Brendan G. McKie

Diversity meets decomposition

Over 100 gigatons of terrestrial plant biomass are produced globally each year. Ninety percent of this biomass escapes herbivory and enters the dead organic matter pool, thus supporting complex detritus-based food webs that determine the critical balance between carbon mineralization and sequestration. How will changes in biodiversity affect this vital component of ecosystem functioning? Based on our analysis of concepts and experiments of leaf decomposition in forest floors and streams, we suggest that changes in species diversity within and across trophic levels can significantly alter decomposition. This happens through various mechanisms that are broadly similar in forest floors and streams. Differences in diversity effects between these systems relate to divergent habitat conditions and evolutionary trajectories of aquatic and terrestrial decomposers.

Continental-scale effects of nutrient pollution on stream ecosystem functioning.

Reading the Leaves Excess inputs of nutrients—a type of pollution known as eutrophication—threatens biodiversity and water quality in rivers and streams. Woodward et al. (p. 1438; see the Perspective by Palmer and Febria) studied how one key ecosystem process—leaf-litter decomposition—responds to eutrophication across a large nutrient pollution gradient in 100 European streams. Leaf breakdown was stimulated by low to moderate nutrient concentrations but was inhibited at high rates of nutrient loading. Leaf-litter breakdown rates across 100 European streams offer insights into ecosystem health during eutrophication. Excessive nutrient loading is a major threat to aquatic ecosystems worldwide that leads to profound changes in aquatic biodiversity and biogeochemical processes. Systematic quantitative assessment of functional ecosystem measures for river networks is, however, lacking, especially at continental scales. Here, we narrow this gap by means of a pan-European field experiment on a fundamental ecosystem process—leaf-litter breakdown—in 100 streams across a greater than 1000-fold nutrient gradient. Dramatically slowed breakdown at both extremes of the gradient indicated strong nutrient limitation in unaffected systems, potential for strong stimulation in moderately altered systems, and inhibition in highly polluted streams. This large-scale response pattern emphasizes the need to complement established structural approaches (such as water chemistry, hydrogeomorphology, and biological diversity metrics) with functional measures (such as litter-breakdown rate, whole-system metabolism, and nutrient spiraling) for assessing ecosystem health.

Ecosystem functioning in stream assemblages from different regions: contrasting responses to variation in detritivore richness, evenness and density

1. The diversity of species traits in a biological assemblage varies not only with species richness, but also with species evenness and organism density, which together influence the concentration of traits within functional guilds. Potential trait diversity at local scales is also constrained by the regional species pool. Implications of such variation for spatio-temporal variability in biodiversity-ecosystem functioning relationships are likely to be complex, but are poorly understood. 2. In microcosm experiments conducted at laboratories in Sweden, Ireland and Romania, we investigated effects of species richness, evenness and density of stream-living detritivores on two related processes: detritivore leaf-processing efficiency (LPE) and growth. Assemblage composition varied among laboratories: one taxonomic order (Plecoptera) was studied in Sweden, whereas two orders, encompassing wider trait variation, were studied in Romania (Trichoptera and Plecoptera) and Ireland (Trichoptera and Isopoda). 3. Relationships between density and both LPE and growth ranged from negative to positive across the study species, highlighting the potential for density-dependent variation in process rates to alter ecosystem functioning, but indicating that such effects depend on species identity. 4. LPE varied with species diversity in the two more heterogeneous assemblages, but whereas LPE in the Romanian study was generally enhanced as richness increased, LPE in the Irish study increased only in less-even polycultures dominated by particular species. Transgressive overyielding was detected in the Irish experiment, indicating complementary resource use and/or facilitation (complementarity). These mechanisms could not be distinguished from the selection effect in the Romanian study. 5. Growth was elevated in Romanian species mixtures, reflecting positive complementarity, but lower than expected growth in some Swedish mixtures was associated with negative complementarity, indicating interspecific interference competition. 6. Our results emphasize the potential importance of detritivore diversity for stream ecosystem functioning, but both the effects of diversity on the studied processes, and the mechanisms underlying those effects, were specific to each assemblage and process. Such variability highlights challenges in generalizing impacts of diversity change for functional integrity in streams and other ecosystems in which the occurrence of important species traits fluctuates over relatively small spatio-temporal scales.

Stream Ecosystem Functioning in an Agricultural Landscape: The Importance of Terrestrial-Aquatic Linkages

The loss of native riparian vegetation and its replacement with non-native species or grazing land for agriculture is a worldwide phenomenon, but one that is prevalent in Europe, reflecting the heavily-modified nature of the continents landscape. The consequences of these riparian alterations for freshwater ecosystems remain largely unknown, largely because bioassessment has traditionally focused on the impacts of organic pollution on community structure. We addressed the need for a broader perspective, which encompasses changes at the catchment scale, by comparing ecosystem processes in woodland reference sites with those with altered riparian zones. We assessed a range of riparian modifications, including clearance for pasture and replacement of woodland with a range of low diversity plantations, in 100 streams to obtain a continental-scale perspective of the major types of alterations across Europe. Subsequently, we focused on pasture streams, as an especially prevalent widespread riparian alteration, by characterising their structural (e.g. invertebrate and fish communities) and functional (e.g. litter decomposition, algal production, herbivory) attributes in a country (Ireland) dominated by this type of landscape modification, via field and laboratory experiments. We found that microbes became increasingly important as agents of decomposition relative to macrofauna (invertebrates) in impacted sites in general and in pasture streams in particular. Resource quality of grass litter (e.g., carbon : nutrient ratios, lignin and cellulose content) was a key driver of decomposition rates in pasture streams. These systems also relied more heavily on autochthonous algal production than was the case in woodland streams, which were more detrital based. These findings suggest that these pasture streams might be fundamentally different from their native, ancestral woodland state, with a shift towards greater reliance on autochthonous-based processes. This could have a destabilizing effect on the dynamics of the food web relative to the slower, detrital-based pathways that dominate in woodland streams.

Chapter 5 – Environmental Warming and Biodiversity–Ecosystem Functioning in Freshwater Microcosms

Predicting the effects of global warming on biodiversity–ecosystem functioning (B–EF) relationships is complicated by potential interactions among abiotic and biotic variables at multiple levels of organisation, including adaptation within regional species populations and changes in community composition and species richness. We investigated the capacity for assemblages of three freshwater invertebrate consumer species (Asellus aquaticus, Nemoura cinerea and Sericostoma personatum) from temperate (southern England) and boreal (northern Sweden) regions to respond to expected shifts in temperature and basal resources, and quantified rates of a key ecosystem process (leaf-litter decomposition). Predictions of assemblage metabolism, derived from allometric-body size and temperature scaling relationships, accounted for approximately 40% of the variance in decomposition rates. Assemblage species composition accounted for further variance, but species richness per se had no discernible effect. Regional differences were evident in rates of leaf decomposition across temperature and resource manipulations, and in terms of the processing efficiency of temperate and boreal consumers of the same species (i.e. after correcting for body size and metabolic capacity), suggesting that intraspecific variation among local populations could modulate B–EF effects. These differences have implications for extrapolating how environmental warming and other aspects of climate change (e.g. species range shifts) might affect important drivers of ecosystem functioning over large biogeographical scales

The importance of litter traits and decomposers for litter decomposition: a comparison of aquatic and terrestrial ecosystems within and across biomes

Summary Plant leaf litter comprises the major common source of energy and nutrients in forested soil and freshwater ecosystems world-wide. However, despite the similarity of physical and biochemical processes, generalizations across aquatic and terrestrial ecosystems regarding litter decomposition drivers remain elusive. We re-analysed data from a published field decomposition experiment conducted in two ecosystems (forest floors and streams) across five biomes (from the tropics to subarctic) with increasing decomposer community complexity (microbes, microbes and mesofauna, microbes and meso- and macrofauna). Using a wide litter quality gradient (15 litter combinations), we aimed to disentangle the roles of decomposer community complexity from that of leaf litter traits (18 traits encompassing four broad trait categories: nutrients, C quality, physical structure and stoichiometry) on litter C and N loss. Comparisons of decomposition drivers between ecosystems were evaluated across and within biomes. Differences in environmental conditions (e.g. climate, soil/water fertility) and litter nutrients – with a particular focus on Mg and Ca – across biomes were the major drivers of litter C loss in both ecosystems, but decomposer complexity also played a prominent role in streams. Within biomes, we observed consistent effects of litter nutrients and stoichiometry on litter C and N loss between ecosystems, but the effects of decomposer complexity differed between streams and forest floors in the temperate, Mediterranean and tropical biomes. Our results highlight that, beyond the litter traits commonly identified as controlling decomposition (e.g. C, N and lignin), micronutrients (e.g. Mg and Ca) can also play an important, and globally consistent, role in both aquatic and terrestrial ecosystems. In addition, in forest streams the complexity of decomposer communities had similar importance as litter traits for predicting litter C and N turnover across all five biomes. The identification of common drivers in our large-scale ecosystem comparison suggests a basis to develop common models across aquatic and terrestrial ecosystems for C and N dynamics during decomposition. Future modelling efforts should account for the global similarities (litter micronutrient effects) and biome-level differences (contingent decomposer effects) found between ecosystems.

When does diversity matter? Species functional diversity and ecosystem functioning across habitats and seasons in a field experiment

Despite ample experimental evidence indicating that biodiversity might be an important driver of ecosystem processes, its role in the functioning of real ecosystems remains unclear. In particular, the understanding of which aspects of biodiversity are most important for ecosystem functioning, their importance relative to other biotic and abiotic drivers, and the circumstances under which biodiversity is most likely to influence functioning in nature, is limited. We conducted a field study that focussed on a guild of insect detritivores in streams, in which we quantified variation in the process of leaf decomposition across two habitats (riffles and pools) and two seasons (autumn and spring). The study was conducted in six streams, and the same locations were sampled in the two seasons. With the aid of structural equations modelling, we assessed spatiotemporal variation in the roles of three key biotic drivers in this process: functional diversity, quantified based on a species trait matrix, consumer density and biomass. Our models also accounted for variability related to different litter resources, and other sources of biotic and abiotic variability among streams. All three of our focal biotic drivers influenced leaf decomposition, but none was important in all habitats and seasons. Functional diversity had contrasting effects on decomposition between habitats and seasons. A positive relationship was observed in pool habitats in spring, associated with high trait dispersion, whereas a negative relationship was observed in riffle habitats during autumn. Our results demonstrate that functional biodiversity can be as significant for functioning in natural ecosystems as other important biotic drivers. In particular, variation in the role of functional diversity between seasons highlights the importance of fluctuations in the relative abundances of traits for ecosystem process rates in real ecosystems.

Trophic complexity enhances ecosystem functioning in an aquatic detritus‐based model system

1. Understanding the functional significance of species interactions in ecosystems has become a major challenge as biodiversity declines rapidly worldwide. Ecosystem consequences arising from the loss of diversity either within trophic levels (horizontal diversity) or across trophic levels (vertical diversity) are well documented. However, simultaneous losses of species at different trophic levels may also result in interactive effects, with potentially complex outcomes for ecosystem functioning. 2. Because of logistical constraints, the outcomes of such interactions have been difficult to assess in experiments involving large metazoan species. Here, we take advantage of a detritus-based model system to experimentally assess the consequences of biodiversity change within both horizontal and vertical food-web components on leaf-litter decomposition, a fundamental process in a wide range of ecosystems. 3. Our concurrent manipulation of fungal decomposer diversity (0, 1 or 5 species), detritivore diversity (0, 1 or 3 species), and the presence of predatory fish scent showed that trophic complexity is key to eliciting diversity effects on ecosystem functioning. Specifically, although fungi and detritivores tended to promote decomposition individually, rates were highest in the most complete community where all trophic levels were represented at the highest possible species richness. In part, the effects were trait-mediated, reflected in the contrasting foraging responses of the detritivore species to predator scent. 4. Our results thus highlight the importance of interactive effects of simultaneous species loss within multiple trophic levels on ecosystem functioning. If a common phenomenon, this outcome suggests that functional ecosystem impairment resulting from widespread biodiversity loss could be more severe than inferred from previous experiments confined to varying diversity within single trophic levels.

Gondwanan mesotherms and cosmopolitan eurytherms: effects of temperature on the development and survival of Australian Chironomidae (Diptera) from tropical and temperate populations

In temperate regions of the northern hemisphere, where stream thermal regimes fluctuate seasonally and predictably, temperature has a role in niche segregation and maintenance of patterns of lotic diversity and distribution, as described by the ‘Thermal Equilibrium Hypothesis’. In Australia, the role of temperature in regulating patterns of diversity and distribution has been obscure, as seasonal variation in stream temperatures can be exceeded by stochastic fluctuation in flow. The thermal responses of five lotic Chironomidae (Diptera) species, contrasting in biogeographic (evolutionary) history, from warm tropical and cool temperate Australian populations, were investigated. All species, including postulated cool-stenotherms, showed broadly eurythermic developmental and morphological responses, and maintained both survivorship and oocyte production at elevated temperatures despite reductions in overall body size. There were subtle differences among species according to biogeographic affinity, with tolerances of Gondwanan species, which were narrower than those of cosmopolitan species, best characterised as ‘mesothermic’, but there was little divergence between populations. These results have implications for the understanding of diversity and distribution of Australian chironomids, and indicate that applicability of the Thermal Equilibrium Hypothesis to Australian lotic faunas may be limited.

Colonisation of experimentally immersed wood in south eastern Australia : Responses of feeding groups to changes in riparian vegetation

We investigated macroinvertebrate abundance and functional feeding groups colonising experimentally-positioned woody substrates of different species in streams with three different riparian vegetation types. Native Eucalyptus forest formed a dense closed canopy over our streams; introduced (exotic, alien) pine plantation forest did not fully shade the streams, and grassland streams were completely open, although with woody riparian vegetation well upstream of our sites. Macroinvertebrate assemblages varied taxonomically and functionally with both wood species and riparian vegetation composition. Two specialist feeding groups responded clearly to riparian vegetation: wood gougers were most common in forested streams, and algal grazers in more open streams. Gougers colonised native Eucalyptus wood in preference to alien species. Other feeding groups responses showed complex interactions between vegetation and wood type. Our results indicate the importance of sampling appropriate substrates when assessing questions of this type – if seeking shifts in functional organisation, the substrates on which the feeding groups of interest occur must be sampled. The composition of the riparian strip may influence xylophilous communities as much as the structure (i.e. whether closed or open).