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Tuesday 17 May 2016

Effectiveness of the International Phytosanitary Standard ISPM No. 15 on Reducing Wood Borer Infestation Rates in Wood Packaging Material Entering the United States

Effectiveness of the International Phytosanitary Standard ISPM No. 15 on Reducing Wood Borer Infestation Rates in Wood Packaging Material Entering the United States

Abstract

Numerous bark- and wood-infesting insects have been introduced to new countries by international trade where some have caused severe environmental and economic damage. Wood packaging material (WPM), such as pallets, is one of the high risk pathways for the introduction of wood pests. International recognition of this risk resulted in adoption of International Standards for Phytosanitary Measures No. 15 (ISPM15) in 2002, which provides treatment standards for WPM used in international trade. ISPM15 was originally developed by members of the International Plant Protection Convention to “practically eliminate” the risk of international transport of most bark and wood pests via WPM. The United States (US) implemented ISPM15 in three phases during 2005–2006. We compared pest interception rates of WPM inspected at US ports before and after US implementation of ISPM15 using the US Department of Agriculture AQIM (Agriculture Quarantine Inspection Monitoring) database. Analyses of records from 2003–2009 indicated that WPM infestation rates declined 36–52% following ISPM15 implementation, with results varying in statistical significance depending on the selected starting parameters. Power analyses of the AQIM data indicated there was at least a 95% chance of detecting a statistically significant reduction in infestation rates if they dropped by 90% post-ISPM15, but the probability fell as the impact of ISPM15 lessened. We discuss several factors that could have reduced the apparent impact of ISPM15 on lowering WPM infestation levels, and suggest ways that ISPM15 could be improved. The paucity of international interception data impeded our ability to conduct more thorough analyses of the impact of ISPM15, and demonstrates the need for well-planned sampling programs before and after implementation of major phytosanitary policies so that their effectiveness can be assessed. We also present summary data for bark- and wood-boring insects intercepted on WPM at US ports during 1984–2008.

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Citation: Haack RA, Britton KO, Brockerhoff EG, Cavey JF, Garrett LJ, Kimberley M, et al. (2014) Effectiveness of the International Phytosanitary Standard ISPM No. 15 on Reducing Wood Borer Infestation Rates in Wood Packaging Material Entering the United States. PLoS ONE 9(5): e96611. doi:10.1371/journal.pone.0096611
Editor: David L. Roberts, University of Kent, United Kingdom
Received: November 23, 2013; Accepted: April 9, 2014; Published: May 14, 2014
This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Funding: The Working Group “Effects of trade policy on management of non-native forest pests and pathogens” was supported by a grant from The Nature Conservancy to the National Center for Ecological Analysis and Synthesis, which is a Center funded by the National Science Foundation (Grant #EF-0553768), the University of California Santa Barbara, and the State of California. Partial funding was provided by the New Zealand Foundation for Research and Technology through contracts C02X0501 (Better Border Biosecurity) and C04X0302 (Forest Biosecurity and Protection) to the author EGB. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors declare that no competing interests exist; however, the three authors from New Zealand (EGB, MK, JT) state that they are employees of Crown Research Institutes (CRI) in New Zealand (NZ ), which are wholly owned by the NZ Government and are constituted as limited liability companies. CRI employment for EGB, MK, and JT does not alter the authors’ adherence to PLOS ONE policies on sharing data and materials.

Introduction

International trade has been responsible for the inadvertent introduction of many exotic (nonnative) insect pests and plant pathogens, of which several have become highly invasive and caused serious environmental and economic impacts to multiple habitats worldwide [1]–[7]. In recent years, introductions of several particularly damaging wood-infesting insects and pathogens in the United States (US) have focused public and regulatory attention on the pathways that transport these pests [8]–[12].
Wood-feeding insects are commonly associated with wood packaging material (WPM), which includes items such as pallets, crates, and dunnage (wood used to brace cargo). Packaging for overseas shipments is commonly constructed from wood because it is relatively inexpensive, generally abundant, renewable, and easily manufactured and repaired. Unfortunately, wood used to construct WPM can be infested with a wide variety of bark and wood pests and thereby serve as a pathway for pest movement. Wood-feeding insects can also be transported in logs, lumber, fuelwood, live plants, and various manufactured wood articles [12]–[16].

As international trade volumes soared in recent decades, many countries became concerned about repeated introductions of invasive forest insects and disease organisms, such as Asian longhorned beetle, Anoplophora glabripennis (Motschulsky) (Coleoptera: Cerambycidae), and pinewood nematode, Bursaphelenchus xylophilus (Steiner et Buhrer) Nickle (Nematoda: Aphelenchoididae), as well as the WPM pathway that often vectors these pests. In response, members of the International Plant Protection Convention (IPPC) developed and adopted International Standards for Phytosanitary Measures No. 15 (ISPM15) in 2002, which provided details on approved phytosanitary treatments for WPM used in international trade [17]. A core value of these international standards is the harmonization of national regulations, which facilitates trade. The original stated goal of ISPM15 in 2002 was to “practically eliminate the risk for most quarantine pests and significantly reduce the risk from a number of other pests” by means of either heat treatment or methyl bromide fumigation of WPM [17]. ISPM15 was slightly revised in 2006 [18], and in 2009 the IPPC adopted several important changes such as lengthening the fumigation exposure time, requiring WPM to be made from debarked wood, requiring debarking prior to fumigation, and specifying tolerance limits on the maximum allowable size for individual patches of residual bark [19].  In addition, the goal of ISPM15 was reworded in 2009 to read as follows “to reduce significantly the risk of introduction and spread of most quarantine pests” associated with WPM [19]. The next version of ISPM15 was published in 2011 but consisted simply of changes in text formatting [20]. The newest version of ISPM15 was approved in 2013 and formally adopted heat treatment using dielectric heating (e.g. microwave) along with the corresponding treatment code DH [21]. More than 78 countries (considering the European Union as 27 countries) have implemented ISPM 15 through October 2013. It is important to recognize that the ISPM15 standards can be applied to wood from any tree species, including tropical and boreal species, as well as softwoods (conifers) and hardwoods (angiosperms).

The United States implemented ISPM15 in three phases over a 10-month period from 16 September 2005 to 5 July 2006. On 16 September 2005 the United States implemented Phase 1, which consisted of officially informing importers and the appropriate National Plant Protection Organization of the exporting country if live pests were found in WPM or if the WPM was not marked in compliance with ISPM15. Phase 2 began on 1 February 2006 and required that all WPM entering the United States (except from Canada) meet ISPM15 treatment standards and be marked accordingly. As part of Phase 2, noncompliant shipments and WPM could be denied entry to the United States, or if feasible, the noncompliant WPM would be removed from the shipment and exported at the expense of the importer, and thereby allow the imported products to enter the United States. Phase 3 began on 5 July 2006 and continues to the present and requires that noncompliant WPM and the associated commodities be immediately exported, usually returning it to the country of origin [22].

The objective of the present paper was to compare pre- and post-ISPM15 infestation rates of WPM associated with imports entering the United States. In this paper, we use the term “infestation rate” to refer to the percentage of consignments with WPM in which live pests were found in WPM when the imported consignments were inspected on arrival at US ports. We expected that if the data from the pre- and post-ISPM15 surveys were comparable then we could estimate the effect that ISPM15 had on WPM infestation rates. Further, we anticipated that implementation of ISPM15 would substantially reduce the number and frequency of live pests in WPM because the supporting documents that accompanied the early drafts of ISPM15 indicated that the proposed treatments for WPM were highly effective against many wood-associated insects and fungal pathogens [23]–[24]. The use of interception data for this purpose seemed acceptable because interception records are among the few datasets available that provide insights into the identity and relative infestation rate of pests associated with traded commodities and WPM [8], [15], [25]. We were able to find one large US dataset with interception data that had been collected in a standardized manner both pre- and post-ISPM15, which upon analysis indicated a moderate decline in pest interceptions on WPM after ISPM15 implementation.
Documenting the actual level of effectiveness of an international policy such as ISPM15 and evaluating the suitability of existing data for such an analysis is important for at least three reasons. First, it is important for determining the level of phytosanitary risk still associated with WPM and whether further revisions to ISPM15 are needed, or if individual countries may wish to require additional measures based on a pest risk assessment. Second, it is essential for estimating and understanding the economic costs and benefits of the implemented policy. And, third, it provides insights into the types of data that should be collected in advance of future international standards. For example, the recent approval of ISPM 36 in 2012 [26], which deals with plants for planting, provided such an opportunity.

ISPM15 Standards

To fulfill the requirements of ISPM15, WPM used in international trade must be marked (stamped) in a specific way to indicate that the WPM was subjected to an approved phytosanitary treatment [21]. The official mark includes the IPPC logo, a 2-letter country code indicating in which country the wood was treated, a producer code to indicate the treatment provider, and a treatment code to specify the treatment used, such as HT for heat treatment or MB for methyl bromide fumigation [21]. Each version of ISPM15 has provided more details on how the wood treatments should be conducted, and even more details were added to the 2013 version [21]. After research showed that bark- and wood-infesting insects, both primary and secondary colonizers, could infest and develop in wood after treatment, especially when bark was present [27]–[28], a debarking requirement for WPM was added in 2009. The tolerance limits for residual bark specified that pieces of bark could remain on WPM after debarking if individually they were either less than 3 cm in width (regardless of their length) or if they were greater than 3 cm wide but less than 50 square centimeters in total surface area [19]–[21]. The debarking requirement was not yet in place during the period of time analyzed in the present study.

Pests Commonly Associated with WPM

The principal bark- and wood-boring insects of quarantine concern for the United States include insects in the beetle (Coleoptera) families Buprestidae, Cerambycidae, Curculionidae (including Platypodinae and Scolytinae); the woodwasp family Siricidae (Hymenoptera), and the moth (Lepidoptera) families Cossidae and Sesiidae. Elsewhere in the world there are many other wood pests of concern to specific countries, including species of powderpost beetles (Bostrichidae, including Lyctinae), wood-boring flies (Diptera), termites (Isoptera), as well as wood-decay fungi and nematodes [29]–[32]. It is important to note that many powderpost beetles and termites are secondary colonizers of treated wood, and therefore are rarely the target pests when ISPM15 treatments are applied to newly constructed WPM.

International Pest Interception Databases

Several countries maintain databases of plant pests that are intercepted at their ports of entry, including maritime ports, airports, and international border crossings. For example, long-term pest interception databases have been maintained by governments and plant protection organizations in Australia, Canada, Chile, Europe and North Africa (by the European and Mediterranean Plant Protection Organization, EPPO), Mexico, New Zealand, and the United States. Typically, inspectors target high-risk products or pathways, rather than conduct random surveys. In addition, interception records are usually included in a country’s database only when pests are found although there are exceptions (such as the AQIM database used in the present study).

Earlier Surveys for WPM-Associated Pests

A comprehensive review of the literature, involving online literature searches as well as direct contacts with several plant protection organizations worldwide, provided a limited number of estimates of WPM infestation rates from before implementation of ISPM15 [33]–[35] and after [28], [36] (Table 1). In general, the pre-ISPM15 surveys were expressed on a consignment basis, such as all WPM in a single shipping container. In contrast, the sampling units used in the two post-ISPM15 surveys were individual WPM items such as a single pallet or a single piece of dunnage. Therefore, the results of these pre- and post-ISPM15 surveys were not directly comparable. Nevertheless, in the pre-ISPM15 surveys, WPM infestation rates ranged from a high of 4.3% of containerized maritime consignments [33] to a low of 0.06% for air cargo consignments [35]. By contrast, in the two post-ISPM15 surveys that involved mostly maritime containerized cargo, infestation rates of individual WPM items ranged from 0.1% [28] to 0.5% [36] (Table 1).

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Table 1. Summary data for the incidence of live insects found in association with WPM during surveys of imported goods that were conducted before or after implementation of ISPM 15 in various countries.

We found only one publication, a master’s thesis [37], which compared interception data that had been collected in a similar manner both before and after implementation of ISPM15. In this study, the author summarized the insect interceptions on WPM that were associated with 10,870 consignments that arrived at the maritime port of San Antonio, Chile during the 18 months immediately before (7733 consignments) and 12 months immediately after (3137) implementation of ISPM15 in Chile. The interception data were expressed on a consignment basis, and included live bark- and wood-infesting insects that were intercepted in WPM. Overall, data from Sánchez-Salinas [37], indicated that the infestation rate of WPM entering Chile fell 47% after ISPM15 was implemented (Table 1).

USDA Pest Interception Databases


The US Department of Agriculture (USDA) Animal and Plant Health Inspection Service (APHIS) maintains two major databases for records of pest interceptions on imported goods at US ports: AQIM (Agriculture Quarantine Inspection Monitoring) and PestID (Pest Interception Database, which was formerly called Port Information Network or PIN). AQIM is a statistically based inspection program based on random sampling of imported shipments at selected US ports. AQIM was designed to monitor the approach rate of agricultural risks on different pathways, and consists of daily or weekly random sampling of international cargo, mail, vehicles, and passenger baggage [38]. WPM was first targeted for inspection in AQIM in 2003 and usually consisted of sampling two containers per week at each of more than 40 participating US ports. Sample selection occurs randomly among commodities known to have associated WPM using a statistically robust stratified sampling plan. Infestation data for WPM are recorded on a consignment basis based on the number of distinct consignments within each of the sampled shipping containers. For each pest interception in AQIM, information is recorded on all pests found to the lowest taxonomic level possible (usually family, genus or species), as well as on the type of cargo inspected, type of WPM present, compliance with ISPM15 marking, and the presence or absence of bark on the WPM. For WPM, all plant pests found are recorded in AQIM, including both bark- and wood-infesting insects as well as those that inadvertently contaminated or “hitchhiked” with the shipment. Negative data, where no pests are found, are also recorded by consignment in AQIM, which allows the calculation of infestation rates (contrary to other interception data where negative inspections are typically not documented).
PestID includes interceptions records of all classes of plant pests intercepted at over 300 ports of entry in the United States, including bark- and wood-infesting insects found in association with WPM. As of January 2014, there were more than 2.5 million interception records in PestID that were recorded since 1984 when what is now known as PestID started as a computerized database. PestID records include information on the identity of intercepted pests, the commodity involved and its country of origin, date and place of interception, and many other details associated with the shipment and inspection such as whether the intercepted pest was associated with WPM. Unlike AQIM, however, PestID does not include information on shipments where no pests were found, and the inspections are not random, but are targeted at specific products, pathways, or countries.
There are other challenges when attempting to interpret PestID data. For example, although APHIS issues inspection guidelines for certain commodities [39], much work prioritization is left to the discretion of experienced, local personnel at the individual ports. As a result, for some commodities and items like WPM, the percentage of arriving shipments inspected can vary over time and among ports. Inspectors may target shipments based on a perceived risk of infestation for certain commodities from particular countries of origin and shippers. Additionally, priority inspection targets vary among ports due to the profile of work to be performed. For example, port inspectors who must clear large volumes of perishable fruits, vegetables, or cut flowers will likely spend less effort inspecting WPM associated with machine parts or quarry products than inspectors at ports that do not receive many perishables. Other limitations on the utility of PestID include: 1) that the data cannot provide an estimate of the number of pests arriving because not all shipments are inspected and inspectors may stop looking at a particular consignment once the first quarantine pest is found, 2) data on many intercepted pests that were classified as “non-quarantine significant pest ” taxa (e.g., cosmopolitan species or species that were regarded to be of low risk) were not included in PestID until March 2009, and 3) variation over time in the numbers of inspectors and their focus likely affected the numbers and kinds of pests that were intercepted.

Although the sampling protocols used in PestID are not random, PestID data are still useful in identifying the most common types of pests arriving in the United States, their countries of origin, and the commodities and pathways they were most often associated with [13], [16], [40].We report various PestID summary statistics below.

Methods

AQIM Data Analyses

We analyzed AQIM records where WPM was recorded for a 6-year period from October 2003 through September 2009. This period was chosen because it begins when APHIS started inspecting WPM as part of the AQIM program and ended in 2009, which was the year when several changes were made to ISPM15 [19]. Therefore, the data analyzed during the post-ISPM15 period in the present paper were collected during a period with consistent regulations. We excluded Canadian shipments from our analysis because the United States did not require Canadian WPM to meet ISPM15 standards during the sampling period. The policy of limited inspection on shipments from Canada is largely because most bark- and wood-infesting insects native to Canada are also native to the United States and because the long shared and largely forested border between the two countries presents no barriers to the migration of native or non-native insects. For example, about 97% of bark and ambrosia beetle species (Scolytinae) native to Canada are also native to the United States [41]. Similarly, we excluded all Chinese imports from our AQIM analysis because as of 17 December 1998, which was nearly six years prior to US implementation of ISPM15, the United States began regulating WPM from China in response to the rapidly increasing frequency of pest interceptions on Chinese WPM in the 1990s and the discoveries of Asian longhorned beetle infestations in New York in 1996 and Illinois in 1998 [8], [42]–[43]. This 1998 regulation on WPM [43] only affected exports from China to the United States. During the period from 1999 until US implementation of ISPM15, noncompliant Chinese shipments were typically fumigated at US ports, whereas after US implementation of ISPM15 most noncompliant shipments were sent back China. In addition, given that Mexico was the origin of more AQIM records than any other country (34% of all AQIM records during the 6-year study period, and 41% of the dataset after removal of the Canadian and Chinese records), we analyzed the remaining data both with and without the records from Mexico. The large number of Mexican consignments in the AQIM database was because several US-Mexico border crossings participated in AQIM program.

In our analyses, we tested separately the initial dates of Phase 1 (16 September 2005) and Phase 3 (5 July 2006) as the division points between pre- and post-implementation of ISPM15. For each date, we tested two scenarios: 1) exclusion of all data related to Canadian and Chinese imports, and 2) exclusion of all data related to Canadian, Chinese, as well as Mexican imports (for reasons explained above). We constructed a 2×2 contingency table for each scenario, comparing pre- and post-ISPM15 infestation rates of WPM, and analyzed each for statistical significance using Fisher’s exact test (right-sided probability, PROC FREQ) [44]. We used a significance level of α = 0.1 because infestation rates of WPM are typically low and we wished to reduce the likelihood of committing a Type II error (i.e., a false negative). We also calculated the power of our analysis to detect large reductions in pest infestation rates using presumed treatment effectiveness levels for ISPM15 of 50%, 70% and 90% mortality of the WPM-associated quarantine pests (PROC POWER) [44]. These results, tested with α = 0.05 and 0.1, would indicate the probability of detecting a 50%, 70% and 90% change in infestation rate had one occurred. When calculating the post-ISPM15 infestation rates in the above analyses, we only used data for those consignments in which the WPM was apparently compliant with ISPM15, i.e., stamped with the ISPM15 mark. We also calculated on an annual basis the percent of inspected consignments in which the WPM had the proper ISPM15 mark after US implementation of ISPM15 (2005–2009), and analyzed the data with nonlinear regression (PROC NLIN) [44]. In addition, we used methods similar to those described above to compare the pre- and post-ISPM15 infestation rates of WPM from the single country of Italy, which was the country of origin for the most borer interceptions on WPM that entered the United States during 1985–2000 [8].

PestID Data Analyses


PestID data cannot be used to statistically analyze for the effects of ISPM15 on interception rates because the data are collected in a nonrandom manner and the number of inspections where no pests are found is not recorded. Nevertheless, we did extract all interceptions of bark- and wood-boring insects in PestID from the 25-year period 1984 through 2008 to demonstrate changes over time in the types of borers being intercepted, the countries of origin, and the imported commodities most often associated with wood pests. As noted earlier, we recognize that the PestID data can be influenced by many factors such as changes in interception policies, staffing, etc. We restricted the dataset to those families of wood borers that were consistently targeted during port inspections over the 25-year period: Buprestidae, Cerambycidae, Cossidae, Curculionidae (including Platypodinae and Scolytinae), Sesiidae, and Siricidae. For records where the imported commodity was reported, we assigned the commodity to one of several trade sectors according to the Global Trade Analysis Project (GTAP) [45]–[46]. For example, some of the common GTAP sectors that we used included fabricated metal products (e.g., ironware, metalware, tubes, and wire), primary metals (e.g., aluminum, iron, and steel), machinery and equipment, quarry products (e.g., granite, marble, and slate), and fruit and vegetables.

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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0096611

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