Virtual Issue: Towards a mechanistic understanding of global change ecology

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November 2016

As part of Functional Ecology's 30th anniversary celebrations, the Journal is holding a special Thematic Topic at this year's BES annual meeting in Liverpool. The theme of the thematic is "Towards a mechanistic understanding of global change ecology". Functional Ecology has published some seminal work in this area and, using our back content as a guide, speakers from our editorial board will look to the future of the topic with a series of exciting talks starting from at the organism level, moving on to communities and ending at the whole ecosystem scale .  

For this Virtual Issue, we asked each of our speakers to look through the Functional Ecology archive and select three or four papers that informed their talk, and to tell us why each paper has been selected. The speakers and the subject of their talks are listed below. All the papers are free to access. 

 

Craig White - Thermal tolerance and adaptation to climate changes

Animals can respond to a changing thermal environment in three main ways: they can move to track the changing environmental temperature, they can alter their phenotypes through plasticity and adaptation to compensate for the changing temperature, or they can die. This collection of papers published in Functional Ecology over the last 6 years addresses the second option, using mainly Drosophila melanogaster as a model organism to examine the capacity of animals to cope with environmental change.
Rezende et al (2011) approach the problem from a methodological perspective, using published data and a mathematical model to predict the consequences of experimental context for estimates of the genetic and environmental components of phenotypic variance in thermal tolerance. Estimates of these variances are important because a trait needs genetic variance in order to exhibit a response to selection. Based on their model, Rezende et al (2011) predict that heritability – the ratio of genetic to total phenotypic variance – will be lower when measured using a ramping protocol in which temperature rises slowly over a long period, and higher when animals are exposed to a constant high temperature (a static protocol). Mitchell and Hoffman (2010) observe such a pattern, finding a reduced adaptive capacity for thermal tolerance measured under ramping. They found that this pattern arises because genetic variance is lower when estimated using a ramping protocol, suggesting that Drosophila melanogaster appears to have little evolutionary potential to extend its upper thermal range under ramping conditions. Hangartner and Hoffman (2016) extended this work, showing that artificial selection for static thermal tolerance caused a correlated increase in ramping thermal tolerance. This finding suggests that static and ramping thermal tolerance are genetically correlated, and therefore that the response to selection will depend on the multivariate genetic architecture of thermal tolerance traits as well as the type of thermal stress experienced (see also Blackburn et al. 2014, J. Exp. Biol. 217, 1918-1924). Overall, however, responses to selection may not be sufficient to keep pace with predicted temperature increases (Hangartner and Hoffman 2016). In the absence of adaptation, animals might use phenotypic plasticity to remodel their physiology to cope with increased temperatures. As with adaptation, however, it seems that plasticity may not be sufficient to keep pace with predicted temperature increases. van Heerwarden et al (2016) show that Drosophila melanogaster exhibits plasticity in upper thermal tolerance, as do many species (e.g. Seebacher et al 2015, Nat. Clim. Change, 5, 61-66), but that the improvement to tolerance conferred by plasticity is modest (no more than 1.01 °C). Overheating risk will therefore be only minimally improved by plasticity.

Thermal ramping rate influences evolutionary potential and species differences for upper thermal limits in Drosophila
Mitchell, K. A. and Hoffmann, A. A. (2010)

Estimating the adaptive potential of critical thermal limits: methodological problems and evolutionary implications
Rezende, E. L., Tejedo, M. and Santos, M. (2011)

Evolutionary potential of multiple measures of upper thermal tolerance in Drosophila melanogaster
Hangartner, S. and Hoffmann, A. A. (2016)

Limited scope for plasticity to increase upper thermal limits
van Heerwaarden, B., Kellermann, V. and Sgrò, C. M. (2016)

Sergio Rasmann - Climate driven changes in plant-herbivore interactions

Understanding how plants and their associated communities will respond to the intensification of global climate change drivers is one of the most crucial exercises needed for preserving biodiversity and maintaining food security. Plants are constantly coping with an extremely complex biotic and abiotic environment. They have evolved a complex immune system for reducing herbivore and pathogen attack, as well as adaptations to deal with abiotic stressors. While most traits have evolved specifically to deal with either biotic or abiotic stress, several traits can serve both functions. In addition, the up-regulation of the stress-responses, both biotic and abiotic, is orchestrated by a similar complex signalling hormonal network. Pineda et al. (2013), in their comprehensive review that integrates several fields of research, spanning from plant physiology, microbial ecology, and functional ecology, outline a mechanistic framework of how plants-microbe-animal interaction could be affected by several global change drivers in the near future.
Probably one of the most documented effects of global climate change is the response of communities to global warming and associated organisms’ range shifts to higher latitudes and altitudes. Such displacements of populations have raised several concerns, including loss of biodiversity, population mismatches between predators and prey, or between herbivorous insects and their host plants. For instance, it has been postulated that Alpine or Arctic ecosystems will suffer from competition from warm-adapted, invading species. Classic examples include the faster colonisation of colder environment by herbivorous insects. How, the low-level-herbivore-pressure-adapted plants will cope with increasing levels of herbivory remains a central question and is tackled in the review by Rasmann et al. (2014). They suggest that, while high elevation plants are less defended against herbivory, due to high protection against abiotic stress may be already ecologically fitted to resist the sudden increase in herbivory pressure that they will likely experience during global change. Along the same lines, Kaarlejärvi et al. (2013) showed that mammalian grazing limited the growth of warm-adapted plants transplanted at higher elevations, indicating that the expansion of lowland plant species to higher altitudes with warming may be hampered by herbivory. Interestingly, while warm-adapted plants responded to warming and fertilisation, tundra plants did not. This suggests that upward migration might transform Alpine communities to be more responsive to warmer climate and nutrient loads. Overall, the ultimate plants’ responses to predicted increases in herbivory during climate change will be the outcome of genetic and epigenetic variation, phenotypic plasticity and rate of adaptation. Nonetheless, while the defence mechanisms and pathways are largely known for a few model plant species, the overall diversity of defences across the plant tree of life is largely unknown, limiting our ability to predict the outcome of novel plant-insect interactions, and ultimately how whole communities will transform out under climate change.

Herbivory prevents positive responses of lowland plants to warmer and more fertile conditions at high altitudes
Kaarlejärvi, E., Eskelinen, A. and Olofsson, J. (2013)

Beneficial microbes in a changing environment: are they always helping plants to deal with insects?
Pineda, A., Dicke, M., Pieterse, C. M.J. and Pozo, M. J. (2013)

Climate-driven change in plant–insect interactions along elevation gradients
Rasmann, S., Pellissier, L., Defossez, E., Jactel, H. and Kunstler, G. (2014)

James Bell - Trophic structures in a changing world

In Pierce et al. (2016)I have chosen a paper that has yet to be published in an issue in Functional Ecology but will undoubtedly receive many citations in the years to come. Grime's competitor, stress-tolerator, ruderal (CSR) theory was erected in the 1970s and it was ahead of its time in terms of models based on trait classification. Things have moved on and what the current authors have done is here remarkable for its ambition and scale because they have sought to understand combinations of leaf traits globally. Well over 100,000 records were analysed with data coming from all continents except Antarctica. The advantage of this approach is that CSR strategies won’t be locally defined as they have in the past because diverse and seemingly unrelated habitats (e.g. tropical broadleaf rainforest, desert shrublands, mangroves and alpine pasture) were used. With this tool, community assembly can be predicted and that will be useful for studies where habitat or climate change is of central interest.
We know that climate change can have a profound effect on the phenology and behaviour of plants and animals. More specifically, the reproduction dates of birds have been shown to advance as the world warms. Saino et al (2004), now more than a decade old, showed the profound effect of temperature not only on egg mass but also its quality as measured by lutein and lysozyme concentrations. As the authors were quick to point out, no study previous to this had investigated the change in egg composition in any wild bird population so Functional Ecology got an exclusive. The main finding of interest for me was that concentrations of these compounds increased with temperature and that’s not a bad thing: lysozyme, for example, has a positive effect on hatchability of eggs and lutein has antioxidant properties. This study suggests that barn swallows have every reason to match reproduction to temperature, although that is increasingly a challenge and may become more chaotic.
The study of personality in animals is a relatively new field but even so, behavioural syndromes have shown to be widespread in spiders. Royauté et al. (2015) used Eris militaris, a rather handsome bronzed-coloured jumping spider to test for personality changes when subjected to sublethal doses of an organophosphate insecticide. The merit in this paper is that it represents a step change to studying the toxicity of insecticides on non-target invertebrates which has in the past relied on very basic LD50 tests and lethal doses. Interestingly, it was only females that showed any effect on movement and prey capture which indicated to the authors that effects may still be present even when population-wide behavioural shifts remain undetected. Sublethal effects are likely to be short-lived but even so, it would be interesting to know how this impacts agroecosystems, particularly if the insecticide strategy is for prophylactic use.

A global method for calculating plant CSR ecological strategies applied across biomes world-wide
Pierce, S., Negreiros, D., Cerabolini, B. E. L. et al. (2016)

Under the influence: sublethal exposure to an insecticide affects personality expression in a jumping spider
Royauté, R., Buddle, C. M. and Vincent, C. (2015)

Timing of reproduction and egg quality covary with temperature in the insectivorous Barn Swallow, Hirundo rustica
Saino, N., Romano, M., Ambrosini, R., Ferrari, R. P. and Møller, A. P. (2004)

C E Tim Paine - Towards a general mechanistic understanding of community assembly

These papers encapsulate what I see as some of the most promising directions to gain deeper insight into the assembly of ecological communities. Kraft et al. (2015) and Craine & Dybzinski (2013) revisit topics that have long been known to shape ecological communities: ecological filtering and resource competition, respectively. Synthesising recent gains in understanding, they sharpen the meanings of these concepts, with the goal of gaining new insight. Eisenhauer et al. (2013) take a complementary but also profitable approach via manipulative experimentation. Most ecological communities are composed of wide-ranging long-lived organisms. By manipulating microbial communities in microcosms, Eisenhauer et al (2013) operationalise the ever-slippery concept of the ecological niche, and evaluate the relationships between niche dimensionality, invasibility and diversity. If we are to effectively conserve, manage and restore ecological communities, we will need further conceptual and experimental work.

Mechanisms of plant competition for nutrients, water and light.
Craine, J.M. and Dybzinski, R. (2013)

Niche dimensionality links biodiversity and invasibility of microbial communities.
Eisenhauer, N., Schulz, W., Scheu, S. & Jousset, A. (2013)

Community assembly, coexistence and the environmental filtering metaphor.
Kraft, N.J.B., Adler, P.B., Godoy, O., James, E.C., Fuller, S. & Levine, J.M. (2015)

Julia Koricheva - Mechanisms underlying biodiversity effects on ecosystem function

Early research on biodiversity effects on ecosystem functioning has been focused largely on consequences of species loss with biodiversity assessed as species richness. However, species diversity is only one of the facets of biodiversity and is not necessarily the most relevant one from the functional point of view. The three selected papers expanded the research on mechanisms of biodiversity effects on ecosystem functioning by exploring other dimensions of biodiversity: functional diversity (Mouchet et al. 2010), indirect genetic effects (Bailey et al. 2013) and ecological interactions between species (Valiente-Banuet et al. 2014).
Many key functional aspects of ecosystems closely depend on interactions between species (e.g. pollination and seed dispersal), but consequences of extinction of ecological interactions have been studied considerably less than consequences of species extinctions. Valiente-Banuet et al. (2014) propose a novel mechanistic model that relates the diversity of both species and interactions between them to the loss of ecological functions. The study finds that the extinction of interactions can be decoupled from the extinction of species and that loss of ecological interactions often precedes species loss, hence affecting ecosystem functions and services at a faster rate than species extinctions. This highlights the importance of including species interactions as the major biodiversity component.
Bailey et al. (2013) review the theory and the empirical evidence for the indirect genetic effects (IGEs) and interspecific genetic effects (IIGEs) as mechanisms of genotypic diversity effects on ecosystem functioning. These effects occur when the expression of genes in a conspecific (IGEs) or heterospecific (IIGEs) neighbour affects the phenotype of a focal species. Bailey et al. show that IGEs and IIGEs are common, albeit often overlooked, mechanisms behind the nonadditive outcomes in genotypic diversity studies. These effects also have primary roles in co-evolutionary process and coadaptation, making them potentially crucial in a climate change context.
Species are not equal in their effects on ecosystem functioning due to differences in their functional traits. Multiple indices of functional diversity have been introduced as a way to assess the diversity of functional traits displayed by species within a community, but there is no consensus on how to quantify the functional diversity. Mouchet et al. (2010) built a typology of existing indices addressing three different facets of functional diversity: functional richness, functional evenness and functional divergence. They investigated the behaviour and redundancy of these indices using artificial datasets and provided guidelines for choosing appropriate functional diversity indices depending on the research question.

Indirect genetic effects: an evolutionary mechanism linking feedbacks, genotypic diversity and coadaptation in a climate change context
Joseph K. Bailey, Mark A. Genung, Ian Ware et al. (2014)

Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules
Maud A. Mouchet, Sébastien Villéger, Norman W. H. Mason and David Mouillot (2010)

Beyond species loss: the extinction of ecological interactions in a changing world
Alfonso Valiente-Banuet, Marcelo A. Aizen, Julio M. Alcántara et al (2015)

Emma Sayer - Dealing with tropical forest diversity to measure ecosystem-level responses to change - lessons learned from fertilisation experiments

Tropical forests underpin a large number of important processes and changes to tropical forest ecosystems could have consequences at a global scale. Although research into ecosystem functioning in tropical forests has advanced rapidly in the last decade, it remains notoriously challenging because of the incredibly high biodiversity in many tropical regions. Approaches using species' traits to common ecological identify patterns could provide a promising solution to deal with highly diverse systems such as tropical forests. Research published in Functional Ecology has demonstrated that, even within a single genus of tropical trees, the traits of individual species can vary widely depending on soil fertility and the life-stage of the individuals (Palow et al. 2012), and hence using functional groups instead of taxonomic identity could resolve some of the issues we face in dealing with tropical diversity. Trait-based approaches have demonstrated that there are clear life-history strategy trade-offs between growth and drought tolerance along a strong rainfall gradient (Brenes-Arguedas et al. 2013) and that community assembly during tropical forest succession appears to be driven by competitive interactions and abiotic conditions (Buzzard et al. 2016). These, and other studies, suggest that we may be able to use trait-based approaches to predict the responses of tropical forest ecosystems to change (Uriarte et al. 2016), which is one of the greatest current challenges in tropical functional ecology.

Re-growing a tropical dry forest: functional plant trait composition and community assembly during succession. Functional Ecology
Buzzard, V., Hulshof, C. M., Birt, T., Violle, C., Enquist, B. J. (2016)

Functional trait divergence of juveniles and adults of nine Inga species with contrasting soil preference in a tropical rain forest
Palow, D. T., Nolting, K., Kitajima, K. (2012)

Plant traits in relation to the performance and distribution of woody species in wet and dry tropical forest types in Panama
Brenes-Arguedas, T., Roddy, A. B., Kursar, T. A. (2013)

A trait-mediated, neighbourhood approach to quantify climate impacts on successional dynamics of tropical rainforests
Uriarte, M., Lasky, J. R., Boukili, V. K., Chazdon, R. L. (2016)

Carly Stevens - Atmospheric nitrogen deposition and its impact on plant communities

Nitrogen deposition is beginning to decline in parts of Europe and as such, there is an increased interest in how long it will take ecosystems to recover. However, there are few long-term studies of recovery from nitrogen addition. Strengbom et al (2001) represents one of the few studies that have examined recovery in a range of ecosystem variables where N has been added over long periods and recovery times span several decades.
Typically responses to N addition are predicted based on growth strategy, with competitive species tending to benefit whilst stress tolerators decline. However, there has been little investigation of the evolutionary basis for these responses. Wooliver et al. (2016) examine the evolutionary processes guiding trade-offs in competitive and conservative growth responses to N addition.
The final paper (Hodgeson et al. 2014) is not a paper specifically about nitrogen deposition but one that highlights the importance of eutrophication as a driver of species responses across trophic levels. There are very few studies that have examined responses to large-scale drivers on multiple trophic levels making this a 'must read paper'. Nitrogen deposition is only one potential cause of eutrophication in terrestrial environments but with critical loads for nitrogen deposition exceeded in many regions it is one that we cannot ignore.

Slow recovery of boreal forest ecosystem following decreased nitrogen input
Strengbom, J., Nordin, A., Näsholm, T. and Ericson, L. (2001)

Plant functional constraints guide macroevolutionary trade-offs in competitive and conservative growth responses to nitrogen
Rachel Wooliver, Alix A. Pfennigwerth, Joseph K. Bailey and Jennifer A. Schweitzer (2016)

A trait-mediated, neighbourhood approach to quantify climate impacts on successional dynamics of tropical rainforests
Hodgson, J. G., Tallowin, J., Dennis, R. L. H. et al. (2014)

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