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Local Adaptive Pigmentation in Asellus Aquaticus -Effects of UV-Radiation and Predation Regime Local adaptive pigmentation in Asellus aquaticus -effects of UV-radiation and predation regime. Johansson, Jonas 2005 Link to publication Citation for published version (APA): Johansson, J. (2005). Local adaptive pigmentation in Asellus aquaticus -effects of UV-radiation and predation regime. Limnology, Department of Ecology, Lund University. 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LUND UNIVERSITY PO Box 117 221 00 Lund +46 46-222 00 00 LOCAL ADAPTIVE PIGMENTATION IN ASELLUS AQUATICUS – EFFECTS OF UV-RADIATION AND PREDATION REGIME LOCAL ADAPTIVE PIGMENTATION IN ASELLUS AQUATICUS – EFFECTS OF UV-RADIATION AND PREDATION REGIME JONAS JOHANSSON Dissertation Lund 2005 A doctoral thesis at a university in Sweden is produced either as a monograph or as a collection of papers. In the latter case, the introductory part constitutes the formal thesis, which summarizes the accompanying papers. These have either already been published or are manuscripts at various stages (in press, submitted or in ms). Cover: photos by Jonas Johansson (front) and Anders Hargeby (back) Layout: Gunilla Andersson/ZooBoTech & GrafikGruppen Proofreading: Jonas Johansson Printed by Xanto Grafiska AB, S Sandby ISBN 91-7105-218-6 SE-LUNBDS/NBLI-05/1057+82pp Contents Page Local adaptive pigmentation in Asellus aquaticus 7 – effects of UV-radiation and predation regime Svensk sammanfattning 21 Tack m.m. 23 This thesis is based on the following papers: IHargeby, A., Johansson, J. and Ahnesjö, J. 2004. Habitat-specific pigmentation in a 29 freshwater isopod: adaptive evolution over a small spatiotemporal scale. – Evolution 58: 81–94. II Johansson, J., Hargeby, A., Marklund, O. and Hertonsson, P. Effects of individual 45 pigmentation on survival and behavior of Asellus aquaticus L. exposed to UV-radiation. – Submitted. III Johansson, J. Predator-prey interactions between a damselfly larvae and a freshwater 55 isopod. – Manuscript. IV Johansson, J. and Hargeby, A. Predatory effects of perch (Perca fluviatilis) on size 67 structure, activity and pigmentation of the freshwater isopod Asellus aquaticus. – Manuscript. Paper I is reprinted with permission from the publisher. LOCAL ADAPTIVE PIGMENTATION IN ASELLUS AQUATICUS – EFFECTS OF UV-RADIATION AND PREDATOR REGIME INTRODUCTION and caves. In dense stands of vegetation Asellus One of the objectives of this thesis was to explore densities can exceed 10,000 individuals per contemporary evolution of locally adaptive pig- square meter (Hargeby 1990). Generally Asellus mentation in a freshwater isopod, and the mech- is regarded as a detritivore (Adcock 1982, Smock anisms behind the adaptation. Isopods are and Harlow 1983), feeding on dead organic mat- known to vary considerably in pigmentation be- ter and the bacteria and fungi associated with the tween habitats (Steiner at al. 1977, Henry et al. material. However, Asellus can also be a grazer, 1996, Turk et al. 1996, Hargeby et al. 2005), and feeding on plant tissue and periphyton (Marcus studies of contemporary evolution are valuable et al. 1978, Arakelova 2001). Invertebrate preda- because they provide opportunity to observe eco- tors as well as waterfowl, and fish (Berglund logical conditions that influence natural selec- 1968, Rask and Hiisivuori 1985) can prey upon tion. The adaptive pigmentation in the studied Asellus. isopod could be a response to a natural habitat alteration, in terms of e.g. food and selection pressure, since the adaptation occurred following SPATIAL AND TEMPORAL VARIATION IN a colonisation of a newly established habitat. Fac- PIGMENTATION tors behind the adaptive change such as the ge- Lake Krankesjön and Lake Tåkern are two shal- netic base of pigmentation, habitat choice, and low Swedish lakes with historical records of struc- selective predation were accounted for. Moreo- tural shifts between periods with clear water and ver, predation is a strong selective force on fresh- abundant submerged vegetation and periods with water invertebrate prey traits and behaviour dominance of phytoplankton and turbid water (Wellborn et al. 1996). Thus, effects of two com- (Blindow 1992). The two alternative states, with mon predators on isopod size dependent anti- either macrophyte or phytoplankton dominance, predator traits and behaviour, survivor, and the are stabilized by biotic and abiotic feedback effect of structural complexity on predation effi- mechanisms, resulting in episodic shifts over a ciency, were also explored. Finally, I examined few years when the submerged vegetation ex- the effect of an abiotic factor, UV-radiation, on pands or disappears (Scheffer et al. 1993). In Lake Asellus behaviour and tolerance. Krankesjön and Lake Tåkern each state tends to last for several years (Blindow et al. 1993). For benthic invertebrates, including Asellus, the ex- STUDY ORGANISM pansion of submerged vegetation during a shift Asellus aquaticus is a very common invertebrate from phytoplankton to macrophyte dominance is in Swedish freshwaters and can be found in vari- likely to change the light climate, food-source ous habitats such as small ponds, eutrophic lakes (periphyton vs. detritus) as well as predation re- 7 Local adaptive pigmentation in Asellus aquaticus gime (Scheffer 1998; Jeppesen et al. 1998 and ref- average pigmentation was lighter in Chara com- erences therein). Asellus is highly exposed to pre- pared to reed. dation from fish in unvegetated areas (Petridis The change in Asellus pigmentation that oc- 1990), and during the periods without sub- curred in the Chara habitat over the 13-year peri- merged vegetation Asellus were most likely re- od could be an example of local adaptive evolu- stricted to the reed belts surrounding the two tion. Many studies have documented local adap- lakes. However, when the submerged vegetation, tive evolution (Merilä et al. 2001) although the mainly different stonewort species (Chara spp.), underlying time scale is often unknown. The expanded Asellus colonised the re-established veg- change also corresponds with previous observa- etation. In Lake Krankesjön, Chara started to re- tions of contemporary adaptive evolution in other colonise the lake bottom in the mid 1980s and natural populations. Contemporary adaptation samples from 1987 showed that Asellus from tends to fall into two general categories (I) coloni- Chara beds exhibited similar pigmentation as zation of new environments, and (II) local adap- those found in nearby reed stands (Paper I; Figure tations in heterogeneous environments and meta- 1). By contrast, in 2000 Asellus in Chara beds population structure (Reznick and Ghalambor were significantly lighter pigmented than Asellus 2001). The ecological processes associated with from nearby reed stands. Thus, there had been a the re-colonization of Chara include exposure to reduction in pigmentation after the expansion of new food source, a new biophysical environ- Chara beds. A similar pattern of differences in ment, and new sets of predators and competitors. pigmentation was also found in Lake Tåkern (Pa- In contrast to several of the case studies of con- per I). Moreover, in Lake Tåkern samples taken at temporary evolution, the environmental change a reed islet situated in-between the Chara and the in the present system was not associated with re- reed belt showed intermediate pigmentation of cent anthropogenic causes. The mechanisms be- Asellus (Paper I). The variability in pigmentation hind the structural shifts in the lakes vary, and was also higher at the islet compared to the other may be multi-causal, and not necessarily driven sites. It should be mentioned that there were not by anthropogenic disturbances (Scheffer 1998). only light pigmented Asellus in the Chara and Therefore, the change in Asellus pigmentation dark pigmented in the reed. In both habitats there could be an adaptive response to a natural habitat were a continuous scale of pigmentation, but the change. FIG. 1. Pigmentation (means+s.d.) in gravid females of Asellus from a Chara site and an adjacent reed site in Lake Krankesjön in May 1987, and from four Chara (S1–S4), and four reed sites (R1–R4) in May 2000. Numerals denote sample size. 8 Local adaptive pigmentation in Asellus aquaticus POSSIBLE SELECTIVE FORCES BEHIND THE den, experiment in which we crossed different DIFFERENCES IN PIGMENTATION combinations of dark and light pigmented Asel- lus. The results indicated a genetic base for Asellus Below I will discuss possible explanations for the pigmentation. Two dark pigmented parents pro- change in Asellus pigmentation that occurred in duced a darker offspring than two light pigment- the Chara. In
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