Marco Pautasso‎ > ‎

Networks, plant health and biodiversity

Marco Pautasso - January 2015

postdoc, EFSA, Parma, Italy


My research interests can be divided in three interrelated areas: (1) network epidemiology, (2) landscape pathology and (3) conservation biogeography. Please see Pautasso (2013, CAB Reviews) for an overview of the links between these three research fields. I am also interested in scientometrics.

Network epidemiology

  • network structure and epidemics
  • Phytophthora ramorum (Sudden Oak Death)
  • disease spread in small-size directed networks

Landscape pathology

  • global change and plant health
  • tree disease incidence as a function of environmental variables
  • geographical genetics of forest trees

Conservation Biogeography

  • seed exchange networks and agrobiodiversity conservation
  • scale-dependence of the biodiversity - human population correlation
  • biogeography of the living collections of botanic gardens


  • meta-analysis
  • peer review
  • file-drawer problem

1. Network epidemiology

Networks are ubiquitous in nature, technology and society. They are sets of nodes connected by links and can be fruitful models in many biological applications (Moslonka-Lefebvre et al. 2011, Phytopathology; Fig. 1). Plant ecology and health will be affected not only by climate change, but also e.g. by increases in trade among countries due to globalization (Pautasso et al. 2010, Biological Reviews). A network approach is a new tool to understand the effects of global change on biodiversity, epidemics and ecosystem services (Jeger et al. 2007, New Phytologist).

Fig. 1. Epidemiology is just one of the many applications of network theory (from Moslonka-Lefebvre et al. 2011, Phytopathology).

My interest in network epidemiology arises from two postdocs (2006-2010) with Mike Jeger (Imperial College London), where we modelled plant trade networks and the risk they pose as dispersal pathways for plant pathogens such as Phytophthora ramorum (the oomycete causing Sudden Oak Death). We reviewed the growing literature on modelling disease spread and control in complex networks and its implications for plant sciences (Jeger et al. 2007, New Phytologist) thereby showing that:

•    much research on epidemics in complex networks has been carried out for large-size (thousands of nodes or more) networks, but there is a question of whether findings from such studies also apply to small-size (hundreds of nodes) networks, which are relevant to many biological applications (including regional plant trade networks);

•    most models of epidemics in networks assume undirected connections, whereas for the plant trade the presence of a link between a plant nursery and a retail trader may not necessarily entail the reverse connection;

•    the vast majority of epidemiological models assume that nodes are either susceptible or infected, but in the case of plant trade it is more realistic to consider a continuum between fully susceptible and fully infected nodes, as plant traders may have a varying proportion of infected plants.

Therefore, we studied disease spread and establishment in small-size, directed networks along a continuum between susceptible and infectious status (Moslonka-Lefebvre et al. 2012, Mathematical Biosciences). We showed with numerical simulations that:

•    the epidemic threshold (the boundary between no epidemic and an epidemic) is significantly lower for scale-free networks compared to local, random and small-world ones, even if the number of nodes is only one hundred (Pautasso & Jeger 2008, Ecological Complexity);

•    inspection policies have a key role in country-wide strategies to keep under control epidemics of emerging pathogens such as P. ramorum, as shown by spatially-explicit simulations integrating information about the distribution of the main hosts of the pathogen with realistic assumptions about the trade in plants (Harwood et al. 2009, Ecological Modelling);

•    the epidemic threshold is strongly negatively correlated to the correlation coefficient between links in and out of nodes, regardless of the network structure and of the connectance level (Moslonka-Lefebvre et al. 2009, J Theoretical Biology);

•    the higher the number of outgoing links from the starting node, the higher the epidemic final size at equilibrium. This correlation increases with connectance level for all the structures investigated and underlines the importance of targeted control towards nodes with more connections (Pautasso et al. 2010, Ecological Complexity);

•    changes in hierarchical categories (e.g. proportions of producers, wholesalers and retailers) of plant trade networks can influence the epidemic development, particularly in non-scale-free structures (local, random and small-world; Pautasso et al. 2010, J Appl Ecology).

After having surveyed the literature on the evolution of plant health regulation (which still needs to take on board insights from network theory, e.g. the importance of targeting super-connected nodes and long-distance connections; MacLeod et al. 2010, Food Security), we reviewed available material on structural changes of the horticultural industry in the various regions of the world and their potential implications for plant health (Dehnen-Schmutz et al. 2010, Scientia Horticulturae).

We also provided updates on

  • using networks in plant epidemiology from the molecular to the international level, with  recommendations for further research (e.g. merging models of epidemics in networks with assumptions about behavioural choices of stakeholders and economic trade-offs; Moslonka-Lefebvre et al. 2011, Phytopathology);

  • networks and plant disease management: concepts and applications (Shaw & Pautasso, 2014, Annual Review of Phytopathology);

  • network epidemiology and plant trade networks (Pautasso & Jeger, 2014, AoB Plants).

2. Landscape pathology

My interest in the landscape pathology of tree diseases (i.e. the analysis of regional outbreaks of tree fungal pathogens) stems from my degree in forest sciences at ETHZ (2002), where after graduating I was involved in a literature review on the susceptibility to fungal pathogens of forests differing in tree diversity (Pautasso et al. 2005, Ecological Studies). When surveying that literature, we realized that there was an increasing amount of studies on regional outbreaks of tree pathogens using tools of landscape ecology, which led to a review highlighting this new interdisciplinary field (Holdenrieder et al. 2004, Trends in Ecology & Evolution; Fig. 2.

Fig. 2. Conceptual model of relationships among host–pathogen systems and landscape structure (from Holdenrieder et al. 2004, Trends in Ecology & Evolution).

Later on, we studied the available data on the occurrence of P. ramorum in plant nurseries, garden centres, historic gardens and patches of woodlands in England and Wales (2003-2006). Spatio-temporal point pattern analysis suggests that the control measures have managed to reduce long-distance spread of the pathogen from nurseries to garden centres, but there is still the risk of local dispersal from infected premises into the semi-natural environment (Xu et al. 2009, Ecography).

A further study analysed data on the incidence of P. ramorum between 2002 and 2009 in counties in England and Wales as a function of environmental variables. While P. ramorum county incidence in nurseries and retail centres was positively related to county area and human population density, county incidence in gardens and the wild did not show such correlations, declined significantly towards the East and was positively correlated with disease incidence in the trade. The latter finding suggests a role of the trade in the dispersal of this pathogen in Britain (Chadfield & Pautasso 2012, Forest Pathology).

Regional outbreaks of exotic tree pathogens are likely to become more common in the future due to climate change and increased long-distance trade. We reviewed the burgeoning literature relevant to plant health and global change and drew some recommendations for landscape managers (Pautasso et al. 2010, Biological Reviews). This review was preceded by an overview of studies of the genetic diversity of tree species across their distributional range (Pautasso 2009, Perspectives in Plant Ecology, Evolution & Systematics). Drawing on the P. ramorum case study, we then worked with social scientists, economists and invasion biologists on the need for risk-management strategies to be based on a better understanding of how stakeholders perceive the risk posed by plant diseases in both managed and natural ecosystems (Mills et al. 2011, Philosophical Transactions of the Royal Society B ; Pautasso et al. 2012, CAB Reviews).

The widespread dieback of European common ash (Fraxinus excelsior) due to the ascomycete Hymenoscyphus pseudoalbidus (Gross et al. 2014, Molecular Plant Pathology) calls for interdisciplinary research and collaboration with the various stakeholders to try and reduce the loss of biodiversity due to ash mortality and human reactions to this epidemic (Pautasso et al. 2013, Biological Conservation).

Further publications relevant to this research interest include:

•    comparative reviews on zoosporic plant pathogens and Mediterannean forest pathogens (Jeger & Pautasso 2008; Garbelotto & Pautasso 2012, both in the European Journal of Plant Pathology);

•    a commentary on the importance of long-term data sets in the study of plant diseases under global change (Jeger & Pautasso 2008, New Phytologist);

•    an overview linking climate change, globalized trade and their impacts on dispersal and invasion of fungal plant pathogens (Jeger et al. 2011, book chapter);

•    a numerical study of the combined use of two biocontrol agents with different biocontrol mechanisms in controlling foliar pathogens, and a review of the literature on this topic (Xu et al. 2011, both in Phytopathology);

•    a conceptual paper on the meanings of ‘plant health’ from different philosophical perspectives (e.g. naturalism vs. normativism, bio- vs. anthropocentrism, reductionism vs. holism; Döring et al. 2012, Plant Pathology);

•    two scientific opinions of the Plant Health Panel at the European Food Safety Authority: a guidance on the environmental risk assessment of plant pests, and an assessment of the European pest risk analysis on P. ramorum (both published in the EFSA Journal, 2011);

•    a review paper on impacts of climate change on plant diseases (Pautasso et al. 2012, European Journal of Plant Pathology);

•    an overview providing a framework for dealing with exotic tree pathogens in a changing world (Pautasso 2013, CABI book chapter);

•    a case study of the effects of global change on forest ecosystems (the Insubric region) (Pautasso 2013, Annali di Botanica);

•    a compilation of the ecological effects of Douglas fir (Pseudotsuga menziesii) cultivation in Europe (Schmid et al. 2014, European Journal of Forest Research);

•    an update on the literature on forest health in a changing world (Pautasso et al. 2015, Microbial Ecology).

3. Conservation biogeography

My interest in conservation and biogeography developed during a PhD in macroecology with Kevin Gaston, Univ. of Sheffield (2002-2005). Using data collected from the literature (about 800 papers), we studied large-scale patterns and determinants of bird assemblage abundances, thereby testing mechanisms behind the latitudinal gradient in species richness (“larger resource pool” or “finer partitioning of the pool” hypotheses; Pautasso & Gaston 2005, Ecology Letters) and less than proportionate individuals-area relationships (Pautasso & Gaston 2006, Global Ecology & Biogeography). A sub-linear spatial scaling of abundances needs to be controlled for in large-scale studies of how global change drivers (e.g. urbanization; Pautasso et al. 2011, Global Ecology & Biogeography) affect biodiversity.

Research on conservation biogeography has then dealt with the scale-dependence of the correlation between human population and biodiversity (Pautasso 2007, Ecology Letters). This is a key issue for biodiversity conservation because high human population density often results in species loss (but also in reduced assemblage abundance, as we showed for birds in Florence; Chiari et al. 2010, Journal of Animal Ecology). These impacts are magnified if species-rich regions also tend to be densely populated (Marini et al. 2012, Global Ecology & Biogeography). We studied mechanisms potentially explaining positive regional species-people correlations:

•    a sampling artefact: more populated regions could simply be more thoroughly sampled. No evidence for this mechanism was found for vascular plants in US counties (Pautasso & McKinney 2007, Conservation Biology), but sampling bias was found to explain positive species-people correlations in Italy for carabid beetles (Barbosa et al. 2010, Animal Conservation), grasshoppers (Cantarello et al. 2010, Naturwissenschaften) and stream macro-invertebrates (Pecher et al. 2010, Basic & Applied Ecology);

•    habitat heterogeneity and/or energy availability: more populated regions may have higher habitat diversity or a climate more favourable to high species richness. Evidence for one or two of these mechanisms was found in European countries for ants (Schlick-Steiner et al. 2008, J of Biogeography), aphids (Pautasso & Powell 2009, Oecologia), grasshoppers (Steck & Pautasso, Acta Oecologica) and stream macro-invertebrates (Pautasso & Fontaneto 2008, Ecological Applications);

•    protection measures: in some special cases people may have protected biodiversity preferentially in densely populated areas, as suggested by a study of ancient trees in Italy (Pautasso & Chiarucci 2008, Annals of Botany). However, in general protected areas tend to be located far from urbanized landscapes and thus from areas with high overall species richness, as shown for birds in Italian regions (Pautasso & Dinetti 2009, Environmental Conservation).

Research has also dealt with geographical patterns in the species richness of the living collections of the world’s botanic gardens, which show positive species-area and species-age relationships, as commonly observed in nature, but also a positive latitudinal gradient, a likely consequence of socio-economic factors (Pautasso & Parmentier 2007, Botanica Helvetica; Golding et al. 2010, Annals of Botany; Parmentier & Pautasso 2010, Kew Bulletin; Fig. 3). Further papers relevant to this research interest are an analysis of global correlates of species richness in rotifers (Fontaneto et al. 2012, Ecography) and a review of observed impacts of climate change on birds in Europe (Pautasso 2012, Italian Journal of Zoology).

Fig. 3. World map of botanic gardens (territory size is proportional to number of gardens). From, accessed August 2008. Creative Commons License, copyright 2006 SASI Group (University of Sheffield, UK) and Mark Newman (University of Michigan, USA).

Publications resulting from the research project on seed exchange networks and agrobiodiversity conservation (NETSEED) at CNRS Montpellier include:

•    a meeting report on a conference held at Montpellier on ‘Genetic Resources in the Face of New Environmental, Economic and Social Challenges’; Pautasso 2012, Biology Letters);

•    a review paper on concepts, methods and challenges in the study of the role of seed exchange for agrobiodiversity conservation (Pautasso et al. 2013, Agronomy for Sustainable Development);

•    an update on the European framework on organic seed regulations (Döring et al. 2013, Organic Agriculture);

•    a case study on the correspondence between genetic structure and farmers’ taxonomy for dry-season sorghum in Cameroon (Soler et al. 2013, Plant Genetic Resources – Characterization and Utilization);

•    ten simple rules for writing a literature review (Pautasso 2013, PloS Computational Biology);

•    and a case study on modelling seed exchange networks for agrobiodiversity conservation (Pautasso, 2015, Agronomy for Sustainable Development).