liui Hua, 1997, and the short-faced scorpionfly and Panorpodidae (Carpenter 1953; Russell 1982;Beuteletal. Panorpodes kuandianensis Zhong, Zhang & Hua, 2011 to 2008;Maetal.2013), and saprophagous in Panorpidae, infer the feeding habits of Panorpodidae. The molar region Apteropanorpidae, Choristidae, Eomeropidae, and of Panorpodidae is glabrous, lacking the long spines for filter- Meropidae (Palmer and Yeates 2005; Palmer 2010; Huang ing (preventing larger particles from entering the pharynx) as and Hua 2011). The knowledge of the feeding habits of larval found in Bittacidae or the tuberculate teeth for grinding as Mecoptera, however, is still fragmentary. present in Panorpidae. The mandibles of Panorpodidae are The larvae of Mecoptera are morphologically diverse unsuitable for grinding, and most likely, larval Panorpodidae and inhabit a wide range of habitats (Byers 1987, 1991). have different feeding habits than larval Bittacidae and The larvae of Nannochoristidae are campodeiform and live Panorpidae. The diversity of the larval feeding habits in in the substrate of shallow streams (Pilgrim 1972;Beutel Mecoptera and its evolutionary advantage are briefly et al. 2009; Fraulob et al. 2012).ThelarvaeofBoreidaeare discussed. scarabaeiform and creep on or bore in live liverworts (Cooper 1974; Russell 1982). The larvae of Choristidae, Keywords Panorpodidae . Bittacidae . Panorpidae . Larva . Apteropanorpidae, Bittacidae, and Panorpidae are Mouthparts . Feeding habits eruciform and have an edaphic lifestyle (Miyaké 1912; Setty 1940;Byers1987, 1991; Tan and Hua 2008, 2009; Jiang and Hua 2013;Jiangetal.2015).Thelarvaeof Panorpidae are either epedaphic (living on soil surface as Introduction of Panorpa obtusa) or euedaphic (living underground as of Neopanorpa lui)(JiangandHua2015). However, the feed- Mecoptera is a small order of holometabolous insects, com- ing habits of larval Panorpodidae remain largely unknown posed of nine extant families, and exhibiting a high degree of to date, although the morphology of the larvae is known (Carpenter 1953;Byers1997;Pollmannetal.2008;Jiang et al. 2014). * Bao-Zhen Hua Mouthparts are closely associated with the feeding [email protected] habits of insects (Stehr 1987; Labandeira 1997;Jervis 1998; Smith and Capinera 2005). The larval mouthparts 1 of the scorpionfly Panorpa communis L. (Steiner 1930; State Key Laboratory of Crop Stress Biology for Arid Areas, Entomological Museum, Northwest A&F University, Grell 1938;Potter1938; Bierbrodt 1942), the snow Yangling, Shaanxi 712100, China scorpionfly Boreus hyemalis L. (Potter 1938), and the 672 L. Jiang, B.-Z. Hua hangingflies Apterobittacus apterus (MacLachlan) and Feeding experiments Bittacus pilicornis Westwood (Applegarth 1939; Setty 1940) were described using light microscopy. Recently, For observing the feeding behavior, larvae were reared in the larval mouthparts of Nannochoristidae (Beutel et al. plastic jars with humid soil at the bottom. The larvae of 2009), Bittacidae (Jiang et al. 2015), and Panorpidae Bittacidae and Panorpidae were daily provided with chopped (Chen and Hua 2011;Maetal.2014a; Jiang and Hua meal worms or housefly pupae on the soil surface. The larvae 2015) are studied using scanning electron microscopy. of Panorpodidae were provided additionally with locally col- However, morphological comparisons of mouthpart com- lected decayed leaves, stems, flowers, and roots. The feeding ponents in relation to their feeding habits have not been behavior was observed every 2 h during day time. conducted. Photographs were taken using a Nikon D90 digital camera The objective of this study was to unravel the feeding (Nikon, Tokyo, Japan). habits of Panorpodidae through comparing the larval mouth- parts of the short-faced scorpionfly Panorpodes Scanning electron microscopy kuandianensis Zhong, Zhang & Hua, 2011 with those of the hangingfly Bittacus planus Cheng, 1949 and of the For scanning electron microscopy (SEM), the larvae were scorpionfly Panorpa liui Hua, 1997, using scanning electron fixed in Carnoy’s solution for 12 h and preserved in 75 % microscopy. In addition, the feeding behavior of the larvae ethanol. The fixed larval mouthparts were dissected and seri- was observed both in the field and in the laboratory. ally dehydrated in a graded ethanol series, replaced by tertiary butanol, freeze-dried for 3 h, sputter-coated with gold, and examined under a Hitachi S-3400N scanning electron micro- Materials and methods scope (Hitachi, Tokyo, Japan) at 5 kV. Insect collecting Results Live adults of B. planus were captured using sweeping nets along the Jialing River source (34° 13′ N, 106° 59′ E, elev. Larval feeding habits 1500–1800 m) in the Qinling Mountains, Shaanxi Province of central China, from the middle of July to late August in 2013. The larvae of B. planus are saprophagous, feeding especially Adults of P. liui and P. kuandianensis were collected from on the inner semi-fluid tissues of dead insects. Larvae crawl Huabo Mountain (41° 06′ N, 125° 02′ E, elev. 650–1100 m) around appropriate dead insects, using their mandibles to in Liaoning Province, northeastern China, from late June to pierce and cut the cuticle; insert their heads into the body early August in 2010–2014. cavity to chew the soft tissues; and at the end leave an empty exoskeleton on the ground (Fig. 1). The larvae of P.liui are also saprophagous, consuming both Insect rearing the soft tissues and chitinous cuticle of dead insects. When the larvae find an appropriate dead insect, they burrow beneath it Adults of B. planus were reared in nylon gauze cages (40 cm× to feed on the carrion. The larvae usually pull small fragments 40 cm×60 cm) under semi-natural conditions (Tan and Hua into their burrow and feed on them underground. 2009). Live potted plants were provided for suspending The feeding habit of P. kuandianensis larvae remains un- adults. Live houseflies were supplied three times a day. A clear. During our rearing experiments, the larvae fed neither piece of wet tissue was put on the bottom of cages for egg on dead arthropods nor on plant leaves, stems, seeds, and collection. Eggs were collected twice a day and transferred roots. Although a dark line was visible through the transparent into plastic jars containing moist soil for overwintering. Larvae were collected from the soil surface in late March 2014. Adults of P. liui and P. kuandianensis were reared in pairs in plastic jars covered with a piece of gauze under natural conditions (Jiang and Hua 2013; Jiang et al. 2014). The jars were filled with 4–5 cm of humid soil for the deposition of eggs. The adults and larvae of P. liui were provided daily with chopped mealworms. Adults of P. kuandianensis received drops of honey twice a day. First-instar larvae were collected from inside the soil. Fig. 1 AlarvaofBittacus planus feeding on a housefly pupa Larval mouthparts of Panorpodidae 673 larval trunk (indicating the larvae had eaten some material), all kidney-shaped, fused from the original cardo and stipes, and the larvae died before molting within 19 days after hatching. connected distally to the galea and lacinia medially and bears the palp laterally. The galea is weakly sclerotized at the basal half and membranous at the apical half, which bears numerous Gross morphology of the mouthparts sensilla and microtrichia. The lacinia is quite small, broadly connected with the galea, and bears plenty of microtrichia on The larval mouthparts of Bittacidae, Panorpidae, and the mesal surface. The maxillary palp is three-segmented. Panorpodidae all are of the mandibulate (biting/chewing) The labium is somewhat reduced and is composed of a type, consisting of a labrum-epipharynx, paired mandibles postmentum, a prementum, and a pair of palpi (Fig. 2d–f: and maxillae, and a labium (Fig. 2). lb). The postmentum is merged with the cranium and bears The labrum is sub-rectangular, articulated proximally with two pairs of sensilla chaetica on the ventral surface. The the anterior region of the clypeus, and furnished apically with prementum is mesally divided by the orifice of the salivary two pairs of setae (Fig. 2a–c: lm). The epipharynx is situated duct and connected distally with a pair of two-segmented pal- on the ventral surface of the labrum (Fig. 2d–f: ep) and is pi, which bear various numbers of sensilla on the apex furnished with numerous microtrichia and various types of (Fig. 2d–f). sensilla arranged symmetrically. The paired mandibles are strongly sclerotized, curved in- ward, and cross each other apically (Fig. 2a–c: md). The man- Mouthparts of B. planus dible is typically dicondylic, bearing a notched ginglymus and a knob-like condyle on the dorsal and ventral corners, respec- The labrum is furnished apically with two pairs of labral setae tively (Fig. 2a–c: gg/cd). The mandible bears three sensilla and numerous microtrichia. The inner pair of setae is approx- trichodea on the lateral surface. imately two thirds the length of the outer pair (Fig. 3a:ls). The paired maxillae each consist of a cardo-stipes, a galea, The epipharynx is grossly subdivided into a terminal rect- a lacinia, and a palp (Fig. 2d–f: mx). The basal cardo-stipes is angular plate and a proximal triangular plate, both furnished Fig.
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