EXPOSURE OF BENTHIC ANIMALS TO METAL SOURCES: CLUES FROM THEIR IRRIGATION BEHAVIOUR.

Céline Gallon, André Tessier* and Landis Hare

INRS-Eau, Université du Québec, C.P. 7500, Sainte-Foy (QC), Canada, G1V 4C7

*Corresponding author: andre_tessier@inrs-eau.uquebec.ca

ABSTRACT

Little is known about how freshwater animals build and irrigate their burrows. Such information is, however, important because it can elucidate the exposure of animals to trace metals as well as explain the contribution of these animals to metal cycling between sediments and the water column. Using oxygen microsensors positioned with a micromanipulator, we determined oxygen microprofiles across burrows of the alderfly Sialis velata (Megaloptera) as well as fluctuations in burrow oxygen over time. We related temporal patterns of oxygen concentrations in burrows to the behaviour of animals, as recorded on an infrared video camera.

INTRODUCTION

Many sediment-dwelling invertebrates dig below the thin oxic surface layer into anoxic sediment to build their burrows (Jorgensen & Revsbech, 1985). Since these animals require oxygen for respiration and because prolonged exposure to hydrogen sulfide is usually lethal, most irrigate their burrows with oxygenated overlying water. For some invertebrates, irrigating their burrow also serves to draw in particles on which they feed. Burrow irrigation by animals creates an oxic microenvironment in the surrounding sediment (Aller & Aller, 1986, Fenchel, 1996) that influences its chemical and biological properties (Aller & Aller, 1986).

We know little about the tube building and irrigation behaviour of benthic organisms or about how this biological activity influences sediment redox conditions. Although a small number of investigators have examined conditions around the tubes of marine animals (Fenchel, 1996; Forster & Graf, 1995; Jorgensen & Revsbech, 1985), only one such study has been conducted on the burrows made by freshwater invertebrates (Wang et al., 2000). Such information is important to elucidate animal exposure to trace metals and to understand the contribution of the microenvironments they create to the cycling of metals.

Current management strategies for metal-contaminated sediments assume that benthic animals take up their metals from the sediment. However, field experiments in two Canadian lakes (Warren et al., 1998; Hare et al., 2000) showed that burrowing insects took up the majority of their Cd from the water column overlying the sediment rather than from the sediment itself. These observations could be explained if these animals created their own oxic microenvironment that is different from conditions in bulk sediment. That is, the chemistry of water in their burrows resembled more that of the overlying water than that of bulk porewaters. Likewise, conditions in burrow walls would have resembled more those of surficial oxic sediment than those of bulk anoxic sediment. If this was the case, then these insect burrows could be considered an extension of the surficial sediment as has been shown for many marine burrowers (Aller & Aller, 1986).

We set out to examine the irrigation behaviour of larvae of the alderfly Sialis velata (Megaloptera) and to relate its behaviour to the oxygenation of its tube and sediment in its surroundings. Larvae of Sialis are widespread in the shallow portions of lakes and slow-flowing rivers (Evans & Neunzig, 1996) where they live in U-shaped burrows (Charbonneau & Hare, 1998) and feed on a variety of insects, annelids, crustaceans and molluscs (Evans & Neunzig, 1996). Given their large size (up to 2.5 cm), larvae of Sialis could be a major contributor to sediment bioturbation and bioirrigation.

METHODOLOGY

We conducted our experiments in darkness, to avoid stressing animals, in a walk-in environmental chamber that was maintained at a temperature of 10±1°C to prevent emergence of the insect (Roy & Hare, 1999). Larvae were obtained from Lake St. Joseph located close to Quebec City on the Canadian Shield. To view burrowing behaviour (Fig. 1), an individual Sialis velata larva was placed in a thin aquarium (thickness 6 mm) filled with L. St. Joseph sediment that had been sieved to remove large particles that might break an oxygen microelectrode. This aquarium was placed in a larger one (20.5 ´ 41 ´ 26 cm) filled with lake water that was bubbled continuously with air to maintain oxygen concentrations near saturation. The larvae were fed regularly with chironomids, up to four days prior to each experiment. Several oxygen microprofiles (25-µm vertical resolution) were obtained by moving, with a micromanipulator, an oxygen microelectrode from the sediment-water interface into the sediment and across the burrow. A two-point calibration of the electrode was made for each experiment between air-saturated water (100% air saturation in oxygen) and anoxic sediment (0% air saturation in oxygen) with the assumption of linearity. Measurements of O₂ concentrations at the exits of the burrow (see Fig. 1) were also made with a time resolution of 10 sec for extended periods of up to 24 h with microelectrodes connected to a data acquisition and control system. Simultaneously, visual observations of animal behaviour were made with an infrared video camera connected to a video recorder. This ensemble of instruments allowed us to associate measured variations in burrow O₂ concentrations with larval behaviour patterns.

RESULTS AND DISCUSSION

Sialis velata’s behaviour

We studied the larval behaviour of two individuals, each of them for a period of 24 hours, to quantify activities that might influence burrow oxygen. Larvae remained in their tubes at all times, generally in one spot (71.0 %; 89.6 % of the time). Three main types of displacement activity were observed: 1) walking forward or backward (3.8 %; 3.6 % of the time); 2) ventilation, consisting of undulations of the abdomen from anterior to posterior (2.4 %; 4.5 % of the time); and 3) lateral U-turns (0.3 %; 0.4 % of the time). The first two resulted in measurable variations in burrow O₂. The time between U-turns varied between 20 min and 6 h.

Temporal and spatial fluctuations of oxygen in the burrow

Figure 2 shows an example of the temporal variations in burrow O₂ concentration measured over a 24-h period. Large fluctuations in oxygen are evident, with peaks as high as 100 % oxygen saturation and valleys as low as 3 % saturation.

This pattern of peaks and valleys can be related in large part to the activity of S. velata (Fig. 3), as recorded on videotape. Ventilation or walking in the direction away from the microelectrode resulted in oxygen peaks because O₂-rich overlying water was drawn towards the microelectrode tip. Walking in the direction of the microelectrode results in a lowering of the oxygen concentration because O₂-poor water present within the burrow was pushed towards the microelectrode tip. Thus all animal movements, including walking and ventilation, contributed to tube irrigation. Subsequent to an oxygen peak, and in the absence of animal movement, a slow and continuous decline in oxygen can be attributed to its consumption by insect respiration as well as to the diffusion of oxygen into the burrow wall.

Our measurements suggest that oxygen concentrations vary along the length of the animal’s burrow. To verify this hypothesis, we recorded oxygen concentrations at both ends of a burrow (microelectrode positioning shown in Fig. 1). Oxygen concentrations at burrow ends fluctuated inversely of each other (Fig. 4), supporting our notion that there is strong spatial variation in burrow oxygen concentrations.

In conclusion, our study has demonstrated that Sialis velata larvae irrigate their burrow with oxygenated overlying water, hence creating an oxic microenvironment that varies temporally and spatially along their tube. Because of this, exposure of this insect to trace metals is more likely to come from metals in the overlying water column rather than those in sediment. Measurements of metal concentrations in overlying water, burrow water, and porewaters would be necessary to confirm this supposition. We suggest that work be conducted on other types of benthic animals, such as sediment feeders, to confirm the relationship between animal behaviour and burrow oxygen levels for a variety of species. Furthermore, measurements of oxygen consumption by both sediment and insects, as well as its variation with sediment type and temperature, would allow us to better model temporal patterns in burrow oxygen. Lastly, measurements of current velocity in burrows would provide us with a key element for determining the role that animals play in influencing fluxes between the sediment and the water column.

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