Chimney Construction by Chironomus Riparius Larvae in Response to Hypoxia: Microbial Implications for Freshwater Sediments
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J. N. Am. Benthol. Soc., 2005, 24(4):858±871 q 2005 by The North American Benthological Society Chimney construction by Chironomus riparius larvae in response to hypoxia: microbial implications for freshwater sediments PETER STIEF1 Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, 28359 Bremen, Germany LARISA NAZAROVA2 Ecological Faculty, Kazan State University, Kremlyevskaya Str. 18, 420008 Kazan, Russia DIRK DE BEER3 Max Planck Institute for Marine Microbiology, Celsiusstrasse 1, 28359 Bremen, Germany Abstract. Many shallow aquatic ecosystems with high nutrient loads experience periods of O2 depletion that evoke behavioral responses by macrobenthic organisms. The sediment-dwelling midge larva Chironomus riparius reduces its deposit-feeding activity and allocates more time to burrow ven- tilation during periods of hypoxia. We investigated another striking behavioral adaptation of this species, i.e., the elongation of U-shaped sediment burrows to chimneys that tower above the sediment surface. Chironomus riparius larvae gradually abandoned burrow construction and took up chimney construction when exposed to hypoxic conditions in laboratory microcosms. Microsensors were used to show that the chimneys were oxic sediment compartments that were periodically irrigated by the larvae with oxygenated surface water. O2 uptake rates per unit interface area were signi®cantly higher for chimneys than for the ¯at sediment surface. This observation was consistent with the dense colonization of the chimneys by bacteria. Chimneys may facilitate the larval acquisition of both O2 for respiration and microbial biomass for food. Given the mass abundance of C. riparius in many polluted and O2-de®cient habitats, the chimneys also may contribute signi®cantly to the patchiness of the benthic microbial community in terms of structure and function. In particular, the presence of chimneys might favor aerobic bacterial populations and their metabolism. Key words: Chironomidae, macrofauna, freshwater sediment, oxygen depletion, biogenic structure, sediment bacteria, diffusive oxygen uptake, animal±microbe interaction, sediment microcosm, micro- sensor. Periods of O2 depletion are common in many (e.g., in streams, ponds, and lakes, Hellmann aquatic ecosystems, including coastal upwelling 1994, Hamburger et al. 2000). regions (Levin 2003), fjords (Rosenberg et al. Benthic macro- and microorganisms must 2001), streams receiving sewage water (Hell- cope with the consequences of hypoxic events, mann 1994), and lake hypolimnia during tem- including shortage of O2 and accumulation of perature strati®cation (Hamburger et al. 2000). toxic substances (e.g., sul®de). Macrofauna may Common features of ecosystems susceptible to have physiological adaptations to these condi- hypoxia or anoxia are high nutrient concentra- tions (e.g., hemoglobin, Choi et al. 2000; anaero- tions, extensive organic sedimentation, and poor biosis, Hamburger et al. 2000), or they may re- exchange of bottom water (Gray et al. 2002, Lev- spond to hypoxia with changes in behavior. in 2003). High nutrient concentrations can be of Ventilation of sediment burrows is intensi®ed in natural origin (e.g., coastal upwelling regions, shallow waters (Leuchs 1986, Heinis and Crom- BruÈ chert et al. 2003), or they can result from mentuijn 1992), bioturbation activity is reduced anthropogenic eutrophication and pollution (Levin 2003), and sediment burrows are elon- gated above the sediment surface (Kon and Hi- 1 Present address: Department of Microbiology, In- daka 1983, Jùrgensen and Revsbech 1985). How- stitute of Biological Sciences, Aarhus University, Ny Munkegade, Building 540, 8000 Aarhus C, Denmark. ever, stress avoidance and behavioral compen- E-mail: peter.stief@biology.au.dk sation are of little importance to sediment bac- 2 E-mail addresses: larisa.nazarova@ksu.ru teria (except for mobile taxa). Instead, external 3 dbeer@mpi-bremen.de conditions regulate the metabolism of bacteria 858 2005] CHIRONOMID RESPONSE TO HYPOXIA 859 from full activity to dormancy. On the micro- uptake vary between inhabited and uninhabited scale, sediments can be considered model habi- sediments and the chimneys? Laboratory micro- tats for studying the bacterial response to hyp- cosm experiments were conducted using ho- oxia and anoxia because sharp O2 gradients de- mogenized freshwater sediments that were ex- termine the metabolic activity of aerobic and an- posed to different O2 concentrations (factor 1) aerobic bacteria within the sediment (Wieringa and to which C. riparius larvae (factor 2) were et al. 2000, Altmann et al. 2003). added or not. The number and size of burrows Here we present an example of the behavioral and chimneys were quanti®ed, total bacterial response of an abundant macrofaunal organism abundance was determined, and O2 concentra- to hypoxic conditions and the implications of tions were measured on a microscale in all treat- this behavior for bacterial colonization patterns ment combinations. in freshwater sediments. Chironomus riparius,a nonbiting midge with aquatic larval stages, is a Methods typical inhabitant of polluted and temporarily Origin of sediment and animals O2-de®cient shallow waters (Pinder 1986, Bair- lein 1989, Penttinen and Holopainen 1995). The Sediment was sampled in a freshwater ditch larvae regularly occur in masses, construct U- ;20 km west of KoÈln (North-Rhine Westphalia, shaped burrows within soft sediments, and feed Germany). The ditch runs through an intensely on the detritus particles and the attached bac- farmed area. The water column is characterized teria that are deposited onto the sediment sur- by high nutrient concentrations and transient O2 face (Pinder 1986). Chironomus riparius larvae tol- depletions. Large populations of various Chiron- omus species inhabit the silty and organic-rich erate O2 de®ciency because their hemolymph sediment of the ditch. A ¯at shovel (10 3 15 cm) contains hemoglobin with a high af®nity for O2 (Choi et al. 2000). The larvae also can switch to was pushed 10 cm into the sediment and the anaerobiosis, but they are less ef®cient than lar- load of sediment was lifted carefully out of its vae of other species (e.g., Chironomus anthracinus, place. Five loads were placed in a 10-L plastic Penttinen and Holopainen 1995, Hamburger et bucket and covered with 2 L of ditch water. The al. 2000). Chironomus riparius larvae increase sediment was sieved through a 1-mm-mesh 8 their undulation activity during periods of low screen, homogenized, and stored at 4 Cinthe dark until use. Egg masses of C. riparius were O2 concentrations in the water column (Leuchs 1986). Occasionally, the larvae elongate their provided by the Institute for Inland Water Man- burrows to reach above the sediment surface, a agement and Waste Water Treatment (RIZA) in behavior described as chimney-projecting behavior Lelystad, The Netherlands. Larvae were bred in 3 3 (Kon and Hidaka 1983, von Danwitz 1983). Bio- laboratory tanks (40 50 15 cm) ®lled with genic structures that pierce through the diffu- aerated, aged tap water and a 5-mm thick layer of sediment. A food suspension of ground sive boundary layer are thought to improve O2 availability for the inhabiting animal (Jùrgensen leaves of stinging nettle (Urtica sp.) and ®sh food (Trouvit, Tetramint) was added 3 times a and Revsbech 1983). Projecting biogenic struc- 8 tures also may generate small-scale habitat het- week. The culture was kept at 20 C under a erogeneity for the benthic microbial community light:dark cycle of 16:8 h. Chironomus riparius lar- by promoting advective nutrient transport and vae grew to a body length of 5 to 7 mm within rd trapping organic particles (Eckman and Nowell 10 to 15 d (3 -instar larvae) and were then 1984, Eckman 1985, Eckman and Thistle 1991, ready for use in the hypoxia experiments. A group of larvae was tested for its sensitivity to Soltwedel and Vopel 2001). a standard toxicant (K Cr O , Grootelaar et al. Our study addressed the following questions: 2 2 7 1996) before the actual experiment. The sensitiv- 1) Does a threshold O concentration induce the 2 ity of larvae taken from our culture lay within chimney-projecting behavior at the expense of the frame of acceptability for use in laboratory sediment burrow construction or is the response exposure experiments. to increasing hypoxia graded? 2) Does the erect shape of chimneys make them a residual oxic sediment compartment under hypoxic condi- Laboratory microcosms tions? 3) Are chimneys preferential sites for bac- Sediment was added to the center compart- 3 3 terial colonization? 4) How does sedimentary O2 ment (10 5 5 cm) of transparent aquaria 860 P. STIEF ET AL. [Volume 24 FIG. 1. Microcosms used for hypoxia experiments (side view). Numbered parts are acrylic aquarium (1), O2 macroelectrode (2), oxymeter (3), O2 control unit (4), magnetic valve (5), gas dispenser (6), stir bar (7), and magnetic stirrer (8). (20 3 5 3 10 cm; Fig. 1). The remaining volume trol treatments) were done in random order. of the aquarium was ®lled with aged tap water. Each run began with a 2-wk preincubation pe- Two stir bars, rotating on either side of the cen- riod during which 4 aquaria were ®lled with tral sediment compartment, homogenized the sediment and allowed to equilibrate at 100% air 8 water. The O2 content of the water body was saturation and 15 C in the dark. After this pre- rd regulated using an O2 control unit (Aquastar V incubation period, ®fty 3 -instar larvae (1 lar- 2.0, iks ComputerSysteme GmbH, Karlsbad, va/cm2) were added to each aquarium in ani- Germany). The O2 concentration of the water mal treatment runs. No larvae were added to was measured next to the sediment compart- aquaria in control treatment runs. Chironomus ri- ment with a calibrated macrosensor. A magnetic parius typically dug into the sediments in ,30 valve opened automatically and N2 gas was min. The O2 content of the aquaria was adjusted blown into the water via a gas dispenser when after 2 d of acclimation. One aquarium was kept O2 concentrations were above the selected value.