Reclaiming contaminated land through manipulating biodiversity

Contents of this post originally appeared on the Applied Ecologist, but with expanded thoughts here.

Five years ago I spent my sabbatical in China and worked closely with a lab in Guangzhou. While there, I built meaningful collaborations and friendships that have continued to advance the science I'm involved with. While in China, I accompanied my friend, Jin-tian Li to a biodiversity field experiment on contaminated post-mining lands in Hunan province, and our discussions led to the just-published paper (please e-mail me if you want a copy) in the Journal of Applied Ecology, first-authored by a former PhD student in my lab, Pu Jia.

Why do we care about degraded lands?

According to the IPBES report on land degradation, the degradation of productive lands and intact habitats is a major threat to sustainability, biodiversity and ecosystem functioning globally, which reduces the resiliency of ecological and economic systems. In many emerging economy countries, environmentally harmful practices that result in contamination render lands and habitats seriously degraded. In many circumstances, the restoration of contaminated habitats to original conditions is not an option because the capacity for these habitats to harbor intact native ecosystems is greatly compromised. In these cases, we need management options that allow us to reclaim contaminated and degraded lands (Nathanail & Bardos 2005), and preferably ones that increase biodiversity and ecosystem function (Rohr et al. 2016).

The potential role of biodiversity in reclaiming contaminated lands

While the ecological literature on the linkages between biodiversity and ecosystem function is vast and rich (e.g., Tilman, Isbell & Cowles 2014), the application of this field of research to reclaiming contaminated lands has been strangely depauperate, and so there’s little guidance on whether we should be planting diverse plant assemblages on contaminated lands, or if we ought to simply plant the most productive species or those that provide efficient phyto-removal of contaminants. This question is of fundamental importance to places like China, where rapid development and industrialization through the 1970s-1990s resulted in severe contamination of lands near mining and mineral processing facilities (Li et al. 2019), and now with China’s commitment to improving it’s environmental health, biodiversity research has the ability to impact policy and management at a national scale.

Our paper

We evaluated whether more diverse plantings increased reclamation and ecosystem functioning of a mine wasteland in Hunan Province, China, which had been severely contaminated with cadmium and zinc over decades. We sowed plots with 1-16 species and these were selected from the herbaceous species that grew around contaminated sites in the region, and more diverse assemblages produced more biomass and were more stable over time. Further, there was less heavy metal contamination of leaf tissues in the more diverse plantings, which reduces the impact on herbivores.

Importantly though, plant diversity spurred plant-soil feedbacks (PSFs) that appeared to drive the increased ecosystem functioning. Higher plant diversity supported higher soil bacterial and fungal diversity. Importantly, higher plant diversity was accompanied with more soil cellulolytic bacteria that exude enzymes that degrade cellulose and so drive decomposition and nutrient cycling, which are essential components of a functioning ecosystem. 




Furthermore, the multi-species assemblages also performed better because these high diversity treatments harboured fewer soil fungal pathogens (and by extension more beneficial soil fungi). This appeared to be driven by the fact that high plant diversity supported a greater diversity of soil chitinolytic bacteria that produce anti-fungal enzymes that degrade the chitin in cell walls of soil-borne plant-pathogenic fungi.

In the search for efficient ways to reclaim contaminated lands, sowing high-diversity plant assemblages appear to be an effective tool. The key for reclamation is to ensure that soil processes like decomposition and nutrient cycling are able to support a self-sustaining ecosystem, and higher plant diversity can ensure this. The next steps will be to field test this in real reclamation projects and to see this research work its way into best practices.

Li, T., Liu, Y., Lin, S., Liu, Y. & Xie, Y. (2019) Soil pollution management in China: a brief introduction. Sustainability, 11, 556.

Nathanail, C.P. & Bardos, R.P. (2005) Reclamation of contaminated land. John Wiley & Sons.

Rohr, J.R., Farag, A.M., Cadotte, M.W., Clements, W.H., Smith, J.R., Ulrich, C.P. & Woods, R. (2016) Transforming ecosystems: when, where, and how to restore contaminated sites. Integrated Environmental Assessment and Management, 12, 273-283.

Tilman, D., Isbell, F. & Cowles, J.M. (2014) Biodiversity and ecosystem functioning. Annual Review of Ecology, Evolution and Systematics, 45, 471-493.

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Moving on up to the regional scale

Like the blind men and the elephant, perspective drives understanding in ecology. The temporal and spatial scale of analysis (let alone the system and species you focus on) has major implications for your conclusions. Most ecologists recognize this fact, but consider only particular systems, scales or contexts due to practical limitations (funding, reasonable experimental time frames, studentship lengths). 

Ecologists have long known that regional processes affect local communities and that local processes affect regional patterns. Entire subfields like landscape ecology, metapopulations, metacommunities, and biogeography (species area relationships) highlight these spatial dependencies. But high-profile ecological research into biodiversity and ecosystem functioning ('BEF') primarily considers only local communities. Recently though, the literature has started to fill this gap and asking what BEF relationships look like at larger spatial scales, and how well local BEF relationships predict those at larger spatial scales.

'Traditional' BEF experiments were done at relatively small spatial scales (often only a few meters^2). Positive BEF relationships were commonly observed, but often were quite saturating – that is, only a few species were necessary to optimize the function of interest. If the impact of biodiversity saturates with only a few species, it would seem that surprisingly few species are necessary to maintain functioning. True, studies that considered multiple ecosystem functions are more likely to conclude that additional diversity is required for optimal functioning (e.g. Zavaleta et al. 2010). But a simplistic evaluation of the facts that a) ecosystem functioning rapidly saturates with diversity, and b) locally, diversity may not be generally decreasing (Vellend et al. 2017), could lead to overly confident conclusions about the dangers of biodiversity loss. Research on BEF relationships, as they transition from local to larger spatial scales, is increasingly suggesting that our understanding is incomplete, and that BEF relationships can grow stronger at large spatial scales.

A number of recent papers have explored this question, and in considering the essential role of spatial scale. Predictions about how BEF relationships will change with spatial scale vary. On one hand, in most systems there are only a few dominant species and these species may disproportionately contribute to ecosystem functions, regardless of the spatial scale. On the other hand, species-area relationships tend to increase rapidly at small scales, as community composition turns over. If that is the case, then different species may make important contributions in different places. Winifree et al. (2018) contrasted these predictions for three crop species that rely on natural bee pollinators (cranberries, blueberries, and watermelons). They censused pollinators at 48 sites, over a total extent of ~3700 km^2. Though at local scales very few bee species were required to reach pollination goals, the same goals at larger spatial scales required nearly an order of magnitude more bee species. These results in particular appeared to be driven by species turnover among sites--perhaps due to underlying environmental heterogeneity.

From Winifree et al. "Cumulative number of bee species required to maintain thresholds of 25% (orange), 50% (black), and 75% (purple) of the mean observed level of pollination, at each of n sites (16). Horizontal dashed lines indicate the total number of bee species observed in each study. Error bars represent 1 SD over all possible starting sites for expanding the spatial extent. For all three crops combined, each x-axis increment represents the addition of one site per crop".

Another mechanism for increased BEF at larger scales is insurance effects. The presence of greater diversity can interact with spatial and temporal environmental variation to increase or stabilize ecosystem functioning. Greater diversity should maximize the differential responses of species to changing conditions, and so buffer variation in ecosystem functioning. Such effects, when they occur through time are temporal insurance, and when they occur via dispersal among sites, spatial insurance. Wilcox et al. (2018) considered the role of synchrony and asynchrony among populations, communities, and metacommunities to ask whether local asynchrony affected stability (see Figure below for a nice conceptual explanation). Across hundreds of plant data sets, they found that asynchrony of populations did enhance stability. However, the degree to which it affected stability varied from very weak to very important (e.g. by 1% to 300%). Maximizing species or population differences at local scales apparently can have implications for dynamics, and so potentially stability of functioning, at much larger scales.

From Wilcox et al. "Conceptual figure showing how stability and synchrony at various spatial scales within a metacommunity combine to determine the stability of ecosystem function (here, productivity). In (a), high synchrony of species within and among local communities results in low stability at the scale of the metacommunity. In (b), species remain synchronised within local communities, but the two communities exhibit asynchronous dynamics due to low population synchrony among local patches. This results in relatively high gamma stability. Lastly, in (c), species exhibit asynchronous dynamics within local communities through time, and species-level dynamics are similar across communities (i.e. high population synchrony). This results in relatively high gamma stability. Blue boxes on the right outline stability components and mechanisms, and the hierarchical level at which they operate. Adapted from Mellin et al. (2014)."

Finally, Isbell et al. (2018) describe ways in which ecosystem functioning and other contributions of nature to humanity are scale-dependent, laying out the most useful paths for future work (see figure below).

From Isbell et al. 2018.

These papers make nearly identical points worth reiterating here: 1) we have done far too little work beyond the smallest spatial scales (~3 m^2) and so lack necessary knowledge of the impacts of losing of biodiversity, and 2) policy decisions and conservation activities are occurring at much larger scales – at the scale of the park, the state, or the nation. Bridging this gap is essential if we are to make any reasonable arguments as to why ecosystem function figure into  large-scale conservation activities.

References:
Sustaining multiple ecosystem functions in grassland communities requires higher biodiversity. Erika S. Zavaleta, Jae R. Pasari, Kristin B. Hulvey, G. David Tilman. Proceedings of the National Academy of Sciences Jan 2010, 107 (4) 1443-1446; DOI: 10.1073/pnas.0906829107. 

Plant biodiversity change across scales during the Anthropocene. Vellend, Mark, et al. Annual review of plant biology 68 (2017): 563-586.

Species turnover promotes the importance of bee diversity for crop pollination at regional scales. RACHAEL WINFREE, JAMES R. REILLY, IGNASI BARTOMEUS, DANIEL P. CARIVEAU, NEAL M. WILLIAMS, JASON GIBBS. SCIENCE16 FEB 2018 : 791-793

Asynchrony among local communities stabilises ecosystem function of metacommunities. Kevin R. Wilcox, et al. Ecology Letters. Volume 20, Issue 12, Pages 1534–1545.

Isbell, Forest, et al. "Linking the influence and dependence of people on biodiversity across scales." Nature 546.7656 (2017): 65.

Decomposing diversity effects within species

The relationship between biodiversity and ecosystem functioning is so frequently discussed in the ecological literature that it has its own ubiquitous acronym (BEF). The literature has moved from early discussions and disagreements about mechanism, experimental design, and species richness to ask how different components of biodiversity might contribute differentially to functioning. The search is for mechanisms which hopefully will lend predictability to biodiversity-function relationships. One approach is to independently manipulate different facets of biodiversity – whether species, phylogenetic, trait-based, or genetic diversity – to help disentangle the relative contribution of each.

A new paper extends this question by considering how within-species diversity – including genotypic richness, genetic differences, and trait differences – contribute to functioning. Abbott et al. (2017, Ecology) use a field-based eelgrass system to explore how independent manipulations of genotypic richness and genetic relatedness affected biomass production and invertebrate community richness. They collected 41 unique genotypes of eelgrass (Zostera marina), and used 11 species-relevant loci to determine the relatedness of each genotype pair. The authors also measured 17 traits relevant to performance including "growth rate, nutrient uptake, photosynthetic efficiency, phenolic content, susceptibility to herbivores, and detrital production ".

Eelgrass meadow.
From
http://www.centralcoastbiodiversity.org/
eelgrass-bull-zostera-marina.html

Each of these of these measures are inter-related, but not necessarily in clear, predictable fashions. Genotypes likely differ functionally, but some traits and some genotypes will vary more than others. Genetic distances or relatedness between species similarly may be proxies for trait differences, but this depends on the underlying evolutionary processes. The relationship between any of these measures and functions such as biomass production are no doubt varied and dependent on the mechanism.

The authors established plots with two levels of genotypic richness, either 2 genotypes or 6 genotypes, where genotypes varied among the 41 available. Fully crossed with the genotypic richness treatment was a genetic relatedness treatment: genotypes were either more closely related than a random selection, less closely related, or as closely related as random. At the end of the experiment, above and belowground biomass were collected, and epifaunal invertebrates were collected, and modelled as a component of the biodiversity components.

Because of early die-offs in many plots, planted genotype richness differed from final richness greatly (very few plots had 6 genotypes remaining, for example). For that reason, final diversity measures were used in the models. The relationship between aboveground biomass or belowground biomass and biodiversity were similar: both genotypic richness and genotypic evenness were positively related to total final biomass, but genetic relatedness was negatively correlated. That is, plots with more related genotypes were less productive. Other variables such as trait diversity was not as important, and in fact they did not find any relationship between trait differences and degree of genetic relatedness between genotypes. Since relatedness seemed unrelated to functional similarities, between genotypes, the authors suggested that possibly that reduced biomass among related genotypes is due to self-recognition mechanisms. Most interestingly, the best predictors of invertebrate grazer diversity were opposite -  – the best predictor was trait diversity, not genotypic richness or genetic relatedness.

Even in this case, where Abbott et al. were able to separate different diversity components experimentally, it's clear that simplistic predictions as to how they contribute to functioning are insufficient. The contributions of genotypic versus trait diversity were not strongly related. Further, trait diversity performed best on the function for which genotypic diversity performed worst. Understanding what this means is difficult - are the traits relevant for understanding intraspecific interactions (resource usage, etc) so incredibly different from those relevant for interspecific interactions with herbivores? Are the 17 traits too few to capture all differences, or too many irrelevant traits? Do we expect different biodiversity facets have unique independent effects on ecosystem functions, or does the need to consider multiple facets simply mean we have an imperfect understanding of how different facets are related? 

The pessimistic and optimistic view of BEF experiments?

The question of the value of biodiversity-ecosystem function (BEF) experiments—their results, their relevancy—has become a heated one in the literature. An extended argument over the last few years has debated the assumption that local biodiversity is in fact in decline (e.g. Vellend et al. 2013; Dornelas et al. 2014; Gonazalez et al. 2016). If biodiversity isn't disappearing from local communities, the logical conclusion would be that experiments focussed on the local impacts of biodiversity loss are less relevant.

Two papers in the Journal of Vegetation Science (Wardle 2016 and Eisenhauer et al. 2016) continue this discussion regarding the value of BEF experiments for understanding biodiversity loss in natural ecosystems. From reading both papers, it seems as though broadly speaking, the authors agree on several key points: that results from biodiversity-ecosystem functioning experiments don’t always match observations about species loss and functioning in nature, and that nature is much more complex, context-dependent, and multidimensional than typical BEF experimental systems. (The question of whether local biodiversity is declining may be more contested between them). 

Biodiversity and ecosystem experiments typically involve randomly assembled plant communities containing either the full complement of species, or subsets containing different numbers of species. Communities containing lower numbers are meant to provide information about the loss of species diversity a system. Functions (often including, but not limited to, primary productivity or biomass) are eventually measured and analysed in relation to treatment diversity. Although some striking results have come out of these types of studies (e.g. Tilman and Downing 1996), they can vary a fair amount in their findings (Cardinale et al. 2012).

David Wardle’s argument is that BEF experiments differ a good deal from natural systems: in natural systems, BEF relationships can take different forms and explain relatively little variation, and so extrapolating from existing experiments seems uninformative. In nature, changes in diversity are driven by ecological processes (invasion, extinction) and experiments involving randomly assembled communities and randomly lost species do nothing to simulate these processes. Wardle seems to feel that the popularity of typical BEF experiments has come at the cost of more realistic experimental designs. This is something of a zero-sum argument, (although in some funding climates that may be true...). But it is true that big BEF experiments tend to be costly and take time and labour, meaning that there is an impetus to publish as much as possible from each one. Given BEF experiments have changed drastically in design once already, in response to criticisms about their inability to disentangle complementarity vs. portfolio effects, it seems they are not inflexible about design though.

Eisenhauer et al. agree in principle that current experiments frequently lack a realistic design, but suggest that there are plenty of other types of studies (looking at functional diversity or phylogenetic diversity, for example, or using random loss of species) being published as well. For them too, there is value in having multiple similar experiments: this allows metaanalysis and comparison aggregation, and will help to tease apart the important mechanisms eventually. Further, realism is difficult to obtain in the absence of a baseline for a “natural, untouched, complete system” from which to remove species.

The point that Eisenhauer et al. and Wardle appear to agree on most strongly is that real systems are complex, multi-dimensional and context-dependent. Making the leap from a BEF experiment with 20 plant species to the real world is inevitably difficult. Wardle sees this is a massive limitation, Eisenhauer et al. sees it as a strength. Inconsistencies between experiments and nature are information that highlight when context matters. By having controlled experiments in which you vary context (such as by manipulating both nutrient level and species richness), you can begin to identify mechanisms.

Perhaps this is the greatest problem with past BEF work, is that there is a tendency to oversimplify the interpretation of results – to conclude that ‘loss of diversity is bad’ but with less attention to ‘why’, 'where', or 'when’. The best way to do this depends on your view of how science should progress. 

Wardle, D. A. (2016), Do experiments exploring plant diversity–ecosystem functioning relationships inform how biodiversity loss impacts natural ecosystems?. Journal of Vegetation Science, 27: 646–653. doi: 10.1111/jvs.12399

Eisenhauer, N., Barnes, A. D., Cesarz, S., Craven, D., Ferlian, O., Gottschall, F., Hines, J., Sendek, A., Siebert, J., Thakur, M. P., Türke, M. (2016), Biodiversity–ecosystem function experiments reveal the mechanisms underlying the consequences of biodiversity change in real world ecosystems. Journal of Vegetation Science. doi: 10.1111/jvs.12435

Additional References:
Vellend, Mark, et al. "Global meta-analysis reveals no net change in local-scale plant biodiversity over time." Proceedings of the National Academy of Sciences 110.48 (2013): 19456-19459.

Dornelas, Maria, et al. "Assemblage time series reveal biodiversity change but not systematic loss." Science 344.6181 (2014): 296-299.

Gonzalez, Andrew, et al. "Estimating local biodiversity change: a critique of papers claiming no net loss of local diversity." Ecology (2016).

Tilman, David, and John A. Downing. "Biodiversity and stability in grasslands." Ecosystem Management. Springer New York, 1996. 3-7.

Cardinale, Bradley J., et al. "Biodiversity loss and its impact on humanity."Nature 486.7401 (2012): 59-67.

Biodiversity and ecosystem functioning: now with more spatial scales, more functions, and more measures of diversity.

Jae R. Pasari, Taal Levi, Erika S. Zavaleta, and David Tilman. 2013. Several scales of biodiversity affect ecosystem multifunctionality. PNAS. 110:25

Responses:
1) Karel Mokany, Hugh M. Burley, and Dean R. Paini. β 2013. Diversity contributes to ecosystem processes more than by simply summing the parts. PNAS. 110:43.
2) Jae R. Pasari, Taal Levi, Erika S. Zavaleta. 2013. Reply to Mokany et al: Comprehensive measures of biodiversity are critical to investigations of ecosystem multifunctionality. PNAS. 110:43.

One of the big topics in ecology in recent years is ecosystem services and functioning. In particular, the question has been how diversity (in its many forms, including species, intraspecific, phylogenetic, or functional) relates to ecosystem function (often, but not always, measured in terms of productivity). Most often, this is framed as a question about how (alpha) diversity at the local scale affects one or two functional responses. Because diversity can be measured at multiple scales (local, regional or landscape, etc), because how we measure diversity is scale-dependent (i.e. alpha, beta, and gamma diversity), and because a functional ecosystem relies on many different services, the obvious next step is to think of biodiversity and ecosystem functioning in a framework that incorporates multiple spatial scales, multiple functions, and multiple measures of diversity.

A new paper in PNAS takes advantage of David Tilman’s long running Cedar Creek biodiversity experiment to explore how multiple functions in a landscape relates to local and regional diversity, and beta-diversity. In Pasari et al. (2013), the authors use five years of data collected for 168 9x9 m plots in the Cedar Creek experiment. These plots contained 1, 2, 4, 8, or 16 perennial plant species, and had measurements for 8 ecosystem functions (invasion resistance, aboveground NPP, belowground biomass, nitrogen retention, insect richness and abundance, and change in soil C and plant N). The authors simulated combinations of these plots to create 50,000 landscapes composed of 24 local plots. Multi-functionality in this case was the (scaled) mean of each of the 8 functions minus their standard deviation, for the landscape. The authors then asked whether the average alpha-diversity of the local plots, the beta-diversity between plots, and the gamma-diversity of the landscape were important predictors of this multi-functionality.

Not surprisingly, when considering the different functional responses individually, the average alpha-diversity of plots in a landscape was the most important determinant. Past research has shown that as local diversity increases, niches may be filled, or functional redundancy may increase, and so ecosystem functioning tends to increase. When considering all 8 ecosystem functions using a single measure though, beta- and gamma-diversity also appeared to be important, although alpha diversity remains the dominant predictor (figure below). It should be noted though that the total explained variance in functionality was always low. Increasing either alpha- or gamma-diversity increased multi-functionality, while the effect of beta-diversity on ecosystem functioning was not linear. “[O]nly experimental landscapes with low β diversity were capable of achieving very high multi-functionality, whereas high β-diverse experimental landscapes more consistently achieved moderate multi-functionality”. One important conclusion suggested by these results, then, is that even at larger scales the most important determinant of ecosystem function is how local communities are assembling, since this determines local diversity.

These results are an important update to the current state of biodiversity ecosystem function research, and add to the large body of research that says that all types of diversity are important insurance for functioning natural systems. It is difficult from this study to get a clear picture of how important each type of diversity is, and when alpha, beta, and gamma diversity might be more or less important. This is in part because despite the upsides of having multiple years of tightly controlled data from the Cedar Creek data, experimental communities artificially combined into landscapes lack realism. For example, beta-diversity captures turnover between communities that may result from spatial dynamics (environmental heterogeneity, dispersal, biotic interactions). All of these characteristics may be very important for functioning at the landscape scale. The response from Mokany et al. expresses some of these concerns, noting that artificially creating landscapes like this may omit important spatial and temporal connections found in real systems.

In addition, and this is a more technical concern about how alpha, beta, and gamma diversity are defined, I’m not clear on what the implications of using all three measures as explanatory variables in the same model may be. Mostly because under the strictest definitions of diversity, these three terms should be dependent on each other – changes in alpha and beta diversity necessarily alter gamma diversity. The authors didn’t use this definition in their study, but to understand the mechanisms that relate diversity and functionality, it may be more informative to take this inter-relationship into account.

Despite any caveats, I think that a role for beta-diversity in ecosystem functioning will be shown in further work, and perhaps its role will prove to be much greater than these initial results show. As we expand our understanding of the scales at which diversity matters, unfortunately this will no doubt highlight the limitations in our conservation focuses even more.

Why greater diversity – even of parasites – might decrease infections

Pieter T. J. Johnson, Daniel L. Preston, Jason T. Hoverman, and Bryan E. LaFonte. 2013. Host and parasite diversity jointly control disease risk in complex communities. PNAS. Early view.

(Host competence - the tendency of host species to become infected and maintain infection.)

There is often a disconnect between the reality that communities and ecosystems are diverse assemblages with numerous, often complicated and variable interactions, and ecological research, which (perhaps necessarily) focuses on interactions between at most two or three species at a time. Disease ecology similarly has often considered interactions between particular host/parasite species pairs. Some researchers have considered the diversity of host species as an important factor in explaining disease transmission and mortality, but the reality is that parasites also interact, and most hosts harbour multiple parasites. Studying disease dynamics in the context of multi-parasite, multi-host interactions is increasingly recognized as key to understanding disease transmission and severity in communities.

With this in mind, a new paper from Pieter Johnson and colleagues attempts to combine research into the effects of both parasite and host diversity on disease. Two possible hypotheses predict the effect of diversity on disease transmission: the ‘dilution effect’ suggests that the presence of multiple hosts should decrease transmission risk, if the result of additional species is a decline in community competence. It is also hypothesized, somewhat contradictorily, that increased host diversity should support a greater variety of parasites, and parasite life cycles. Both these hypotheses take a host-centric view: understanding how changes in host diversity alter disease risk also requires that we understand how changes in parasite diversity affect disease transmission.

Mutations caused by Ribeiroia infection.
From:http://www.nature.com/scitable/knowledge/library/ecological-consequences-of-parasitism-13255694

The authors looked at the contribution of host and parasite diversity to parasite transmission success using field data and laboratory experiments. First, they looked at existing data on infections of the pathogenic trematode Ribeiroia ondatrae, in amphibian species. Observations showed a positive correlation between larval trematode diversity (parasites) and the richness of free-living species (hosts). Of course the two diversities might be correlated for many unrelated reasons, like site isolation, evolutionary history, or habitat productivity. But a closer analysis showed what appeared to be an interaction between Ribeiroia infection in Pseudacris regilla (Pacific tree frog, the most common amphibian in the survey) and the total number of amphibian species at a site (figure below). Infection by Ribeiroia was highest when there was low amphibian richness and low parasite richness. It dropped significantly lower when amphibian richness was high and/or parasite richness was high.

From Johnson et al. 2013 PNAS. Results of field observations.

In addition to these observations, the authors manipulated both parasite and host species richness, first in small laboratory microcosms and then in larger and more realistic outdoor mesocosms. Results from the laboratory microcosms showed that increases in both amphibian richness (one vs. three species) and parasite richness (one vs. five species) reduced the average number of Ribeiroia in Pseudacris regilla as well as the total infection rate in the amphibian community. The mesocosms had similar results, with both host and parasite diversity negatively influencing Ribeiroia infection. In support of the generality of these results, effect sizes were comparable between the two experiments. These effects were also quite large: for example, in the mesocosm high-host, high-parasite richness treatment there were 52.4% fewer Ribeiroia per P. regilla and 38.2% fewer Ribeiroia overall compared to the low-host, low-parasite richness. Clearly multi-species interactions are crucial for understanding infection by Ribeiroia.

From Johnson et al. 2013 PNAS. Results of the microcosm and mesocosm experiments,
 showing the effects of host and parasite diversity on transmission.

The results make it clear that if you want to understand disease transmission in communities, both host and parasite diversity should be considered. To some extent, both of the initial hypotheses were supported – host and parasite diversity were correlated in the wild, but (in agreement with the dilution effect) infection rates declined as host diversity increased. One factor missing from these hypotheses is the dynamics of the parasite community: in the paper, the authors found models of transmission that included both host and parasite richness were superior. Further, past and future studies that consider only host richness may be inadvertently accounting for the effects of parasite richness on transmission as well, if those two host and parasite diversities are correlated.

There are a number of possibilities for why both host and parasite communities alter parasite transmission success. If host diversity changes the susceptibility of the community to infection (i.e. as diversity increases, the number of low competence/susceptible species increases) then low-competence hosts could act as sinks for parasite infections. Increases in parasite diversity could result in inter-parasite competition and interactions via host immunity.

One future step will be to move beyond simple measurements of species richness to understanding how species identity or characteristics are tied to the putative mechanisms. For example, how do communities of host species vary from low to high diversity sites? Do sites in fact tend to assemble with increasing numbers of low competence host species? The implications are also of interest to other types of studies of community ecology – after all, host-parasite interactions are not very different from predator-prey interactions, and similarly, despite knowing that interactions are complex and involve multiple species, we tend to focus on two or three species examples.

Biodiversity and ecosystem functioning – without fungi?

Different subfields of ecology have a propensity to remain remarkably isolated – researchers in aquatic systems independently develop hypotheses that already exist in some form in other systems, and vice versa. Population ecology and community ecology, despite their obvious relevance to each other, are rarely integrated. There is a tendency – resulting from limits on our time, experience, and possibly imagination – to stay within whatever box we’ve defined for ourselves.

Historically, it seems that biodiversity and ecosystem functioning has lost sight of the progress made in classical ecology in understanding the mechanisms behind species coexistence (and all the functional implications that follow). Studies of ecosystem functioning often vaguely reference concepts such as “niche partitioning”, which would hardly be explicit enough for most papers on coexistence. Fortunately, there are periodically attempts to unifying ecological knowledge.

One of the most important contributions to understanding coexistence is Chesson’s (2000) framework of equalizing and stabilizing effects. Unlike previous approaches to species interactions, which tended to reference these vaguely-defined “niche differences”, Chesson proposed that species interactions depended on both fitness differences (differences in absolute growth rates after niche differences are controlled for) and niche differences (ecological differences between species which cause intraspecific competition to exceed interspecific competition). He also suggested rigorous methods to quantify these concepts. This framework has been applied both to the obvious questions of species coexistence and diversity maintenance, as well as predator-prey relationships (2008) and the phylogenetic structure of communities (2010).

In a recent paper, Ian Carroll et al. apply this framework to the search for the mechanisms behind biodiversity and ecosystem functioning. They point out that the questions in studies of ecosystem functioning are directly analogous to Chesson’s concepts – selection effects result from fitness or competitive differences between species, while complementarity relates to the partitioning of resources, or niche differences between species. The added benefit is that Chesson has provided clear definitions for these concepts.

While this may not be world-altering, it’s encouraging. Anytime different areas of ecology intersect, both benefit. Of course there are difficulties – no doubt the question of how to measure niche differences and fitness differences will be contentious (as attempts to translate ecological theory into ecological methodology often are) - but the possibility that a few general ecological concepts explain diverse observations is worth pursuing.

Enhanced biodiversity-ecosystem function relationships in polluted systems

*note: this text was adapted from an Editor's Choice I wrote for the Journal of Applied Ecology.

In this era of species loss and habitat degradation, understanding the link between biodiversity and functioning of species assemblages is a critically important area of research. Two decades of research has shown that communities with more species or functional types results in higher levels of ecosystem functioning, such as nutrient processing rates, carbon sequestration and productivity, among others. This research has typically used controlled experiments that standardize environmental influences and manipulate species diversity. However, a number of people have hypothesized that biodiversity may be even more important for the maintenance of ecosystem functioning during times of environmental stress or change rather than under stable, controlled conditions. It is during these times of environmental change that preserving ecological function is most important, as changes in function can have cascading effects on other trophic levels, compounding environmental stress. Therefore, explicitly testing how biodiversity affects function under environmental stress can help to inform management decisions.

Image from Wikimedia commons

In a recent paper in the Journal of Applied Ecology, Li and colleagues examine how algal biodiversity influences productivity in microcosms with differing cadmium concentrations. Cadmium (Cd) is a heavy metal used in a number of products and industrial processes, but it is toxic and Cd pollution is a concern for human populations and biological systems, especially aquatic communities. This is especially true in nations currently undergoing massive industrial expansion. In response to concerns about Cd pollution effects on aquatic productivity, Li et al. used algal assemblages from single species monocultures to eight species polycultures grown under a Cd-free control and two concentrations of Cd, and measured algal biomass.

Their results revealed that there was only a weak biodiversity-biomass relationship in the Cd-free teatment, which the authors ascribed to negative interactions offsetting positive niche partitioning. In particular, those species that were most productive in their monocultures were the most suppressed in polycultures. However, in microcosms with Cd present there were positive relationships between diversity and biomass. They attribute this to a reduction in the strength of competitive interactions and the opportunity for highly productive species to persist in the communities.

While a plethora of experiments generally find increased ecosystem function with greater diversity, Li et al.’s research indicates that the effect of biodiversity on function may be even more important in polluted systems. If this result can be duplicated in other systems, then this gives added pressure for management strategies to maintain maximal diversity as insurance against an uncertain future.

Li, J., Duan, H., Li, S., Kuang, J., Zeng, Y., & Shu, W. (2010). Cadmium pollution triggers a positive biodiversity-productivity relationship: evidence from a laboratory microcosm experiment Journal of Applied Ecology, 47 (4), 890-898 DOI: 10.1111/j.1365-2664.2010.01818.x

Happy Year of Biodiversity

It’s ironic that during the International Year of Biodiversity, the US is experiencing an environmental disaster on a massive scale. Unfortunately, this disaster is just another failure in environmental protection, part of a long series of failures which seem to characterize this Year of Biodiversity. Even as the political will behind the 2010 biodiversity targets seems to have waned (and most indicators suggest that declines in diversity are unchecked), evidence continues to mount for the functional value of biological diversity.

This week’s issue of Nature features a couple of pieces focusing on biodiversity through a political or economic lens. Although the economic benefits and services provided by species-level diversity has been well illustrated, in “Population diversity and the portfolio effect in an exploited species”, Schindler et al. (Nature, 465, 609-612) new evidence that at even finer divisions than the species, diversity plays an important role. In this case, they find that genetic diversity at the population level is an additional and significant contributor to ecosystem stability. Schindler et al. examine the effects of hundreds of locally-adapted populations of sockeye salmon on the valuable salmon fishery in the Bristol Bay area of Alaska. They suggest that the portfolio effect (or the robustness of biodiversity to variable conditions – like a diverse financial portfolio) can function at the population level as well as the species level. High levels of intra-specific diversity can produce temporal variation among populations in response to environmental variability, resulting in catches that are more stable year-to-year, and making fishery closures less likely, a clear economic benefit.

Populations are declining at an even faster rate than species themselves: the more we understand the importance of conserving diversity at multiple biological scales (ecosystem, species, population, even the individual?), the more complicated and onerous the task of conserving diversity becomes.

In the same issue of Nature is an editorial on the possibility of an IPCC-like panel for biodiversity. At this very moment (give or take a few time zones), government representatives from all over the world are deciding whether or not to create this panel. So far, they have a catchy name for it, the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES), which hopefully hasn’t been written in stone. But they also have a strong recognition of the inextricable links between biodiversity, ecosystem services and human wellbeing – links that are highlighted in the Schindler et al. article. Furthermore, an explicit goal of IPBES is to address the currently tangled state of biodiversity organizations, conventions and programs by forming a unified front of sound biodiversity policy and science. The Convention on Biological Diversity had set a target of halting biodiversity loss by 2010 and we have failed spectacularly. Is IPBES the solution?

Wanted: an IPCC for biodiversity. Nature, 465, 525-525

Schindler, D.E., Hilborn, R., Chasco, B., Boatright, C.P., Quinn, T.P., Rogers, L.A. & Webster, M.S. Population diversity and the portfolio effect in an exploited species. Nature, 465, 609-612

By Nick Mirotchnick and Caroline Tucker

Don’t miss the mechanism when testing for biodiversity effects

Variation in the strength of diversity effects among experimental studies raise the question when and where consequences of diversity loss is strongest. As in grassland experiments, diversity effects on plant biomass production can be observed in systems with marine macroalgae. However, even among marine macroalgae experiments variation in the strength of the diversity effect cannot be explained because of largely differing experimental set-ups (i.e. long-termed vs. short-termed studies, mesocosms vs. field experiments, using inter- or subtidal habitats). From literature Stachowicz et al. assumed that short termed factors regulating diversity effects in such systems could be attributed to spatial complementarity in photosynthesis rates or different limiting nutrients. Long-term regulating factors could be attributed to habitat differentiation, temporal complementarity, fascilitation, recruitment and natural heterogeneity of substrate. In a very elegant way Stachowicz and his co-workers tested whether mechanisms responsible for diversity effects change with experimental procedure and/or study type within the same marine algae system. In a series of three experiments, that is a short-termed mesocosm with transplanted thalli, a short-termed (two month) field-experiment with naturally recruited thalli and heterogeneous substrate, and in a long-term (three years) field-experiment, the authors were able to show that strong diversity effects are positively correlated with experimental duration, environmental heterogeneity and population responses (recruitment). Whereas in the mesocosm species identity affected biomass production, in the field studies it was species richness but not identity. Fractional change of species biomass could be explained by species identity in the mesocosm, and by both identity and richness in the field. The authors are making an important point by showing that mechanisms for diversity effects are not exclusive but occur together and become stronger over time. They conclude that the absence or the detection of only weak diversity effects in short-termed experiments does not necessarily mean that there is no effect because such approaches detect only a limited number of potential mechanisms.


John J. Stachowicz, Rebecca J. Best, Matthew E. S. Bracken, Michael H. Graham (2008). Complementarity in marine biodiversity manipulations: Reconciling divergent evidence from field and mesocosm experiments. Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.0806425105