Corresponding author: René Eschen (
Academic editor: W. Rabitsch
The trade in plants for planting is a major pathway for the introduction and further spread of alien plants, pests and diseases. Information about the structure of plant trade networks is not generally available, but it is valuable for better assessing the potential risks associated with the trade in live plants and the development of prevention and mitigation measures and policy. The discovery of two larvae of
Eschen R, Grégoire, JC, Hengeveld GM, de Hoop MB, Rigaux L, Potting RPJ (2015) Trade patterns of the tree nursery industry in Europe and changes following findings of citrus longhorn beetle,
The international trade in plants for planting is a major pathway for the introduction of alien tree pests and diseases (
During the first decade of the twentieth century, Japanese maple (
Greater focus on CLB by European authorities following a small outbreak of CLB in the Westland area in the Netherlands in 2007 (
Another discovery of CLB took place in December 2009 in the Boskoop area in the Netherlands (
Until this event it was presumed that CLB could not establish in the Netherlands,
Using this database, this paper describes the trade in woody plants for planting through the Netherlands with particular focus on CLB and
Data about the import of all
The best available data about the movement of pests into the EU come from pest interceptions during phytosanitary import inspections at the port of entry and findings away from the point of entry. Interceptions of pests regulated in Annex Ia and IIa of Council Directive 2000/29/EC (
Data about all transactions by producers and traders in the Boskoop area for a two-year period (July 2008–June 2010) were digitised and included the identity (genus and species), number, origin and destination of all shipped plants. Only the transactions for 138 producers in 2009, the year with the largest number of records, were analysed, because of the incompleteness of the records for 2008 and 2010 in the database. In some instances the same plants have been traded within the Boskoop area itself and later to customers outside the Boskoop area. Therefore the total number of plants is lower than recorded in the database, but it is impossible to identify plants that were traded multiple times.
In order to minimize the possibility that individual recipients could be identified and to facilitate working with the large number of recipients, as well as graphical representation of the data, the post codes of the recipients were assigned to the corresponding Nomenclature of Units for Territorial Statistics (NUTS) regions. NUTS regions were established by Eurostat and correspond to administrative regions of EU, acceding EU, candidate EU, as well as European Free Trade Association (EFTA), countries at three hierarchical levels. The lowest level (3) was used in this study as it provides high resolution, although it does not correspond to the same administrative level or average surface area in all countries. For example, NUTS 3 corresponds to “départements” in France, and to the usually much smaller “Kreise” in Germany. Plants of all genera combined were shipped to 800 of the 1,453 NUTS 3 regions, but
The recipients of
The relationships between producers and the destinations of shipped
The relative abundance of eighteen tree genera, that included the most common European tree species, and two miscellaneous groups with the remaining conifer and broadleaved species were taken from
The distribution of the
During the period 1998–2012, the total number of
The number of imported
In 1999–2002 the main source of
From 2000 to 2012 CLB was intercepted by EU member states on 24 occasions, mainly on imported planting material from China (Fig.
Interceptions of
From 2006 to 2010, 190 consignments, containing a total of 3,971,805
In 2009, 2,738,974
Thirty-six of the Boskoop producers shipped
Plants were delivered to 27 countries (Fig.
The number of
Recipients of
Twenty-one producers sold
Trade flow of
In order to better understand and manage invasions by tree pests through the trade in plants for planting, analysis of trade networks is urgently needed, but detailed data on this trade are rarely available (
Phytosanitary import inspections are aimed at confirming compliance with prescribed phytosanitary measures in the exporting country, not at quantifying pest abundance. Hence, notifications cannot usually be interpreted as a quantitative measure of pest infestation rate, but in this case it has been possible to directly relate import volume to inspection frequency and infestation rates in Europe, based on data collected through the destructive sampling of thousands of plants in these consignments as stipulated in the EU emergency measures, which is a more reliable detection method than the standard visual inspections. One in twenty imported consignments of
The vast majority (99%) of the
A study of the nursery trade for landscapers and retailers in the US indicated that the dominant characteristic of buyer preference was plant quality (
The majority of
Regions with many or large nurseries or retail distribution centres may act as highly connected nodes in the European plants-for-planting trade network, with only few trading steps between the point of import into Europe and the consumer (
It can be argued that consignments that are split up as the plants are distributed throughout Europe are difficult to regulate or control in terms of quality and plant health. High risk locations are nurseries that grow vast amounts of host plants imported from areas where CLB is present, of which there were not many in Boskoop. The imported plants may stay for several months to several years at a nursery for root setting before they are ready for sale. In particular in these high-risk nurseries, more than one beetle may emerge from infested plants, mating may occur and mated females can oviposit on other host plants in or outside the nursery. There are several reports where this has taken place. In France, several beetles were found in a nursery and in Guernsey 10 adults were caught in one greenhouse. At two locations in the Netherlands, infested outdoor trees were found in the neighbourhood of nurseries growing vast amounts of
Once large consignments are imported, they are either directly marketed via wholesale companies or become increasingly fragmented and it is difficult to trace plants to their true origin. The lack of traceability makes the management of an outbreak more difficult as it takes more time and effort to discover the origin of the plants and the destination of other plants from the same consignment or producer. The experience with data collection following the outbreaks in the Boskoop area revealed that a large number of producers only kept paper records of plant movements, which had to be entered into an electronic database when other Member States demanded that the Netherlands provide these in the aftermath of the Boskoop incident. The absence of readily available transaction records may cause delays in the tracing and management of outbreaks outside tree producing areas. Hence, it is essential that electronic records of transactions are kept, possibly in centralised databases, in order to access such data when required by NPPOs for the purpose of
Raising awareness and quality levels to reduce the risk of CLB establishment may best be attained by focussing on checks for larger consignments, that is, before they become fragmented (
It is clear from our data on trade in
This research has received funding from the European Union Seventh Framework Programme FP7 2007-2013 (KBBE 2009-3) under grant agreement 245268 ISEFOR. RE was financially supported through a grant from the Swiss Secretariat for Science, Education and Research to join the EU COST Action PERMIT. We thank Roelof Blanken and Erik van Ede (Dutch NPPO) for help in making the raw data accessible. Marc Kenis, Antoon Loomans, Dirk Jan van der Gaag, Marco Pautasso and two referees made constructive comments on an earlier version of the manuscript. Thanks to Alicia Leroux for editing our English.
Table S1
Data type: measurement
Explanation note: Summary of dynamics of the import of
Table S2
Data type: measurement
Explanation note: Summary of the intra-European trade in