Differential responses of littoral communities to ultraviolet radiation in an alpine lake

Ecology, Jan, 1999 by Rolf D. Vinebrooke, Peter R. Leavitt

INTRODUCTION

The direct effects of ultraviolet (UV) radiation on aquatic food webs may be mediated by community- and species-specific sensitivities that result from differences in adaptive strategies and habitat conditions. UV radiation can inhibit algal photosynthesis (Moeller 1994), especially when phytoplankton are trapped in shallow epilimnetic waters (Vincent et al. 1984, Milot-Roy and Vincent 1994) without the opportunity for active avoidance (see Hader 1993). However, algae from different habitats show a wide range of sensitivities to UV radiation (Jokiel and York 1984, Xiong et al. 1996) with certain species producing photoprotective pigments (Carreto et al. 1990, Garcia-Pichel and Castenholz 1991). Similarly, epilimnetic zooplankton can be adversely affected by damaging solar radiation (Williamson et al. 1994) with differential sensitivities existing between heavily pigmented and pale species (Hairston 1980, Byron 1982, Ringelberg et al. 1984). UV radiation can also suppress benthic invertebrates (Bothwell et al. 1994) and the development of periphyton on hard surfaces (Bothwell et al. 1993, Vinebrooke and Leavitt 1996), such as on rocks (epilithon), as they lack adequate refuge from UV radiation. In comparison, UV radiation may not adversely affect sediment-dwelling algae (epipelon) that are capable of active avoidance via vertical migration through the sediments (Vincent et al. 1993).

The ecological impacts of UV-B (280-320 nm) and UV-A (320-400 nm) radiation can also differ. Recent research on the biological effects of UV-B radiation (see Vincent and Roy 1993, Karentz et al. 1994, Williamson 1995) show that the damaging effects of UV radiation increase exponentially as wavelengths decrease (Cullen et al. 1992). However, because total UV-A irradiance exceeds that of UV-B, UV-A radiation can have a greater overall impact on physiological processes (see Karentz et al. 1994). For example, Bothwell et al. (1994) reported that UV-A radiation suppressed periphyton more than shorter wavelengths, while UV-B radiation was more damaging to herbivorous chironomids. Moreover, UV-A radiation can counteract the adverse effects of UV-B radiation by activating repair processes (Quesada et al. 1995).

UV radiation may indirectly affect communities by altering biotic interactions, such as competition, herbivory, and predation. For example, phytoplankton that are outcompeted by periphyton for nutrients (Hansson 1988a) may benefit from suppression of periphyton by UV radiation. Alternately, inhibition of periphyton by UV radiation can be offset if grazers are more sensitive to UV radiation than are algae (Bothwell et al. 1994). In addition, herbivores may experience reductions in food availability because UV radiation can suppress algal abundance and promote the growth of less edible, thick-walled taxa (van Donk and Hessen 1994, Xiong et. al. 1996). Photoprotective pigments in prey species may increase their susceptibility to visually feeding predators (Morgan and Christy 1996). However, many indirect UV effects may be weak in unproductive systems where predator limitation is expected to be minimal (Menge and Sutherland 1987).

The ecological effects of UV radiation are also mediated by dissolved organic matter (DOM) content and lake morphometry. DOM is the primary attenuator of UV radiation in lakes (Scully and Lean 1994, Morris et al. 1995, Schindler et al. 1996). Low concentrations of DOM cause a spectral shift with increasing water depth owing to stronger attenuation of UV-B radiation (Kirk 1994). As well, photolysis of DOM by UV radiation can produce toxic byproducts, such as peroxides (Scully et al. 1996), and enhance the availability of resources to algae and bacteria (Wetzel 1992). Lake morphometry may set the limits on the effects of UV radiation as organisms are expected to exploit depth refugia in deep lakes (Williamson 1995). UV radiation might have a more pronounced impact in shallow waters where a higher proportion of biota are exposed to high UV irradiances.

The purpose of this study was to experimentally test for differential responses of shallow-water periphyton and phytoplankton to the direct and indirect effects of natural UV radiation. Our primary hypothesis was that sediment-dwelling periphyton (epipelon) should show higher tolerance of UV radiation than either phytoplankton or periphyton on hard surfaces (epilithon) because many epipelic taxa can potentially exploit a depth refuge from UV radiation. We also hypothesized that the effects of UV radiation would be wavelength- and taxon-specific with UV-B radiation damaging to small, translucent organisms more than large, pigmented species. Finally, we tested whether the magnitude of indirect UV effects on algae depended on the abundance of higher trophic levels, or on differential sensitivities between algae and invertebrates to UV radiation (see Bothwell et al. 1994).

TABLE 1. Select ice-free limnological conditions of Pipit Lake
(an alpine lake in Alberta, Canada) in 1995. Weekly measurements
were taken from the epilimnion during July and August.

Feature                                         Value

Total chlorophyll ([[micro]gram]/L)            0.4-0.8

TDN ([[micro]gram]/L)                           50-90

TDP ([[micro]gram]/L)                            3-5

Surface water temperature ([degrees] C)        3.2-9.2

1% UV-A radiation depth (m)                    4.1-12.4(*)

Percentage of lake bottom exposed
to [greater than]1% UV-A irradiance           15.0-37.7

1% UV-B radiation depth (m)                    1.2-3.9(*)

Percentage of lake bottom exposed
to [greater than]1% UV-B irradiance            5.7-14.5

Secchi depth (m)                               6.5-9.5

Maximum lake depth (m)                          20.6

Mean lake depth (m)                             12.6

DOC (mg/L)                                     0.5-1.3

Turbidity (NTU)                                  0.62

Conductivity ([[micro]second]/[cm.sup.2])        195

pH                                               8.1

* Estimates are based on 380-nm (UV-A) and 305-nm (UVB) wavelengths
and were derived from model equations that predicted diffuse
attenuation coefficients from measured DOC concentrations (see
Morris et al. 1995).