JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY 78(2), 2005, pp. 181–185 SHORT COMMUNICATION

Tracheal Gills of the Dobsonfly Larvae, or Hellgrammite Corydalus cornutus L. (Megaloptera: Corydalidae)

1 ALEXANDER BARCLAY,RICHARD W. PORTMAN, AND PEGGY S. M. HILL The University of Tulsa, Tulsa, Oklahoma 74104

The dobsonfly, Corydalus cornutus (L.), is a medium to large insect found throughout most of North America east of the Continental Divide from Mexico to Canada (Brown and Fitzpatrick, 1978; Contreras-Ramos, 1998). The order Megaloptera is thought to be one of the oldest orders to exhibit complete metamorphosis (McCafferty, 1983). Adults are typically between 25 and 70 mm long (Lehmkuhl, 1979), but the species ‘‘...spends most of its life cycle as a predaceous lotic larva known as the hellgrammite’’ (Brown and Fitzpatrick, 1978:1091). Hellgrammites are found along the edges of lakes and ponds, under stones in streams (Pennak, 1953) and in riffles (Brown and Fitzpatrick, 1978; Epperson and Short, 1987). They are well known to fishermen and valued as live bait. They can be kept for days in damp moss (Pennak, 1953), perhaps because the larvae have a complete set of spiracles along the body (McCafferty, 1983) that are functional out of water. The name ‘hellgrammite’ is of uncertain origin and has been defined as simply as ‘‘Insect larva used for bait’’ (Eisiminger, 1981:147). Hellgrammites are noted for several characteristics besides their being used for fish bait. They have one of the highest rates of productivity known for a predatory aquatic insect, with an increase in biomass (up to 1000 times from the first to the final instar) that is more comparable to that of primary consumers (Epperson and Short, 1987). This might be related to their ability, rarely reported for insects, to compensate for temperature fluctuations to maintain relatively constant metabolic rates year round and thus allocate a high level of energy to growth (Brown and Fitzpatrick, 1978). The larval period is as long as 2–3 years (Pennak, 1953; Knight and Simmons, 1975) but likely one year for early-hatching individuals in Texas (Brown and Fitzpatrick, 1978; Epperson and Short, 1987). Lastly, hellgrammites have tufts of tracheal gills (Pennak, 1953) in addition to spiracles in pairs along the base of the first seven abdominal segments (Fitch, 1982; Kinnaman et al., 1984) that appear to be an important respiratory adaptation (Lee, 1929; Carey and Fisk, 1965; Fitch, 1982; Kinnaman et al., 1984). Interest in the functional role of tracheal gills in respiration led to conclusions ranging from no known function to speculation that they were efficient respiratory structures (see review in McColl, 1943), or even used to trap food from the water stream that would later be collected by preening or combing the gills (Carey and Fisk, 1965). Hellgrammites introduced to hypoxic conditions protract their tracheal gills and begin ventilatory movements (Kinnamon et al., 1984). A correlation between oxygen content of streams where aquatic larvae are found and gill surface area was found in mayflies and caseless caddisflies (Dodds and Hisaw, 1924). After experiments on mayfly tolerance to low oxygen content of the water, McColl (1943) stated that in time of emergency, tracheal gills might be the single most important factor to determine life or death. Lee (1929) stated that even though little was known about the respiratory physiology of the Megaloptera, ‘‘It is inferred that gas exchange takes place chiefly through these structures’’ (119). Kinnaman et al. (1984) stated that although ‘‘movement of tracheal gills facilitates gas exchange across gills and integument ... no data are available on the sites of gas exchange in hellgrammites, nor have effects of gill movements on the rate of oxygen flux into the animal been measured’’ (26). This study was conducted to provide some details of the morphology of tracheal gills in the hellgrammite to contribute to the discussion of respiration in these well-known, but less well-studied, animals.

Material and Methods A late instar hellgrammite was collected in Spavinaw Creek, Mayes County, Oklahoma just below the Spavinaw Lake dam (368229590N, 95829520W) on 12 September 2003. In preparation for dissection, this individual was submerged in 95% ethanol until all body movement had stopped. A tracheal gill tuft from the first abdominal segment was removed, mounted on a scanning electron microscope stub with silver paste and allowed to dry for two days. It was then given a gold coating with a SC500A sputter coater (Emscope Laboratories Ltd.),

1 Corresponding author: Faculty of Biological Science, 600 South College, Tulsa, Oklahoma 74104; Phone: (918)631-2992; e-mail: [email protected] Accepted 13 January 2005; revised 28 January 2005 Ó 2005 Kansas Entomological Society 182 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

Fig. 1. Tracheal gill tuft from the first abdominal segment of a late instar larva of Corydalus cornutus at 203 magnification.

Fig. 2. Branching filaments of a tracheal gill tuft from the first abdominal segment of a late instar larva of Corydalus cornutus at 1003 magnification. VOLUME 78, ISSUE 2 183

Fig. 3. Highly convoluted surface of a single filament from a tracheal gill tuft from the first abdominal segment of a late instar larva of Corydalus cornutus at 10003 magnification.

Fig. 4. Dissected base of the tracheal gill tuft from the first abdominal segment of a late instar larva of Corydalus cornutus at 1503 magnification. 184 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

Fig. 5. One tracheal vessel at the base of the tracheal gill tuft from the first abdominal segment of a late instar larva of Corydalus cornutus at 10003 magnification. Note the ribbed structure of the vessel. dried for 30 min and viewed with a Hitachi S2300 scanning electron microscope. Five images with magnification from 320 to 31000 were photographed.

Results The hellgrammite was able to survive for approximately 28 hours after being submerged in 95% ethanol. It was observed over the first two hours after being introduced to the solution and then again at five hours. It ceased movement some time between five and 22 hours but was still alive at 28 hours when it was dissected and the first tracheal gill was removed. During the first five hours the tracheal gills were noted to move in pulses as rapid as twice per second. These tracheal gills of C. cornutus have been noted to beat in a wave in the following sequence: segment 3 first, then 4, 5, 6, 7, 2 and 1 (Fitch, 1982; Kinnaman et al., 1984); although, this pattern may not persist in circumstances of oxygen or temperature stress (Carey and Fisk, 1965). The sequence is rhythmic and repeated from 25 to 120 times per minute (Carey and Fisk, 1965; Fitch, 1982). SEM examination of the isolated tracheal gill at 203 magnification showed a hair-like tuft of filaments extending from a base of larger vessels (Fig. 1). A closer view of the filaments at 1003 magnification shows that the smallest branches are about 20 lm in diameter (Fig. 2). A close-up of a single filament at 10003 reveals a high level of convolution of the surface of the filament (Fig. 3). Dissection of the base of tracheal gill filaments at 1503 magnification shows the aggregation of larger vessels at the base of the filaments (Fig. 4), and a closer view at 10003 shows the inside of a single vessel from Fig. 4 with the characteristic supporting ribs of terrestrial insect tracheae (Fig. 5).

Discussion The tracheal system of insects has allowed them to efficiently exchange gases with the environment to survive ‘‘...but also for such energy consuming activities as rapid locomotion and flight’’ (Lee, 1929:215). Further, ‘‘So far as is known all water inhabiting insects are descended from terrestrial forms and are only secondarily aquatic’’ (Lee, 1929:226). In the dobsonfly larva, both spiracles and tracheal gills lead into the tracheal system that distributes oxygen throughout the hellgrammite’s body. Hellgrammites fan or pulse these tracheal gills VOLUME 78, ISSUE 2 185 rhythmically in a manner consistent with promoting increased diffusion of gases across the gill membranes. The surfaces of the gill filaments are highly convoluted in a manner that increases surface area for this gas exchange. The tracheae leading to the gill filaments appear to have sufficient support to allow them to withstand pressures required to passively move oxygen in from the medium, rather than losing gases to the surrounding water. Although our study did not test the physiological exchange of gases across tracheal gills, the morphological evidence presented here supports the working hypothesis that tracheal gills are not only functional, but play an important role in gas exchange in hellgrammites. Further study will answer questions of how these structures facilitate respiration in this fascinating insect.

Acknowledgments We thank H. Wells for collection of the specimen and for review of the manuscript.

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