Gaps in border controls are related to quarantine alien insect invasions in Europe

Abstract

Alien insects are increasingly being dispersed around the world through international trade, causing a multitude of negative environmental impacts and billions of dollars in economic losses annually. Border controls form the last line of defense against invasions, whereby inspectors aim to intercept and stop consignments that are contaminated with harmful alien insects. In Europe, member states depend on one another to prevent insect introductions by operating a first point of entry rule--controlling goods only when they initially enter the continent. However, ensuring consistency between border control points is difficult because there exists no optimal inspection strategy. For the first time, we developed a method to quantify the volume of agricultural trade that should be inspected for quarantine insects at border control points in Europe, based on global agricultural trade of over 100 million distinct origin-commodity-species-destination pathways. This metric was then used to evaluate the performance of existing border controls, as measured by border interception results in Europe between 2003 and 2007. Alarmingly, we found significant gaps between the trade pathways that should be inspected and actual number of interceptions. Moreover, many of the most likely introduction pathways yielded none or very few insect interceptions, because regular interceptions are only made on only a narrow range of pathways. European countries with gaps in border controls have been invaded by higher numbers of quarantine alien insect species, indicating the importance of proper inspections to prevent insect invasions. Equipped with an optimal inspection strategy based on the underlying risks of trade, authorities globally will be able to implement more effective and consistent border controls.

Figure 1. Insect dispersal through agricultural trade.

We defined the Trade Volume to be inspected (TV) to importing European country d when importing commodity c from origin country o, as the value of trade in commodity c (in US$), if both insect species i exists in origin country o and commodity c is a host. Therefore, if either insect i does not exist in origin o, or commodity c is not a potential host, then the TV of that o-c-i-d trade is equal to zero. Thus TV is only positive on pathways that could potentially move quarantine insects through trade, and should be interpreted as a measure of the likelihood of alien insects moving through trade. We calculated the Trade Volume to be inspected Per Interception (TVPI) as the TV divided by the number of interceptions made per origin o, commodity c, insect species i, or European destination d. Other factors which affect the likelihood of insect dispersal, such as pre-export controls, were not included in this study since all exporters must fulfill the International Plant protection Convention (IPPC) standards and regulation. TVPI and TV do not measure other factors that determine establishment success, such as climate, host-plant availability and ecological processes.

Figure 2. Trade volume and the number of interceptions.

The relationship between the Trade Volume to be inspected (TV) and the number of alien insect interceptions at Europe’s borders on agricultural imports (2003–2007), by A) country of origin (r = 0.02, n = 146, p = 0.810), B) commodity type (r = −0.01, n = 126, p = 0.910), C) alien insect species (r = 0.23, n = 116, p = 0.013) and D) European importing countries (positive correlation, r = 0.73, n = 28, p = 0.00001). Only the top 25 data points by TV and number of interceptions are displayed. Notes: B) ⁺see Table S5 for full FAO commodity names. C) 1 =  Cacoecimorpha pronubana, 2 = Pheletes californicus, 3 = Tetranychus evansi, 4 = Spodoptera eridania, 5 = Frankliniella occidentalis, 6 = Unaspis citri, 7 = Opogona sacchari, 8 = Rhynchophorus palmarum, 9 = Metamasius hemipterus, 10 = Liriomyza trifolii, 11 = Anastrepha fraterculus, 12 = Maconellicoccus hirsutus, 13 = Aleurocanthus woglumi (see Table S3 for taxonomy). D) 1 = Luxembourg, 2 = Latvia, 3 = Estonia, 4 = Slovakia, 5 = Malta, 6 = Cyprus, 7 = Lithuania, 8 = Hungary, 9 = Slovenia, 10 = Bulgaria, 11 = Austria, 12 = Finland, 13 = Romania, 14 = Poland.

Figure 3. European country import volumes and interceptions.

Heat maps showing A) Trade Volume to be inspected (TV), B) the number of border insect interceptions (+1) and C) the Trade Volume to be inspected Per Interception (TVPI) in Europe. In each map, log values were used and split linearly into a 5 point scale, with 1 representing the smallest 20% of the log value range, through to 5 which represents the highest 20% of the log value range. In all maps, white countries scaled 0, were not included in this study.

Figure 4. Border controls and the level of invasion.

Trade Volume to be inspected Per Interception (TVPI) and the level of invasion in Europe. We found a positive correlation between the TVPI (2003–2007) and the number of quarantine insects that have established per European country (r = 0.54, n = 28, p = 0.003). The effect of TVPI on invasion is still significant (p = 0.0398) if we include climatic factors such as capital city latitude (p = 0.00002), country area (p = 0.0504) and altitudinal range (p = 0.0027) as proxies of climatic range for each reporting country (generalised linear model with Poisson errors) (Fig. S1).