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Surviving Submerged—Setal Tracheal Gills for Gas Exchange in Adult Rheophilic Diving Beetles

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Surviving Submerged—Setal Tracheal Gills for Gas Exchange in Adult Rheophilic Diving Beetles JOURNAL OF MORPHOLOGY 270:1348–1355 (2009) Surviving Submerged—Setal Tracheal Gills for Gas Exchange in Adult Rheophilic Diving Beetles Siegfried Kehl* and Konrad Dettner Department of Animal Ecology II, University of Bayreuth, 95440 Bayreuth, Germany ABSTRACT The gas exchange in adult diving beetles 2002). Adult Dytiscidae (predaceous diving beetles) (Coleoptera: Dytiscidae) relies on a subelytral air store, are often used as a prime example of aquatic which has to be renewed in regular intervals at the insects having a transportable air store for respi- water surface. The dive duration varies from a few ration. This air store in the subelytral cavity, must minutes to 24 h depending on the species, activity, and be renewed at regular intervals at the water sur- temperature. However, some species remain submerged for several weeks. Stygobiont species do not ascend to face (Alt, 1912; Wesenberg-Lund, 1912; Ege, 1915; the surface and gas exchange of these species remains Rahn and Paganelli, 1968; Gilbert, 1986; Wichard unclear, but it is assumed that they require air filled et al., 2002; Balke, 2005). The spiracles of the voids for respiration or they use cutaneous respiration. adult beetles open into the subelytral cavity (Gil- In this study, we investigate the gas exchange in the bert, 1986). For gas exchange, adult Dytiscidae running water diving beetle Deronectes aubei, which break the water surface with the tip of the abdo- survive submerged for over 6 weeks. The diffusion dis- men and atmospheric air enters the subelytral cav- tance through the cuticle is too great for cutaneous res- ity and flows into the emptied tracheae. During piration. Therefore, the dissolved oxygen uptake of sub- diving most Dytiscidae often press an air bubble merged beetles was determined and an oxygen uptake out of the subelytral cavity which functions as a via the rich tracheated elytra was observed. Fine struc- ture analyses (SEM and TEM) of the beetles showed physical gill or, more precisely, as a compressible tracheated setae mainly on the elytral surface, which gas gill (Rahn and Paganelli, 1968). The dive dura- acts as tracheal gills. Prevention of the air bubble forma- tion varies from a few minutes to 24 h depending tion at the tip of the abdomen, which normally act as on species, activity, and water temperature physical gill in Dytiscidae, resulted in no effect in oxy- (Madsen, 1967; Calosi et al., 2007). For example, gen uptake in D. aubei, but this was the sole way for a Hydroporus palustris can remain three hours sub- submerged Hydroporus palustris to get oxygen. The merged at 208C water temperature before it shows setal gas exchange technique explains the restriction of signs of oxygen deficiency (Gilbert, 1986). How- D. aubei to rivers and brooks with high oxygen concen- ever, some species remain submerged for very long tration and it may also be used by subterran living div- periods. Hydroglyphus hamulatus remains sub- ing beetles, which lack access to atmospheric oxygen. The existence of setal tracheal gills in species in running merged in an oxygen-rich lake for 10 weeks water which are often found in the hyporheic zone and (Meuche, 1937) or Oreodytes sanmarkii, Nebriopo- in stygobiont species supports the known evolution of rus depressus, and Stictotarsus duodecimpustula- stygobiont Dytiscidae from species of the hyporheic tus for more than 35 days (Madsen, 2007). Stygo- zone. For species in running water, setal tracheal gills biont species (species of groundwater) do not could be seen as an adaptation to avoid drifting down- ascend to the surface for gas exchange (Castro and stream by the current. J. Morphol. 270:1348–1355, Delgado, 2001) and the respiration of subterranean 2009. Ó 2009 Wiley-Liss, Inc. water beetles is still not understood. Some authors assume subterranean dytiscids use air filled voids KEY WORDS: Dytiscidae; elytra; oxygen uptake; for respiration (e.g., Spangler and Decu, 1999; respiration; tracheation Cooper et al., 2007) and others propose cutaneous respiration (Ue´no, 1957; Ordish, 1976; Smrzˇ, INTRODUCTION Various insect taxa returned from terrestrial to *Correspondence to: Siegfried Kehl, University of Bayreuth, Ani- aquatic environments secondarily and evolved var- mal Ecology II, Universita¨tsstr. 30, 95440 Bayreuth, Germany. ious adaptations for gas exchange independently E-mail: [email protected] from each other. The tracheal system of aquatic insects can be either closed or open and insects can Received 16 February 2009; Accepted 10 April 2009 use oxygen dissolved in water or atmospheric air Published online 28 May 2009 in for respiration (Resh and Solem, 1984; Pritchard Wiley InterScience (www.interscience.wiley.com) et al., 1993; Eriksen et al., 1996; Wichard et al., DOI: 10.1002/jmor.10762 Ó 2009 WILEY-LISS, INC. SETAL TRACHEAL GILLS IN DYTISCIDAE 1349 1981). Smrzˇ (1981) suggested gas exchange via the carefully spread over the elytra with a small brush, assuring intraelytral tracheae in subterranean species, that the legs and head were not covered. In the closed system, untreated specimens were first measured, then those with cov- because the elytra of stygobiont diving beetles are ered elytra and afterwards the synthetic resin was removed richly tracheated and the longitudinal tracheae and a control was measured again. Because of the low level of have a greater relative diameter compared to most oxygen uptake, two beetles were measured simultaneously. Af- epigeic species. Madsen (2007) described small air ter the beetles were placed in the respiration chamber, the oxy- bubbles on the elytral surface of submerged run- gen saturation was measured in intervals to avoid a down- wardly drifting signal due to oxygen consumption by the elec- ning water Dytiscidae and suggested an exchange trode. The oxygen saturation was measured for 60 min every 10 with the tracheal system of the elytra. The rheo- min for 1 min with an x-t chart recorder and the oxygen uptake philious diving beetle Deronectes aubei (Mulsant) was calculated over the last 30 min. A 1-mm gauze fixed with a was observed under laboratory conditions in oxy- rubber ring in the respiration chamber separated the beetles from the rotating stir bar. gen saturated water at 138C, it remained sub- In the flow through respirometer, oxygen uptake of D. aubei merged for more than 6 weeks without the access and H. palustris (Linnaeus) was measured under constant oxy- to atmospheric oxygen. This species normally lives gen saturation. The flow of the flow-through respirometer, a in fast running waters in mountainous and alpine glass tube (150 mm length and 16 mm diameter) connected to a regions under gravel and stones (Fery and Bran- water tank (modified from Hanke et al., 1980), was adjusted to 2 ml/min. Control and test water were collected in bottles and cucci, 1997) and sometimes deep in the streambed. the oxygen content was measured by Winkler titration accord- To investigate the gas exchange of D. aubei and a ing to the German standard protocol (DIN 38408, part 21, possible oxygen uptake via intraelytral tracheae, 1984). Oxygen uptake was calculated by the difference of oxy- oxygen uptake was measured with a flow through gen concentration of control and respiration chamber water. Because of the low levels of oxygen uptake groups of nine speci- and closed respirometer under laboratory condi- mens of D. aubei and 10 specimens of H. palustris were meas- tions. In addition, the fine structures of the elytra ured for 1 h. The mean oxygen uptake was calculated for a were examined with scanning electron microscopy single specimen in mg/h. For D. aubei, four series of oxygen (SEM) and transmission electron microscopy uptake measurements were conducted: oxygen uptake of (TEM) techniques. Comparison of the relative di- untreated specimens, oxygen uptake of specimens where the physical gill was prevented by covering the tip of the abdomen ameter of the intraelytral longitudinal tracheae of with synthetic resin, oxygen uptake of specimens with synthetic adephagan water beetles of different habitats pro- resin covered elytra, and a final control measurement where vided information about the occurrence of cutane- the synthetic resin was removed from the elytra. Individuals ous respiration in aquatic beetles. were placed in the respiration chamber for 1 h before respira- tion water was collected. This was not possible in H. palustris because the activity of the beetles and also the frequency of using the physical gill decrease with duration of the experi- MATERIALS AND METHODS ment, so that the respiration water was collected for 1 h, start- Electron Microscopy ing 10 min after placing the beetles in the respiration chamber. Therefore, for H. palustris, a first and second measurement of For SEM, elytra were dehydrated in ethanol series, air dried, untreated specimens was conducted without opening the respi- mounted on stubs, and sputter-coated with gold. The samples ration chamber. Afterwards, the beetles were measured with a were viewed and photographed using a Philips SEM (FEI XL covered pygidium and with covered elytra. 30 ESEM). For TEM, the elytra were fixed in 2.5% glutaraldehyde in 0.1 mol/l cacodylate buffer (pH 7.3) for 1 h, embedded in 2% aga- Relative Diameter of Longitudinal Tracheae rose and fixed again in 2.5% glutaraldehyde in 0.1 mol/l caco- The diameter of the intraelytral longitudinal tracheae was dylate buffer overnight. Elytra were washed three times in 0.1 measured using a microscope (4003 magnification) for 45 ade- mol/l cacodylate buffer for 20 min and osmicated in 2% osmium phagan water beetles of different habitats. In some species, the tetroxide for 2 h. Elytra were washed and stained in 2% uranyl elytra were bleached with potassium hydroxide. The maximum acetate for 90 min, dehydrated in an ethanol series (30, 50, 70, determined diameter of longitudinal tracheae and the length of 95, and 3 3 100%), transferred to propylene oxide and embed- the elytra of the respective species were used to calculate the ded in Epon 812 (Serva, Heidelberg, Germany).
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