Invasions Biologiques aux Antipodes Subpolaires des Hémisphères Nord et Sud

Dans la communauté scientifique, l’étage montagnard alpin et les zones froides subpolaires sont considérées comme moins affectées par les espèces exotiques envahissantes. Toutefois, cela pourrait changer brusquement sous les scénarios de changements climatiques futurs (cf. réchauffement) et l’augmentation des activités humaines (cf. activités de récréation) dans ces écosystèmes jugés plus difficile d’accès.

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Vue sur les montagnes d’Abisko au Nord de la Suède (Crédit photo : Ive Van Krunkelsven)

Au cours de ces trois dernières années, j’ai eu la chance de pouvoir travailler aux côtés d’Ann Milbau, d’Anibal Pauchard, de Martín Nuñez et de Jonas Lembrechts sur un projet de recherche financé par la Suède (voir page 20 de ce document rédigé en suédois) et dont l’objectif était précisément de s’intéresser aux principaux déterminants du succès d’invasion des plantes exotiques envahissantes dans ces écosystèmes froids et extrêmes situés à haute latitude et à haute altitude. Suite à de multiples réunions de travail en Suède, en Argentine et en France associées à de nombreux échanges par email pour mettre au point le protocole, discuter des analyses et des résultats, échanger nos points de vues vis-à-vis des hypothèses préalablement posées, rédiger un article scientifique, et enfin répondre aux commentaires et critiques aiguisées de nos pairs, ces travaux ont été récemment publiés dans la revue Proceeding of the National Academy of Science (PNAS, USA).

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Jonas Lembrechts récolte les précieuses données (Crédit photo : Ive Van Krunkelsven)

Le résultat est clair, les perturbations d’origine anthropique telles que les sentiers empruntés par les randonneurs en été et les skieurs en hiver sont la clé pour assurer le transport, la germination, la croissance, la floraison et donc l’installation des plantes exotiques envahissantes dans ces territoires reculés et encore immaculés en matière d’invasions biologiques. En l’absence de telles perturbations, ni l’augmentation des températures liée au réchauffement planétaire, ni l’apport d’azote lié à la pollution atmosphérique, ni la pression de propagules exercée par les randonneurs qui transportent les graines sous les semelles de leurs chaussures ne permettent un succès suffisant pour l’installation de ces plantes exotiques envahissantes.

ezgif-com-gif-makerPour arriver à ce résultat, un dispositif expérimental unique en son genre a été mis en place le long de plusieurs gradients d’altitudes situés dans des massifs montagneux à l’extrême nord de la Scandinavie, à Abisko en Suède, et à l’extrême sud de la Pantagonie, à Punta Arena au Chili, couvrant ainsi les antipodes subpolaires des hémisphères Nord et Sud. Au sein de ce dispositif, nous avons fait varier plusieurs facteurs, en plus de la température via l’altitude, comme la présence ou non d’une perturbation (cf. retrait de la végétation native : D+ vs. D-), l’apport ou non de nutriments azotés (cf. engrais : N+ vs. N-) ainsi que l’intensité de la pression de propagules (cf. nombre de graines : P+ vs. P-) de 6 plantes exotiques envahissantes. Chaque placette a été subdivisée en 48 unités, soit 6 répétitions (1 par espèce) pour chacune des 8 combinaisons des facteurs D, N et P (D+/N+/P+, D+/N+/P-, D+/N-/P+; D-/N+/P+, D-/N-/P+, D+/N-/P-, D-/N+/P-, D-/P-/N-).

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Vue sur l’une des nombreuses placettes du dispositif (Crédit photo : Ive Van Krunkelsven)

La conclusion principale issue de ces travaux est qu’il est primordial de limiter et confiner au maximum le niveau des perturbations d’origine anthropique, au risque de voir la végétation de ces écosystèmes complètement modifiée par l’installation et la propagation d’espèces exotiques envahissantes. Le risque est d’autant plus important que l’effet des activités humaines sera combiné au réchauffement climatique actuel et futur. Il semble donc impératif de mettre en œuvre rapidement des stratégies de gestion de ces écosystèmes en limitant les perturbations humaines à hautes latitudes et altitudes, pour limiter le risque d’invasions par les plantes exotiques envahissantes.

Pour une version en anglais, rédigée et illustrée par le premier auteur de l’étude, Jonas Lembrechts, c’est ici. Vous trouverez également un communiqué de presse sur le site l’Université de Picardie Jules Verne (UPJV) ainsi que sur le site echosciences des Hauts-de-France.

The Climatic Debt Explained

I guess some of you may wonder: what the hell is the climatic debt? Well, in ecology, this term is used to refer to communities of living organisms being in a state of disequilibrium with climate (cf. the equilibrium between community composition and climatic conditions has been disrupted). This is best illustrated by time-lagged response of living organisms to climate change. The inertia of long-lived organisms such as trees or perennial plants after a climate-forcing event makes forest ecosystems particularly prone to the climatic debt.

In a recent paper led by Romain Bertrand, we found that the magnitude of the disequilibrium with climate, aka climatic debt, in understory plant communities across the French forests (see map) increases with the severity of baseline temperature conditions, the exposure to climate warming and species thermal tolerance.

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I’m really proud to write these few lines, not only because this is an important result (sorry I might be biased here) but mostly because it is always inspiring, rewarding and cool to work with a good buddy on a fun topic. Romain and I discussed this idea of “explaining the climatic debt” a very long time ago. It all started in 2011, few days after Romain’s original work on the assessment of the climatic debt in french forests’ understory plant communities was published. Well, we were not smart enough to use the fancy “climatic debt” at that time but reported it as “biotic responses lagging behind climate change” instead. Anyway, the thing is that we received a thorough (and inspiring) commentary from Pieter De Frenne and his colleagues arguing that the climatic debt we found in understory plant communities of temperate deciduous forests could be the result of changes in forest management practices. The reasoning behind this argument being that the abandonment of coppicing (a traditional sylvicultural practice in Europe: see picture below) and the subsequent natural succession towards mature close forests may provide microclimatic conditions that buffer understory plant communities against macroclimate warming. This is indeed a very important hypothesis and you can learn more on the potential importance of microclimate as a moderator of plant responses to macroclimate warming by reading the excellent paper written by Pieter De Frenne and his team. Although neither their commentary nor our reply was published, this was a fruitful discussion that has generated new and exiting findings.

The seminal analyses that we provided five years ago in our reply to the commentary just involved the respective impacts of macroclimate warming and changes in understory light conditions on the magnitude of the climatic debt and demonstrated that changes in understory light conditions had a minor impact on the climatic debt, as it is also the case in the now published paper. It would have been a shame to stop there given the efforts made to provide a convincing reply (we might have been too much convincing on this). So, we elaborated a list of the potential drivers involved in the climatic debt that we observed in understory forest plant communities. In that respect, Romain went far beyond our initial list and provided a very comprehensive (23 explanatory variables) analysis of the potential determinants of the climatic debt not only involving environmental (i.e. baseline conditions and exposure to environmental changes) and anthropogenic (e.g. sylvicultural practices, land-use changes, habitat fragmentation) constraints but also plant traits and characteristics involved in persistence (e.g. species’ life span and thermal tolerance) and migration (e.g. species’ dispersal limitation) mechanisms.

Although we expected climate-change exposure to be an important determinant (plants are more likely to lag behind climate change in locations where the magnitude of the change is the highest), we were very surprised to find that both baseline temperature conditions and species’ intrinsic ability to tolerate water and thermal stresses outweigh the impact of climate-change exposure. Warmer baseline conditions (cf. lowland forests at low latitudes) contribute to a high climatic debt and yet these ecosystems are usually given less priority than cold ecosystems (e.g. mountains) in conservation biology. Similarly, species’ persistence mechanisms as a response to climate change have been neglected so far due to the strong emphasis on migration mechanisms involved in climate-driven range shifts that are particularly pronounced along the elevation gradient where short distances between isotherms allow plants to move upslope. And yet, both lowland ecosystems and persistence mechanisms are very important to consider, especially so for forest plant which dispersal abilities are very limited. Consequently and importantly, persistence mechanisms outweigh migration mechanisms in explaining the climatic debt in forest ecosystems. We also note that lowland ecosystems and warm climates in general are richer in stress-tolerant plants, which could be a reason why warmer climates are more likely to harbour plant communities lagging behind climate change.

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Carpet of flowering bluebells (Hyacinthoides non-scripts) in a coppice dominated by beech (Fagus slvatica) and hornbeam (Carpinus betulus) (Vadencourt Wood, 80560 Contay, France). Due to its wide climatic-niche breadth and its affinity for moist and buffered microhabitats, bluebells likely contribute to increase the climatic debt in the understory (Photo: J. Lenoir).

Unfortunately, plants can only tolerate a limited amount of change in temperature conditions and future climate change projections suggest temperature increases that may go far beyond the thermal tolerance of plants, thus initiating local extirpation events with potential cascading effects for living organisms relying on these habitat-forming species.

Evidence Against MacArthur’s Latitude–Niche Breadth Hypothesis

According to Robert MacArthur, the realized niche breadth of species is positively associated with latitude (cf. MacArthur’s latitude-niche breadth hypothesis), namely niches in highly diverse tropical regions near the equator are narrower than in less diverse boreal and polar regions (MacArthur, 1972). If you want to know more on this hypothesis, I highly recommend to read the paper from Vázquez & Stevens (2004) who deeply discuss the concept behind this hypothesis and made a thorough meta-analysis of the evidence for or against the latitude-niche breadth hypothesis, concluding that the null hypothesis (i.e, that there is no correlation between latitude and niche width) cannot be rejected. According to Klaus Rohde (see his post on MacArthur’s latitude-niche breadth hypothesis), a priori assumptions of this hypothesis are flawed: “The latitude-niche breadth hypothesis makes equilibrium assumptions, implicitly and explicitly assuming that niche space is more or less saturated with species. However, there is much evidence for an overabundance of vacant niches and that most ecological including tropical systems are far from saturation” (for a discussion and examples see Rohde 2005).

In a recent paper published by Safaa Wasof who will soon defend her PhD, we tested the niche conservatism hypothesis among distant populations of the same species and for a fairly large number (n = 888) of native European vascular plant species occurring in both the Alps (central Europe) and Fennoscandia (northern Europe). In addition to that, we also compared the realized niche breadth between populations from the Alps and populations from Fennoscandia, assuming that niche breadth would be wider for populations thriving in Fennoscandia than for those thriving in the Alps according to MacArthur’s latitude-niche breadth hypothesis. Well, we found the opposite pattern: populations from central Europe in the Alps have, on average, a wider climatic niche breadth than populations from northern Europe in Fennoscandia, thus contradicting MacArthur’s latitude-niche breadth hypothesis. Although we compared only two regions and did not cover the entire latitudinal gradient from the Tropics to the North Pole, our result is cristal clear.

If you want to know more about this result, you are very welcome to read Safaa’s paper (Wasof et al., 2015). However, this result was not the central message of Safaa’s paper which we twisted on the niche conservatism hypothesis and its relevance for species distribution models. Here I would like to focus more specifically on MacArthur’s latitude-niche breadth hypothesis and the result we found. This is also a nice opportunity for me to present a slightly different set of analyses that we ran together with Safaa but which did not get into the manuscript or the appendices (Safaa’s paper is just the tip of the iceberg).

So, instead of using growing degree days (GDD) and the aridity index (AI) solely to capture species realized climatic niche, like we did in Safaa’s paper, we here used a larger set of bioclimatic variables (8 out of the 19 bioclimatic variables from WorldClim: BIO2, BIO5, BIO6, BIO7, BIO8, BIO15, BIO18, BIO19) that we subsequently reduced to a bi-dimensionnal climatic space by using a Principal Component Analysis (PCA). We used the 1-km resolution bioclimatic grids that we each clipped to the two study regions (see Figure 1A for an example based on BIO5) before running the PCA (Figure 1B). The resulting first (PC1: Figures 1C and 1D) and second (PC2: Figures 1E and 1F) PCA axes captured 49% and 24%, respectively, of the total inertia. Note that Figures 1C, 1D, 1E and 1F are showing the spatial distribution of the PC1 and PC2 variables of the analog climatic space solely (cf. purple point cloud in Figure 1B).

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Figure 1: Study area and climatic space

Focusing on the analog climatic space solely to make climatic niches comparable between the two regions (cf. same reference), we used a set of 440 species, out of the 888 species belonging to the common species pool, for which we had enough data to compute the climatic niche breadth across both regions and along both PC1 and PC2 axes. Figure 2 shows an example of the realized climatic niche of Corydalis cava across the PC1-PC2 bi-dimensionnal climatic space for both the Alps (on the right) and Fennoscandia (on the left).

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Figure 2: Realized climatic niche of Corydalis cava across the PC1-PC2 bi-dimensionnal climatic space for both the Alps (in red) and Fennoscandia (in blue).

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Corydalis cava (Source: Wikimedia Commons).

Niche breadth along both PC1 and PC2 was computed as the 95% confidence interval around the optimum value (cf. maximum density position). Figure 3 shows the result for all 440 studied species along PC1 (Figure 3A) and PC2 (Figure 3B). I guess statistical tests are useless here given the strength of the signal. For most European vascular plant species, populations from the Alps have wider realized climatic niche along both PC1 and PC2 than populations from Fennoscandia.

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Figure 3: Realized climatic niche breadth for 440 vascular plant species occurring in both the Alps and Fennoscandia

This trend towards wider niches in the Alps than in Fennoscandia (Figure 3) invalidates MacArthur’s latitude–niche breadth hypothesis. In Safaa’s paper we discuss several potential drivers behind this result. My favorite one implies greater genetic diversity due to a diversity of refugia close to the Alps (Schönswetter et al., 2005), corresponding to greater habitat heterogeneity, thus increasing the likelihood for a species to widen its fundamental climatic niche in the Alps.

References

MacArthur (1972) Geographical ecology. Princeton University Press, Princeton

Rohde (2005) Nonequilibrium ecology. Cambridge University Press, Cambridge

Schönswetter et al. (2005) Molecular evidence for glacial refugia of mountain plants in the European Alps. Molecular Ecology, 14: 3547–3555.

Vázquez & Stevens (2004) The Latitudinal Gradient in Niche Breadth: Concepts and Evidence. The American naturalist, 164: E1–E19

Wasof et al. (2015) Disjunct populations of European vascular plant species keep the same climatic niches, Global Ecology and Biogeography, 24: 1401-1412