Host associations between xylophagous longhorn beetles (Coleoptera: Cerambycidae) and American commodity tree species from Chinese collection sources

A small number of longhorn beetle species (Coleoptera: Chrysomeloidea: Cerambycidae) have the potential to become invasive forest pests. International trade in live plants and wood packaging material are known invasion pathways for longhorn beetles. Once an invasive pest is intercepted in a new region, a rapid pest risk analysis is often needed to determine the appropriate response. For accurate risk quantification, natural history evidence is necessary. This information is also vital in preventing introduction. This study gathered insect collection data, especially references to host plants, of xylophagous longhorn beetles from the Institute of Zoology, Chinese Academy of Sciences, Beijing, China. Beetle associations with three important host groups were investigated: Fagaceae, Citrus spp., and avocado (Persea americana). We performed a systematic literature review to identify previously documented cerambycidae associated with these plants. Here, we report insect-plant host associations for 39 species of longhorn beetles based on a review of the literature; 43 interactions were documented, 10 interactions were novel. No host associations were recorded with avocado in China. This information serves as a foundation for pest risk analysis in determining threats posed by potentially invasive longhorn beetles into new regions.


Introduction
Longhorn beetles, also commonly called long-horned or longicorn beetles, are often intercepted in new regions. While most are harmless, a small number can be highly invasive forest pests. Many species cannot successfully invade new regions. Yet, a small percentage can travel over long distances through human mediated transport and cause significant damage. All longhorn beetles are phytophagous, with juveniles often feeding internally on the xylem of the plant tissue and adults feeding externally on fast growing twigs and branches. The xylophagous species consume woody tissues, but even within this group there is a high degree of variability in behavior and host selection (Haack and Slansky 1987). Tree hosts of xylophagous longhorn beetles may be attacked under a range of conditions, from healthy trees to those recently dead . The larvae of xylophagous longhorn beetles feed either under the bark or in the xylem (Hanks 1999). Most cerambycid species colonize dead or severely stressed trees, but some are able to colonize living trees, in which they damage the flow of nutrients within the host causing dieback, wilting, and occasionally tree death .
Longhorn beetles may oviposit into commercial plants or wood packing material, conferring opportunities to "stowaway" on trade consignments originating within native ranges (Meurisse et al. 2019). International export of live plants, coupled with the use of wood packing material in a wide range of industrial transport practices, increases opportunistic invasion into new regions (Hulme et al. 2008). These pathways have been highlighted by recent invasions of several alien xylophagous longhorn beetles such as the Asian longhorn beetle Anoplophora glabripennis (Motschulsky, 1854) from its native range in Southeast Asia into Europe and North America (Hérard and Roques 2009). Once arrived in the new region, Asian longhorn beetle quickly established due to the wide host plant range. Attacks on local trees caused ecological and economic damage. Lengthy eradication efforts have been undertaken in the UK (Straw et al. 2015), USA (Haack et al. 2010), Italy, and in Central Europe (Hérard and Roques 2009; ). In the USA between 2006 and 2013 costs for eradication of Asian longhorn beetles were estimated to be $537 million (Eyre and Haack 2017).
Potentially invasive longhorn beetles are frequently intercepted at ports of entry into the USA (Haack and Cavey 2000). Pest risk analysis is used to gauge the appropriate level of response, such as regulation or monitoring. Guidelines and international standards for phytosanitary measures have been developed for pest risk analysis (FAO 2004(FAO , 2007Devorshak 2012). These standards utilize scientific evidence to determine the threat posed by the organism. Once the risk posed by a pest is quantified in this manner, appropriate responses such as whether it should be regulated, what, if any, measures should be imposed. A transparent, evidence-based approach is critical in determining potential pest status as well as guiding the managed response to biological invasions. A critical initial element of the pest risk assessment process is a literature review and synthesis of scientific data (Baker et al. 2009). This examination process determines the known information for adventive species. Yet, access to the primary data is often limited. Journals, datasets, herbaria, and gray literature can provide conflicting information about an organism or use unverified sources. In addition, language barriers can reduce the accessibility of information on international pests.
Over 36,000 species of longhorn beetle are recognized worldwide with many having little documented natural history. This knowledge gap complicates pest risk assessment as assumptions are made without direct scientific data. Taxonomic groupings can help to identify pest families. However, this is imprecise. Similarly, host plants and consignment origins can identify an invasion pathway (Eschen et al. 2015). However, plant hosts are only determined based on known examples in the country of origin, while data on suitability of the new hosts usually do not exist. Some xylophagous longhorn beetles, such as Xylotrechus arvicola (Olivier, 1800), have shown different host preference in invaded regions (García-Ruiz et al. 2012). Changes in host preferences are the most problematic issue when attempting to quantify the risk posed by a new species. If a host association is known, then a pathway and impacts may be quantified more accurately. For example, the presence or absence of a coevolved congener on a shared host may help predicting impacts of an invasive pest species (Mech et al. 2019). Therefore, knowing host associations may play a key role in accurately predicting invasive capability and impacts of alien longhorn beetles.
We inspected resources from the Institute of Zoology, Chinese Academy of Sciences, Beijing, China (here after IZCAS) to expand the range of known host associations. Collection records occasionally contained additional collection information such as the feeding or oviposition host tree.
This study focused on potential invasive pests of three groups of tree hosts that are economically and environmentally important in North America, and hence potentially susceptible to invasive Asian Cerambycidae: Fagaceae, the Citrus genus, and avocado. A comprehensive host search for all records or all hosts was beyond the boundaries of enquiry of this pilot project. Fagaceae are ecologically and economically important across the world, not just in the target region of the USA. The genus Citrus and the species avocado (Persea americana (Mill.)) were also selected because recent introductions of alien invasive species have highlighted susceptibility of these plant commodities to invasion and economic damage. The American citrus industry is worth $3.35 billion dollars (Simnitt and Calvin 2019) and the avocado industry $400 million dollars per annum (Perez and Minor 2018). Our target beetle species were xylophagous longhorn beetles, and excluded species feeding on non-woody plants. The specific questions for our survey were: (1) Which Cerambycidae species in the IZCAS collection and related materials have been recorded as feeding on, or associated with, the target plants? (2) For the identified beetle species, what plant associations have already been reported in previous literature? (3) Can this method provide data to support pest risk analysis?

Materials and methods
The survey of collection material was undertaken in situ at IZCAS. The original records were inspected for each of the more than 40,000 specimens in the collection. Collection notes and supporting documents were examined and explicit references to host trees recorded. Figure 1 shows a typical IZCAS collection specimen.  Each host label record involving an identified target tree species was recorded. For each beetle species that had an identified host plant, all synonyms were collated using online databases and published information resources (Table 1). Host associations were partly quantitative, we differentiated between singleton records (1-10), occasional records (11-25), and abundant records (26+) ( Table 2).
To complement the specimen label survey, a systematic literature review of online resources was then conducted (Table 1). All host interactions were recorded. The records from each database were compared highlighting the previously unpublished host interactions Novel hosts for these beetles, as well as the previously reported hosts are listed in Table 2. A comprehensive host record analysis is commonly the first step in pest risk analysis as part of a wider systematic literature review process. In addition to the databases listed, a Google Scholar® search was conducted with the first 100 records of all English and Chinese (Mandarin) language results, checked manually. This process was completed for the senior synonym and each junior synonym of each beetle species discovered as part of the scan. Species names were confirmed using the ITIS website (www.itis.gov; retrieved 03/10/2020). Beetles were identified to species and status followed Lin and Yang (2019). Table 2. Known host interactions of xylophagous longhorn beetles at IZCAS. Examples in bold indicate previously recorded host interactions identified in the literature. Abundance of total sampled specimens in IZCAS is simplified as 1-10 *, 11-25 **, 26+ *** in the Species Name column. Host Species abundance represent the number of specimens recording that host association. When no further information is given in the species column the original literature source identified the plant host to family level. Scientific names of the host trees were revised and confirmed according to the Taxonomic Cheo 1936;Lieu 1945;Gressitt 1951;DFZJP 1983;Hua 2002 Salicaceae Salix sp.

Results
We investigated the known records for 40,843 specimens at IZCAS. As a result of our investigation we identified a total of 39 species of xylophagous longhorn beetle associated with Fagaceae, Citrus, and avocado. The 39 identified beetle species had 43 documented host associations with at least one of the target trees. Some beetle species were recorded on more than one target tree host. By systematically reviewing the known literature we followed a similar process to a preliminary risk assessment and discovered 33 interactions previously documented. The remaining 10 associations were novel and previously unrecorded (Table 2). When a hostinteraction was previously recorded on a plant of the same genus (e.g. Quercus sp.), we did not consider this a newly documented host association. No associations of Chinese longhorn beetles with avocado were recorded.

Discussion
The 10 new associations, previously unpublished, may be used to help determine potential pest risk. The remaining 33 associations provide important corroboration of previously recorded single observations. Multiple reported observations increase data reliability (Groom et al. 2017).
Some of the beetles identified in our study have the potential to become an important economic pest and warrant further study. We identified two Anoplophora species, A. imitator (White, 1858) and A. lurida (Pascoe, 1856) on Fagaceae. This genus has two pest species already recognized as being of global concern, A. chinensis (Forester, 1771) andA. glabripennis. Lingafelter andHoebeke (2002) note that two thirds of the 36 species within this genus have no recorded natural history, so the threat of other Anoplophora is unknown. Another species identified in our study, Anoplistes halodendri subsp. pirus (Arakawa, 1932), has been previously misidentified in the literature as A. halodendri (Pallas, 1776). A. halodendri subsp. pirus had caused mass mortality of sea buckthorn (Hippophae rhamnoides Linné) and sweetvetch (Hedysarum scoparium Linné) in China (Liu et al. 2012). While not definitive, evidence of pest status in other regions can identify potential pest status in adventive regions (Eyre and Haack 2017).
Avocado is native to South and Central America yet it has been planted in China for roughly 100 years (Liu and Zhou 2000). It has sporadically been trialed as a commercial crop. Commercial trials often have higher levels of vigilance and observation compared to amenity horticulture, and various provenance and pest susceptibility trials have been conducted in China (Luo and Jin 1995;Li 2000). As such, the lack of host-associations identified here are unexpected. Xylophagous longhorn beetles are documented as attacking avocado in other regions. In Hawaii, the invasive longhorn beetle Acalolepta aesthetica (Olliff, 1890) is an emerging pest of avocado, despite the beetle being native to Australia (Matsunaga et al. 2019). Similar studies in regions where avocado is longer established may highlight pests and associations that have been previously unrecorded.
Lack of scientific data during the pest risk analysis process could lead to an underestimation of the impacts of invasion, particularly if a species is not considered a threat to a major agricultural crop or commercial plantation (Devorshak 2012). Our two-stage survey method aimed to identify previously unpublished host interactions between xylophagous longhorn beetles and a limited range of commodity tree species that are ecologically or economically important in the USA.
Host associations records may indicate the likely area of risk of understudied alien species. Many longhorn species have little documented ecology making pest risk analysis processes difficult (Eyre and Haack 2017). Three beetle species had no host-associations identified in our systematic literature review prior to this research. In order to perform a risk assessment, the area at risk cannot be assessed without information about the host. Likewise, the level of host-specificity would be unclear. Prior to this study that identified a Fagaceae host (Quercus sp.) it could be assumed that a species like Chloridolum laotium (Gressitt & Rondon, 1970) is oligophagous on pine trees as Pinus spp. were the only previously recorded hosts. Similar results can be seen with Chlorophorus annulatus (Hope, 1831) (previously only recorded on Coffea sp.) and Metastrangalis thibetana (Blanchard, 1871) (previously only recorded on Metasequoia glyptostryboides Hu & Cheng). The results indicate a more diverse host association than previously known for these species. This information may be used to determine a longhorn beetles potential area at risk which impacts the pest risk assessment and phytosanitary regulation.
Despite generating useful information, there are still limitations to this study. Many other associations have probably been recorded but are inaccessible. Groom et al. (2017) discuss the difficulties of finding accurate biodiversity data, lack of interoperability and standardization, and paywalls, where access to information requires a subscription service or payment to be made. Language differences can present a special barrier, especially when collection records follow traditional or local plant taxa names, rather than the Latin binomial nomenclature. These issues increase the likelihood of host associations being unusable or incomplete during the pest risk analysis process because regulations are implemented based on species names (FAO 2007) Previous records can themselves be inaccurate. When using historical data of this nature we cannot verify the accuracy of the host plant identified by the specimen collector in the museum collections. Often, the tree name has been translated and with colloquial or family names used for groups of similar species. As such, identification of hosts can only be made as accurate as the translated local name. Additionally, whether the plant was a feeding host or oviposition host is not recorded. The records in Table  2 identify the number of observations recorded by the original collectors in the IZCAS collection. We can infer that specimens frequently collected on the same plants likely have an association.
Our focus on the tree genus or species in question, but not on its phylogenetic relatives, can be also seen as a limitation. Many insects switch hosts within a higher phylogenetic group, regardless of whether they coevolved with the plant species or not. For example, records at IZCAS do not indicate any Cerambycidae associations on avocado, but many Chinese longhorn beetles exploit native Lauraceae trees and may potentially switch to avocado. However, the strength of our inference is that all studied tree taxa are widely planted in China, and thus served as an analog of sentinel gardens, or living in situ laboratories for new host association studies (Eschen et al. 2019).
This method could be used on other collections and other target groups to highlight species of potential pest status. Equally, documented host feeding evidence is also utilized outside of the pest risk assessment system and could provide ecological information about these organisms in many types of future studies.