Sep 3, 2007 - several replicate metal stakes hammered into the stream bed. Macroinvertebrates were able ... natural acidity (Woodward et al. 2002, I). Finally ...
What are the effects of natural versus humancaused acidity on stream species diversity and ecosystem functioning? av
Zlatko Petrin AKADEMISK AVHANDLING som med vederbörligt tillstånd av Rektor vid Umeå universitet för avläggande av filosofie doktorsexamen i ekologi framläggs till offentligt försvar i Lilla hörsalen, KBC-huset, lördagen den 22 september 2007, kl. 10.00. Avhandlingen kommer att försvaras på engelska.
Examinator: Prof. Lennart Persson, Umeå universitet. Fakultetsopponent: Prof. Steve J. Ormerod, Cardiff School of Biosciences, Cardiff University, Cardiff, UK.
Department of Ecology and Environmental Science Umeå University Umeå 2007 Sweden
DOCUMENT NAME ORGANIZATION Department of Ecology and Environmental Science Doctoral dissertation Umeå University DATE OF PUBLICATION SE-901 87 Umeå, Sweden 03 September 2007 AUTHOR: Zlatko Petrin TITLE: What are the effects of natural versus human-caused acidity on stream species diversity and ecosystem functioning? ABSTRACT: Human activities have caused acidification of freshwater systems on a large scale resulting in reduced species diversity and ecological functioning in many lakes and streams. However, many naturally acidic freshwater systems have also been found, for instance in northern Sweden. In regions where such naturally acidic aquatic ecosystems have prevailed over evolutionary periods, species diversity and ecological functioning are not automatically impaired due to possible adaptation to the putatively adverse environmental conditions. I studied species diversity patterns and ecological functioning in anthropogenically acidified, naturally acidic, circumneutral, and limed streams to test the adaptation hypothesis and examine the ecological effects of variation in naturally acidic water chemistry. Species diversity was studied using benthic macroinvertebrates, while functioning was modelled using the decomposition rates of leaf litter. In accordance with the evolutionary species pool hypothesis, species richness was reduced more strongly in regions with anthropogenic than natural acidity when compared to circumneutral streams, supporting the adaptation hypothesis. In contrast, the patterns in ecological functioning along the pH-gradients did not differ between regions with anthropogenic and natural acidity, likely resulting from compensation: the biomass of tolerant taxa probably increased which thus rescued the loss in functioning otherwise mediated by the more sensitive taxa. Furthermore, the naturally variable acidic water chemistry clearly supported distinct macroinvertebrate assemblages, as was reflected in differing patterns of species diversity and ecological functioning. Such naturally acidic waters that were rich in dissolved organic carbon supported higher ecosystem process rates and lower species diversity than waters that contained little dissolved organic carbon. Upon liming naturally acidic streams microbial leaf decomposition increased, whereas shredding decreased along with changes in shredder abundances. The abundance of large caddisflies decreased, while the abundance of small stoneflies increased. The results suggest that various types of benthic macroinvertebrates with varying levels of adaptation and tolerance inhabited the hydrochemically variable naturally acidic streams. The distributions of macroinvertebrates in response to different pH levels and differences in acid quality and how these distributions translate into varying patterns of species diversity and ecological functioning are worthy of further investigation. This will likely improve our understanding of how such naturally acidic streams and their biota can be successfully managed. KEY WORDS: acid rain, aquatic insects, biodiversity, ecosystem function LANGUAGE: English NUMBER OF PAGES: 25 + 5 papers ISBN: 978-91-7264-345-1 SIGNATURE:
DATE: 09 August 2007
What are the effects of natural versus humancaused acidity on stream species diversity and ecosystem functioning?
Zlatko Petrin
Department of Ecology and Environmental Science Umeå University Umeå 2007
Department of Ecology and Environmental Science Umeå University SE-901 87 Umeå, Sweden
Copyright © 2007 by Zlatko Petrin ISBN: 978-91-7264-345-1 Printed by VMC, KBC, Umeå University, Umeå, 2007
CONTENTS List of papers.................................................................................................................... 1 Introduction...................................................................................................................... 2 Objectives...................................................................................................................... 4 Methods ............................................................................................................................ 4 Study regions................................................................................................................. 4 Study sites ..................................................................................................................... 5 Water chemistry ............................................................................................................ 5 Species diversity............................................................................................................ 5 Ecological functioning................................................................................................... 6 Data analyses................................................................................................................. 6 Results and discussion ..................................................................................................... 7 Effects of anthropogenic versus natural acidity............................................................. 7 Effects of varying naturally acidic water chemistry ...................................................... 9 Effects of liming naturally acidic streams ................................................................... 10 Summary and conclusions............................................................................................. 11 Future directions............................................................................................................ 11 Acknowledgements ........................................................................................................ 12 References....................................................................................................................... 12 Thank you! ..................................................................................................................... 18
Appendices I – V
Species diversity and functioning in naturally acidic streams
LIST OF PAPERS This thesis is a summary and discussion of the following papers, which are referred to in the text by their Roman numerals. I
Petrin, Z., Laudon, H. and Malmqvist, B. 2007. Does freshwater macroinvertebrate diversity along a pH-gradient reflect adaptation to low pH? Freshwater Biology 52: doi:10.1111/j.1365-2427.2007.01845.x.
II
Petrin, Z., Laudon, H. and Malmqvist, B. Do natural acidity and anthropogenic acidification have different effects on species diversity and ecosystem functioning? (manuscript)
III
Petrin, Z., Englund, G. and Malmqvist, B. Species richness, but not ecosystem functioning, is lost at a higher rate in recently acidified than in naturally acidic streams. (submitted manuscript)
IV
Petrin, Z., McKie, B. G., Buffam, I., Laudon, H. and Malmqvist, B. 2007. Landscape-controlled chemistry variation affects communities and ecosystem function in headwater streams. Canadian Journal of Fisheries and Aquatic Sciences 64. (in press)
V
McKie, B. G., Petrin, Z. and Malmqvist, B. 2006. Mitigation or disturbance? Effects of liming on macroinvertebrate assemblage structure and leaf-litter decomposition in the humic streams of northern Sweden. Journal of Applied Ecology 43(4): 780 – 791.
Papers I, IV, and V are reproduced with kind permission from the publishers.
1
Introduction
INTRODUCTION The industrious activities of the human population have caused the release of large quantities of acidifying substances followed by the acidification of numerous freshwater systems on continental scales. Such anthropogenic acidity is generally detrimental for both species diversity and ecological functioning (Schindler 1988; Rosemond et al. 1992; Driscoll et al. 2001). In addition, many naturally acidic freshwater systems have been found (Collier et al. 1990; Renberg et al. 1993a; Laudon & Bishop 1999). And in some regions, including northern Sweden, acidic freshwater systems have prevailed for several thousand years (Renberg et al. 1993a; Korsman 1999). In such regions, where abundant naturally acidic freshwater systems have existed over evolutionary periods, an adapted and specialized fauna may have evolved (Collier et al. 1990; Dangles et al. 2004). Therefore, habitats that have both been historically persistent and abundant may today support a larger pool of suitable species than would be expected for habitats characterised by putatively adverse environmental conditions. Consequently, species diversity ought not to be expected to be automatically impaired at acidic sites when compared to circumneutral sites in regions where acidity has been natural (cf. evolutionary species pool hypothesis, Taylor et al. 1990; Pither & Aarssen 2005). Little is known about what characteristics enable freshwater organisms to thrive at naturally low pH and how that ability translates into species diversity and ecological functioning patterns, although the need to study the adaptability of freshwater biota to low pH was recognized early (Jewell 1922). Species diversity and ecological functioning in naturally acidic freshwater systems have been studied in both Sweden and New Zealand (Collier et al. 1990; Dangles et al. 2004; Collier et al. 2006). Generally, these studies suggest that the species richness levels and the rates of decomposition of leaf litter are comparable between naturally acidic and circumneutral sites, and that relatively high species richness is maintained even at pH levels around 4.0 – 4.5. In New Zealand, no anthropogenically acidified sites were included in the studies for comparison (Collier et al. 1990; Collier et al. 2006). Furthermore, whereas microbial decomposition remained unaffected by low pH, decomposition mediated by leaf feeding insects appeared to be lowest at acidic sites (Collier et al. 2006). Thus, the evidence for unimpaired ecological functioning in naturally acidic streams appears to be equivocal. In Sweden, the evidence for similar species richness and leaf decomposition rates between naturally acidic and circumneutral streams was scarce and limited to a small number of streams in a small area in the province of Västerbotten (Dangles et al. 2004). The Swedish data was compared to data from a small set of reference streams in a small anthropogenically acidified region in France. Therefore, the comparison may have been confounded by different biogeographical histories. Or idiosyncratic ecological responses in the two regions, which are possibly not representative, may have explained the observed patterns. Thus, it was still unclear whether the 2
Species diversity and functioning in naturally acidic streams observed species richness and ecological functioning patterns were at all relevant for Sweden and if they could be scaled up geographically. In contrast to New Zealand, no refuges remained during the Pleistocene ice ages in Scandinavia. Consequently, evolutionary changes have taken place during a comparatively short period in Sweden. In addition, the low number of replicates due to logistical constraints and the large among-stream variation in many studies may have resulted in low statistical power (cf. Arnqvist & Wooster 1995). Therefore, the lack of a pH effect in naturally acidic systems could reflect the shortcomings of study designs rather than genuine ecological patterns. Last, ecological functioning may not be generally impaired even where acidity is anthropogenic: tolerant, functionally redundant organisms may increase in biomass where sensitive biota have become excluded from acidic environments and thereby compensate for the loss in functioning (Walker 1992; Johnson et al. 1996; Niyogi et al. 2002). Thus, it was still controversial whether anthropogenic acidity generally affects ecological functioning in freshwater systems and whether naturally acidic freshwater systems differ in their functionality from anthropogenically acidified environments. Hence, more work was needed to assess the generality of previous findings. Our understanding of how natural variation in acidic water chemistry affects community structure and ecological functioning was also limited. For instance, dissolved organic carbon (DOC), a major cause of acidity in naturally acidic streams (e.g. Hemond 1994; Laudon & Bishop 2002a), appears to have both ameliorating and toxic effects depending on its specific levels and on additional water chemistry variables (Kullberg et al. 1993; Thomas 1997; Steinberg et al. 2006). Furthermore, inorganic aluminium appears to be widely toxic to freshwater biota, but its specific ecological effects depend on both the pH and DOC levels (Hall et al. 1985; Burton & Allan 1986; Herrmann 2001). Even in the absence of direct fitness effects on freshwater organisms of, for instance, DOC (Qualls & Haines 1990), interactions among different water chemistry variables may facilitate nutrient uptake or complex bind toxic metals, including inorganic aluminium (McCahon & Pascoe 1989; Thomas 1997; Dobranskyte et al. 2006). In contrast, in naturally acidic streams in New Zealand acidity, whether caused by humic or mineral acids, did not appear to notably control how macroinvertebrates were distributed across streams (Winterbourn & McDiffett 1996). However, the generality of this result and its implications and significance for freshwater biota in naturally acidic streams elsewhere, including northern Sweden, remained to be investigated. Liming acidic freshwater systems started at the end of the 1970s in Sweden. In the beginning of the 1990s an elaborate liming programme was implemented to mitigate the negative effects of acidification on freshwater biota (Ahlström et al. 1995). That liming programme was soon extended to include acidic streams in northern Sweden. The main purpose was to amend water quality in order to conserve freshwater diversity and improve recreational fisheries. However, only minor anthropogenic contributions to acidity had been reported for northern 3
Methods Sweden, suggesting that acidity had been largely natural there (Laudon & Bishop 2002b; Laudon et al. 2004c). Consequently, freshwater organisms may have become adapted and perhaps specialized to living under conditions that were presumed to be harmful (Dangles et al. 2004). Therefore, liming may in fact disturb the ecosystem rather than alleviate the negative effects of low pH. But, the effects of liming naturally acidic streams on ecosystem structure and ecological functioning had not been studied yet, and it was still unclear whether liming had aided in achieving the management goals.
Objectives In order to address the above limitations and fill in some important gaps in our understanding of how natural acidity affects species diversity and ecological functioning, as well as to study some of the mechanisms underlying species distributions and functioning in naturally acidic freshwater systems, I tried to answer the following questions: Are macroinvertebrate species richness and leaf decomposition rates reduced by anthropogenic acidity, but remain unaffected by natural acidity in Sweden, in particular, and globally across different regions? How does variation in naturally acidic water chemistry, especially in pH and DOC levels, affect species richness and the rates of decomposition of leaf litter? What are the effects of liming naturally acidic streams on species diversity and leaf decomposition rates?
METHODS Stream hydrology, hydrochemistry, and freshwater biota have been intensively studied in Scandinavia. Therefore, comprehensive data are available particularly on macroinvertebrate distributions with respect to pH in Swedish streams (Ahlström et al. 1995). Stream macroinvertebrates are generally diverse, and their distributions are often closely associated with various gradients in water chemistry, especially the gradient in acidity (Herrmann et al. 1993). Thus, stream macroinvertebrate communities are suitable for monitoring the status of streams and studying how catchment level processes, including acidification, affect species diversity and ecological functioning (Resh & McElravy 1993).
Study regions Natural acidity is widespread in northern Sweden (Korsman 1999; Laudon & Bishop 1999; Bishop et al. 2000), and probably across the boreal region in general. In northern Sweden natural acidity stems mainly from the lack of buffering bases in the bedrock, exacerbated by dilution by rain and snow-melt water, and the high content of humic acids in stream water (Laudon & Bishop 1999; Bishop et al. 2000; Laudon & Bishop 2002b). But anthropogenic acidification is relatively unimportant in northern Sweden (Laudon & Bishop 4
Species diversity and functioning in naturally acidic streams 2002b; Laudon et al. 2004c). In contrast, in southern Sweden anthropogenic acidification is widespread (Warfvinge & Bertills 1999). However, acidic water chemistry in the south has also been affected by moderate natural background acidity, calcareous bedrock, eutrophication, and historical increases in alkalinity due to land use change (Renberg & Hellberg 1982; Renberg et al. 1993a; Renberg et al. 1993b). Nevertheless, only limited time for marked evolutionary modifications in response to acidification has been available in the south compared to the north of Sweden.
Study sites The Swedish study sites constituted headwater to third order forest streams. The sites were selected to represent naturally acidic, anthropogenically acidified, and circumneutral water chemistry both in Sweden and globally (I, II, III), different types of water chemistry regime within the natural acidity category (IV), and the impact of liming (V). The Swedish study sites typically comprised 50 m long riffle reaches with a cobble and stone bed. The riparian broad-leaf vegetation mainly consisted of grey alder, Alnus incana (L.) Moench, black alder, Alnus glutinosa (L.) Gaertner, and birch, Betula spp. that also contributed the predominant leaf litter found in the streams.
Water chemistry At each site various water chemistry variables were measured including pH. The DOC content was determined by measuring absorbance at 254 nm (Laudon et al. 2004a, II, V), or by combustion and analysis as CO2 after acidification and sparging of filtered, 0.45 µm, water samples (Buffam et al. 2007, IV). Alkalinity was measured by Gran titration (Gran 1952, II, V). Inorganic aluminium (Ali) concentrations were determined as the difference between total and organic aluminium after fractionation using a cation exchange column (Cory et al. 2006, IV). Part of the water chemistry data were compiled by governmental authorities and by the Environmental Assessment department of the Swedish University of Agricultural Sciences, Uppsala, including time series data that in some cases exceeded a decade (I, II).
Species diversity Benthic samples were collected using a Surber net (GB Nets, Cornwall, UK, mesh 250 µm and 500 µm, sample area 0.1 m2; II, IV, V). All samples were preserved in 70 % ethanol until further processing in the laboratory. The samples were then sorted, and the macroinvertebrates identified to the lowest possible taxonomic level, usually species, but genus for a few caddisfly and beetle taxa and most Diptera. Ceratopogonidae, Chironomidae, and Simuliidae were identified to the family level. Worms were classified as Oligochaeta and Nemathelminthes, and mites as Acari. Macroinvertebrate abundances, observed taxonomic richness, and species density, the number of taxa identified per unit area, were recorded. Whenever feasible, sample-based rarefied taxonomic 5
Methods richness was computed to account for differences in abundances among sites because more species are recorded by chance alone when more individuals are collected (Gotelli & Colwell 2001). Species abundance data was based on standardized kick samples when the data was compiled by governmental authorities or the Environmental Assessment department, SLU, Uppsala. Then individual-based rather than sample-based rarefied taxonomic richness was computed as no replicate benthic samples were available (I).
Ecological functioning In small forest streams, especially in headwater streams, the decomposition of leaf litter constitutes an important ecological process channeling allochthonous energy to the ecosystem (Gessner & Chauvet 2002). The decomposition of leaf litter was modeled by measuring leaf mass loss (II, IV, V). Leaves of grey and black alder were picked prior to abscission directly from the trees, air-dried at room temperature, and enclosed in coarse and fine mesh bags, 10 mm and 0.5 mm, respectively. One pair of fine/coarse mesh bags was attached to each of several replicate metal stakes hammered into the stream bed. Macroinvertebrates were able to freely enter and feed on the material in coarse mesh bags, but were excluded from fine mesh bags. After exposure the mesh bags were retrieved, separately enclosed in zip-lock bags, and stored at -20 ºC until further processing in the laboratory. The material was sorted and remaining leaf material separated from other detritus and mineral particles. The leaf material was then dried, weighed, and combusted to provide ash free dry mass results. An exponential decay model was employed to calculate the leaf litter decomposition rate. Leaching and handling losses were accounted for (Benfield 1996). Temperature varied among streams and therefore decomposition data was standardized for temperature using metabolic theory (Brown et al. 2004). Mass loss in fine mesh bags is mainly caused by microbial activity, primarily that of hyphomycete fungi. The mass loss in coarse mesh bags, however, is caused by both microbial decomposition and the feeding activities of leaf-eating insects, that is shredding (Gessner & Chauvet 2002). Shredding was therefore estimated by calculating the difference between the mass loss measured in coarse mesh bags and that measured in the corresponding fine mesh bags. Mass loss, particularly in coarse mesh bags, is also caused by hydrological wear. But such physical abrasion is of little importance in headwater streams, probably due to limited shear stress; and no hydrologically extreme events were observed in the larger streams.
Data analyses The data was analysed using various statistical tools. Fixed and mixed analysis of variance and covariance, and generalized linear models were employed to study the effects of water chemistry variables, study region, and treatments on species richness, species density, macroinvertebrate abundance, and the rates of decomposition of leaf material (I, II, IV, V). Analysis of similarities was used to 6
Species diversity and functioning in naturally acidic streams assess the effects of water chemistry and treatments on species composition (Clarke 1993, II, IV, V). Similarity percentages were calculated to determine which species contributed most to dissimilarities between groups of sampling units (Clarke 1993, II, IV, V). Non-metric multidimensional scaling was employed to group sites by their taxonomic composition (Clarke 1993, II, IV, V), and canonical correspondence analysis was used to assess the importance of pH for controlling macroinvertebrate assemblages in regions with anthropogenic and natural acidity (Woodward et al. 2002, I). Finally, a meta-analysis was used to integrate data from different studies across geographical scales (Arnqvist & Wooster 1995, III).
RESULTS AND DISCUSSION Acidity and related water chemistry variables, including the DOC content and alkalinity, generally restrict the distribution of freshwater biota (Herrmann et al. 1993; Courtney & Clements 1998; Vinson & Hawkins 1998). Low pH has been proposed to affect macroinvertebrate community structure and ecological functioning for instance through physiological and ecological mechanisms, including altered quality of food resources (Hall et al. 1980; Herrmann et al. 1993; Ledger & Hildrew 2005). Whatever the mechanisms, in the absence of phylogenetic constraints time and continuing selection are likely to improve the organisms’ tolerance of high acidity levels through adaptation. Consequently, in regions where acidic systems have prevailed over evolutionary time scales, the distribution of macroinvertebrates is expected to encompass putatively hostile habitats characterized by high levels of acidity (cf. evolutionary species pool hypothesis, Taylor et al. 1990; Pither & Aarssen 2005). I found evidence for such distributional differences between recently anthropogenically acidified and longterm naturally acidic systems, but also evidence for limitations to the differences in freshwater macroinvertebrate distributions (I, II, III).
Effects of anthropogenic versus natural acidity The results were in general agreement with the adaptation and evolutionary species pool hypothesis: species richness tended to be more strongly affected in regions where acidity was human-caused than in regions with long-term natural acidity (Collier et al. 1990; Dangles et al. 2004; Pither & Aarssen 2005, I, II, III). Although the interpretation of the results from single studies in some instances might seem equivocal, the different lines of evidence taken together were evocative. Those lines of evidence included at least a tendency of or clearly higher losses in richness where acidity was anthropogenic rather than natural (Dangles et al. 2004, I, II, III). The caddisfly richness versus pH relationships in northern and southern Sweden were strongly diverging: richness increased along the pH-gradient in the south, but tended to decrease in the north (I). The species abundance distributions were in agreement with the hypothesis of tolerance and adaptation to low pH in more than 50 % of the tested taxa, which also included the allegedly more sensitive mayflies and bivalves (I). The species composition 7
Results and discussion differed between acidic and circumneutral streams (I, II). The mayfly and caddisfly assemblages were more strongly associated with anthropogenic than natural acidity (I), and the differences in macroinvertebrate assemblages between naturally acidic and circumneutral streams in northern Sweden were largely driven by the sensitive mayflies, whereas all taxa contributed to a similar extent in the south (II). Last, the regional differences in the macroinvertebrate richness patterns were not restricted to single regions with idiosyncratic species pools or biogeographical colonization histories, but applied generally as was revealed by the meta-analysis (III). Contrary to the expectations, the rates of decomposition of leaf litter were not affected more at acidic sites in the south than in the north of Sweden when compared to circumneutral sites in the same region (II). Thus, there was no evidence for differential patterns for this function along the pH-gradients between the two regions. In addition, shredder assemblages, the faunal elements responsible for the breakdown of a large proportion of leaf material, differed regionally, but not between pH levels (II). Furthermore, when studied across multiple regions, the patterns of the loss in function along the pH-gradients also did not differ between regions with anthropogenic and natural acidity (III). Thus, adaptive features in macroinvertebrates did not translate into differences in ecological functioning, and no differences were found between regions with anthropogenic and natural acidity in how ecological functioning changed with pH. Instead, the results on the patterns of leaf litter decomposition rates along the pH-gradients appeared to be consistent with the functional redundancy hypothesis: the biomass of tolerant freshwater biota likely increased, and tolerant organisms thus compensated for the loss in function otherwise mediated by the more sensitive biota (Odum 1985; Schindler 1987; Niyogi et al. 2002). Generally, where redundancy is high, ecological functioning will likely not be markedly affected unless species diversity is strongly reduced (Walker 1992; Johnson et al. 1996). Because there may be regional differences in what causes acidity the interpretation of the data has a certain limitation. Mineral acids are likely to prevail where acidity is anthropogenic, while organic acids often prevail where acidity is natural (Hemond 1994; Laudon & Bishop 2002a). However, such differences in the quality of acidity did not appear to affect species assemblages and species richness patterns in a region with both anthropogenic and natural acidity in New Zealand (Winterbourn & McDiffett 1996). But the generality of that result and its applicability beyond New Zealand remain to be tested. Indeed, varying naturally acidic water chemistry appeared to affect species diversity and ecological functioning in northern Sweden (IV). But that study did not include anthropogenically acidified streams and therefore does not automatically suggest that systematic differences in acidic water chemistry between regions with anthropogenic and natural acidity cause different patterns of species diversity and ecological functioning. If, on the other hand, the chemical causes of acidity are eventually found to be of marginal importance for how freshwater biota are 8
Species diversity and functioning in naturally acidic streams distributed with respect to naturally low pH (Winterbourn & McDiffett 1996), then adaptations to acidic conditions are likely to account for the relatively higher species diversity in naturally acidic than anthropogenically acidified streams when compared to circumneutral systems (cf. Taylor et al. 1990; Pither & Aarssen 2005, III). The adaptations may have developed over evolutionary time periods in situ or in neighbouring regions followed by immigration. Yet, the exact process remains irrelevant for the validity of the hypothesis. In contrast, the absence of differences in the patterns of ecological functioning along the pHgradients in regions with anthropogenic and natural acidity is parsimoniously explained by compensatory, ecological processes, and therefore no evolutionary explanations need to be invoked.
Effects of varying naturally acidic water chemistry To investigate the ecological effects of variation in naturally acidic water chemistry, I studied macroinvertebrate community structure and ecological functioning in streams exhibiting two different types of naturally acidic water chemistry regimes, the forest and the mire regimes. Forest regime sites were largely groundwater-influenced, and the stream water was thus relatively clear during baseflow, but rich in DOC during hydrological episodes (Bishop et al. 2004; Laudon et al. 2004a; Laudon et al. 2004b; Buffam et al. 2007, IV). Mire regime sites on the other hand were characterised by DOC-rich water from wetlands during baseflow, whereas the stream water became relatively diluted during episodes (Laudon et al. 2004a; Buffam et al. 2007, IV). Leaf decomposition was higher at mire regime sites reflecting elevated shredding due to a higher abundance of shredders at these sites and, to a lesser extent, increased microbial activity (IV). Apart from differing abundances, particularly of stoneflies and caddisflies, the shredder assemblages exhibited few compositional differences. In contrast to functioning, macroinvertebrate richness was higher at forest regime sites (IV). Moreover, benthic macroinvertebrate assemblages showed clear compositional differences between the regimes. Despite distinct patterns regarding the two water chemistry regimes, richness and ecological functioning did not clearly correlate with the corresponding water chemistry variables, that is, when the ecological variables were directly related to pH, the DOC content, and the concentration of Ali (IV). Nevertheless, the growth and survival of two stonefly species suggested some degree of acclimation and adaptation to the different water chemistry regimes (IV). The lower richness at mire regime sites likely reflected the fact that mire regimes sites tended to maintain lower pH levels for a longer period of time. That corresponds to previous research suggesting that high acidity often reduces species richness, both where acidity is anthropogenic and where it is natural, albeit to different degrees (Otto & Svensson 1983; Rosemond et al. 1992; Guérold et al. 2000, I, II, III). The results on ecological functioning, however, contrasted with many previous findings suggesting reduced species richness at mire regime sites was compensated for, if not overcompensated for, by higher 9
Results and discussion shredder abundances that rescued functioning (cf. functional redundancy hypothesis, Odum 1985; Schindler 1987; Niyogi et al. 2002). This mechanistic interpretation is in agreement with other studies reporting that ecological functioning did not vary with pH in northern Sweden and in regions with natural acidity in general (Dangles et al. 2004, II, III). Hydrochemical variation is particularly large in headwater streams and often clearly exceeds the variation encountered in larger lotic freshwater systems (Temnerud & Bishop 2005; Cory et al. 2006; Buffam et al. 2007). Distinct benthic macroinvertebrate communities causing different species diversity and ecological functioning patterns reflect this variation in stream water chemistry (IV). Thus, naturally acidic streams should not be considered all the same ecologically. Instead, they likely support an evolutionarily and ecologically largely unexplored pool of freshwater biota that are characterized by varying degrees of tolerance and adaptation to acidity, high DOC levels, and possibly other supposedly less favourable chemical and hydrological conditions.
Effects of liming naturally acidic streams Liming acidic freshwater systems by adding CaCO3 has been used with varying success to improve water quality and thus facilitate the recovery of freshwater biota (Bradley & Ormerod 2002). However, liming may also constitute a disturbance and may then cause undesired effects (Weatherley 1988; Ormerod et al. 1990) which is arguably more likely if the limed streams are naturally acidic and harbour a tolerant and adapted fauna. In naturally acidic streams in northern Sweden microbial decomposition was enhanced by liming, whereas shredding was reduced (V). The effect was stronger during the spring than autumn. Liming also affected shredder assemblages in the spring: while the abundance of large caddisflies decreased as a result of liming, that of the smaller stoneflies increased, and overall shredder diversity declined (V). The evenness decreased, and species richness tended to decrease following liming in spring, too. Moreover, liming also affected benthic assemblages in the spring. However, abundance, richness, density, and evenness of benthic macroinvertebrates were not affected (V). The results suggest some of the components of the stream community including microbial decomposers and shredding stoneflies tended to benefit from liming, whereas other components such as shredding caddisflies decreased in biomass, reflected in impaired shredding. Varying effects on the different components have been implied and reported previously following liming (Ormerod et al. 1990; Bradley & Ormerod 2002). However, the results agreed with previous findings in that shredding and species assemblages in naturally acidic streams in northern Sweden appeared to change with changes in acidity-related water chemistry variables including pH (Dangles et al. 2004, I, II, IV). The observed changes in the faunal composition and the increased microbial decomposition rates following liming are nevertheless also suggestive of perturbation and may indicate that a potentially undesired ecosystem has been created that did not 10
Species diversity and functioning in naturally acidic streams correspond to either untreated acidic or circumneutral stream ecosystems (Weatherley 1988; Ormerod et al. 1990). Thus, liming may not have contributed to conserving biodiversity in naturally acidic streams in northern Sweden.
SUMMARY AND CONCLUSIONS Contrary to what has been found for anthropogenically acidified streams, species richness in naturally acidic streams was not reduced to the same extent when compared to circumneutral streams, likely reflecting tolerance and adaptation to high acidity levels, or varying responses to differences in acid quality (Collier et al. 1990; Dangles et al. 2004, I, II, III). Thus, time since the onset of acidification possibly contributed to differences in macroinvertebrate distributions between naturally acidic and anthropogenically acidified freshwater systems providing comparative support for the evolutionary species pool hypothesis (Taylor et al. 1990; Pither & Aarssen 2005, I, II, III). Alternatively, differences in the quality of acidity between streams that have been anthropogenically acidified or are naturally acidic may account for differing patterns in species richness (Collier et al. 1990; Dangles et al. 2004, I, II, III), though the extent of the sensitivity of freshwater biota to varying acidic water chemistry requires further investigation (Winterbourn & McDiffett 1996). However, tolerance and adaptation did not translate into differing patterns of ecological functioning: the reduction in ecological functioning under acidic conditions did not appear to differ between anthropogenically acidified and naturally acidic streams, probably due to compensatory processes (Niyogi et al. 2002; Dangles et al. 2004, II, III). Despite the generally consistent results, variation in chemistry of waters that are naturally acidic, particularly in headwater streams, was large. The hydrochemical variation was reflected in the largely unexplored varying species diversity and ecological functioning patterns implying a large diversity of adaptive features in headwater stream organisms (Temnerud & Bishop 2005; Cory et al. 2006; Buffam et al. 2007, IV). Finally, that variation in the diversity and functioning of freshwater communities along with the likely tolerant and adapted faunal components may have compromised efforts to preserve biota in naturally acidic systems by liming (Ormerod et al. 1990; Bradley & Ormerod 2002, V).
FUTURE DIRECTIONS The conclusions in this thesis are largely based on observational studies that are a necessary first step in addressing questions concerning the ecology of naturally acidic freshwater systems. However, observational studies are also correlative. They, therefore, do not allow drawing unambiguous conclusions regarding the mechanisms that brought about the observed relationships. In order to explain whether the different effects of anthropogenic and natural acidity on species diversity patterns derive from adaptation or differences in the quality of acidity, future studies should aim at distinguishing between these two remaining hypotheses using an experimental approach along with comparative studies. 11
Acknowledgements Studying streams in geographically adjacent regions, but where acidity is chemically similar yet has different causes, anthropogenic and natural, would help disentangling the effects of acid quality from those of adaptation. In addition, common garden experiments will be a necessary further step to reveal whether freshwater organisms are adapted to high levels of acidity because the adaptation concept usually relates to the species and population levels rather than to whole communities. If so, the presence of adapted organisms in regions with natural acidity may result from two different processes, the evolution of adaptive features in situ over many generations, and immigration of already adapted biota from neighbouring regions. These two processes will likely be reflected in different levels of endemism and nestedness implying various degrees of adaptability of freshwater biota to low pH in general. Due to the implied differences in endemism, information on the mechanisms is likely to aid environmental managers in deciding what kind of measures, including rigorous protection and reintroduction, constitute appropriate ways of conserving the diversity and functionality of naturally acidic freshwater environments for the future.
ACKNOWLEDGEMENTS I thank Grete Algesten, Ines Anderl, Johan Baudou, Peder Blomkvist, Ishi Buffam, Lars Brydsten, Anna Cord, Göran Englund, Per-Ola Hoffsten, Thomas Hörnlund, Mats Jansson, Cecilia Karlsson, Hjalmar Laudon, Fabio Lepori, Björn Malmqvist, Brendan McKie, Hans-Göran Nilsson, Per Nilsson, Christian Otto, Dirk Prüss, Viktor Sjöblom, Darius Strasevicius, Kristina Ulvcrona, and Martin Wiss, who contributed to various aspects of the studies presented in this thesis or the thesis itself including general advice, data handling, constructive criticism of the manuscripts, help with the work in the field and laboratory, advice regarding species indentifications, logistical support, permission to use laboratory facilities, and help with the water chemistry analyses. The environmental management authorities pointed out suitable study sites and provided detailed water chemistry data. The research presented in this thesis was supported by The Swedish Research Council FORMAS (to BM and HL), the Knut and Alice Wallenberg Foundation, the Swedish Environmental Protection Agency (to HL), the J C Kempe Memorial Foundation Scholarship Fund, the Göran Gustafsson Foundation for Nature and Environment in Lappland, and the Oscar and Lili Lamms Memorial Foundation (to ZP).
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Species diversity and functioning in naturally acidic streams
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Thank you!
THANK YOUUUUUUUUUU! First and foremost I want to thank my supervisor Björn who gave me the opportunity to work on such an exciting topic. I am grateful to the members of the Stream Ecology Group, the former PhD students Per-Ola, Darius, and Micael, for gladly sharing their time, and the post docs Brendan, for cooperation, and Fabio for discussions. It has been an honour working with my other cooperating colleagues and co-authors, Ishi and Hjalmar, whose different perspective, the hydrologists’ and hydrochemists’ view, and coordination and time management have been an inspiration for my own work. I am indebted to the former and present members of my advisory committee, Christian, Göran (another coauthor), Mats, and Martin. They followed my development as a PhD student, showed real interest in the troubles I had faced, and offered constructive advice in various matters. And I want to thank Kikki and my examinator Lennart for helping overcome administrative obstacles. I particularly enjoyed being actively involved in the R study group together with Arne, Johan, Lena, and Ullis. It was a pleasure discussing the Aikaiki Information Criterion, the Kolmogorov-Smirnov Test, heteroscedasticity, the Poisson distribution … with you! I always wanted to write a couple of those tongue twisters in some publication. Finally, I shall succeed. During my time as a PhD student I was involved in a variety of teaching obligations. The timing was not always optimal, for instance when I had to do teaching during the field season. But all coordination problems had eventually been solved. Representatively for many Swedes I thank Tommy for teaching me the importance of taking it easy! Parts of the freshwater ecology course were among those I enjoyed teaching most. And I want to thank Johan for the confidence he has placed in me, when he entrusted me with teaching substantial parts of the statistics course, another obligation I gladly assumed. Many more people contributed to my stay here being worthy of remembrance. Annika, the green-fingered, has been happy to share her quality time, her knowledge about plants and other things, and her high spirits. She and Anna strived with me for touching the skies. Örjan good-naturedly used life-saving surgery to rescue the firebug several times. Arne has shared some of my sorrows and many funny moments during work and in private. Estherházy vigorously advertised the Swabian lifestyle. Dirk has proven an optimistic and true philosopher, a master of the art of living, and great fishing companion despite meagre success. Anna (another one) has simply proven a loving down-to-earth friend. Lena has never refused having a nice chat. Emma has patiently shared the office with me. Martin, you know who, has made my life as PhD student a colourful experience. Alex has been a loyal friend since primary school. Thank you friends, thank you folks, and thanks to all the people who I have not named! I thank Theresia and Hans for welcoming me in their family and Susanne for being my sister. I am most grateful to my parents, who have believed in me, even 18
Species diversity and functioning in naturally acidic streams though they may sometimes not have understood my career decisions, and who have loved me and who always wanted only one thing for me, to be happy. I am most grateful to them for encouraging me to do what I really wanted to do and for giving me that freedom by consistently supporting me in various ways. Thank you! Last, I thank Ines, who has shared many years of her life with me. No description meets the time we have spent together. So I simply say: Thank you Ines! Thank you for believing in me, thank you for supporting me, for being my friend, and my longtime companion.
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