Learning to Love Leftovers

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1 Learning to Love Leftovers Using By-Catch to Expand Our Knowledge in Entomology LORI R. SPEARS E ach year, federal and state agencies, including universities, conduct field surveys for invasive species in an attempt to detect new introductions early in the invasion process. National surveys for invasive insects are administered and coordinated by the United States Department of Agriculture s Animal and Plant Health Inspection Service Plant Protection and Quarantine AND RICARDO A. RAMIREZ (USDA-APHIS-PPQ) and the Forest Service through Farm Bill (www. aphis.usda.gov), the Cooperative Agricultural Pest Survey (CAPS) (caps.ceris. purdue.edu), and Early Detection Rapid Response (EDRR) ( programs. Thousands of traps are placed annually and monitored usually every one to two weeks throughout the U.S., mostly during the time of expected pest activity. These extensive trapping and monitoring efforts have led to improved pest detection and management and have supported additional pest-related research (e.g., Cranshaw 2011). Fortunately, these proactive and preventive program activities have resulted in few detections of new invasive species, at least relative to the number of traps, collection periods, and total number of Fig. 1. Japanese beetle (P. japonica) traps vary in color. Green traps capture fewer bees than bi-colored traps and have been preferred by some survey coordinators (photo credit: K. Watson, Utah Department of Agriculture and Food). 168 American Entomologist Fall 2015

2 specimens in samples. On the contrary, non-target insects are frequently captured in traps and some insects are caught in high numbers. This is because monitoring traps are generally non-selective and pheromone lures used to attract insects to traps vary in their selectivity. Unfortunately, these unintentionally trapped insects (termed by-catch ) are typically discarded, in part, because the federal databases only seek information regarding presence/absence of invasive species and funding usually does not cover evaluation of by-catch. Further, there is no centralized venue for reporting information on these leftover insects, even though many of them are of agricultural, forestry, and urban importance. Consequently, a concerted effort has been made to increase trap and pheromone specificity and decrease capture of non-target insects (e.g., Fleischer et al. 2005; Martín et al. 2013; Meagher and Mitchell 1999; Mori and Evenden 2013; Panzavolta et al. 2014). Hamilton et al. (1971), for example, found that white or yellow traps used for detecting the invasive Japanese beetle (Popillia japonica Newman) attracted large numbers of bumble bees (Bombus spp.), but that green traps captured fewer bees. As a result, many pest detection personnel now prefer to use green traps (Fig. 1) when surveying for the Japanese beetle (C. Burfitt, personal communication; H.W. Rogg, personal communication). While considerable efforts are made to reduce insect by-catch, comparatively fewer efforts seek additional information from these captures. We discuss the benefits of analyzing insect by-catch, such as aiding the detection of new non-target species and acting as a value-added collection with ecological merit (Buchholz et al. 2011). The hope is that the scientific community will consider insect by-catch as an additional way to address patterns and processes of entomological and ecological interest. By-Catch in the Primary Literature To determine the prevalence of by-catch in the recent literature, we conducted a brief literature search (during December 2013 and January 2014) of the Web of Science database for articles published from 1990 to 2013 with the search terms by-catch and non-target in the title, abstract, or keywords. We excluded Fig. 2. Number of papers published, , that examine by-catch and categorized by taxonomical group. Many papers examined multiple taxa. articles that did not specifically analyze by-catch. Approximately 281 articles were selected for review based on the criteria outlined above. Interestingly, most of the organisms that were analyzed as by-catch were aquatic, and only 47 articles examined arthropod by-catch, most of which were crustaceans (Fig. 2). This suggests that the vast majority of insect by-catch is apparently left unanalyzed, or if analyzed, unreported or not specifically mentioned in the title, abstract, or keywords. Therefore, the actual number of articles reporting data on by-catch may be underestimated. Indeed, we are aware of studies that were not detected during the search (e.g., Dodds et al. 2012; Rabaglia et al. 2008; Skvarla and Holland 2011). What Lessons Can We Learn from Non-Arthropod By-Catch Studies? Given the large number of papers that analyze aquatic by-catch, it stands to reason that entomologists can learn a lot from these studies. For example, fisheries by-catch has contributed to a better understanding of the behavior, habitat use, and other characteristics of the species involved (Soykan et al. 2008). Thus, one key lesson we can take from the fisheries literature is that data collection efforts can be expanded beyond traditional methods to include these incidental captures and therefore advance the understanding of biological and ecological factors driving insect populations. We discuss this in more detail for arthropods later (see subsection Insect by-catch as value-added collections, within this paper). A second lesson from the fisheries literature is that by-catch can have important consequences for non-target insect populations and may interfere with ecosystem services such as pollination and natural pest control. By-catch is an important contributing factor to the population declines of many marine species, and has led to negative impacts on marine ecosystems through changes in biotic interactions and nutrient cycles (Lewison et al. 2014). Unfortunately, insect by-catch has not been monitored or regulated, and so impacts on beneficial populations and ecosystem services may be going unnoticed (Read et al. 2006). How Much By-Catch is Discarded? It is unknown exactly how much insect by-catch is being discarded each year. An evaluation of this estimate is not easily attainable, as by-catch is not a component of survey databases and there is no standardized reporting of these data. We can only speculate on the amount of by-catch being discarded using data we collected during a recent survey for invasive insects. In 2013, we placed 90 tri-colored bucket traps (Fig. 3) in alfalfa and corn fields throughout Utah as part of a CAPS survey for three invasive moth pests. Trap contents were collected every two weeks from June to September following standard CAPS survey protocols (CAPS 2013). Some of the most frequently captured by-catch American Entomologist Volume 61, Number 3 169

3 Although considerable progress has been, and continues to be, made to reduce non-target captures, insect by-catch is an inevitable consequence of trapping and monitoring programs. Further, our capture numbers parallel captures from other field studies that have used different sampling strategies, and so it is likely that by-catch can help maximize survey and research benefits. Additional opportunities to collect data should not be overlooked, especially since large amounts of data are evidently unanalyzed or unreported. Fig. 3. Bucket trap used for monitoring invasive moth species (e.g., Helicoverpa armigera) (photo credit: L.R. Spears, Utah State University). were identified to species. Approximately 15,496 non-target moths and 5,999 beneficial insects (pollinators and natural enemies), belonging to at least 82 species, were collected from these traps (Table 1). During the same year, the Washington State Department of Agriculture regional Lepidoptera screening lab received more than 28,000 moth specimens from seven states (including Washington and Utah), and none of these specimens were targeted pests (note: most states pre-screen their samples and send only suspected individuals) (C. Looney, personal communication). Further, 35 other states placed approximately 3,579 bucket traps for the same three invasive moth pests in agricultural fields (including but not limited to alfalfa and corn fields) across the U.S. (available online at caps.ceris.purdue. edu to registered CAPS partners). Despite potential dissimilarities among state (and crop) captures, it is possible that in just a few months, nearly three-quarters and a quarter of a million non-target moths and beneficial insects were captured as by-catch, respectively. However, these estimates consider only one trap type and only pheromones set specifically for the invasive species related to this commodity survey. Federal and state agencies have been very responsive to making changes to survey methods when by-catch is abundant. As previously mentioned, many pest detection personnel prefer to use green traps when surveying for Japanese beetles, rather than white or yellow traps, since the former result in fewer bumble bee captures. Additionally, several states have recently raised concerns about high abundance of bee captures in tri-colored bucket traps (Fig. 3), and as a result, USDA s Center for Plant Health Science and Technology is in the process of re-assessing trap efficacy (H.W. Rogg, personal communication). What Can We Gain from Examining Insect By-Catch? The detection of new non-target species. Invasive species that are targeted during early detection surveys are determined based on their likelihood of being introduced, becoming established, and posing a significant risk to agriculture or other environmental resources. However, it is not clear whether targeting specific invasive species compromises detections of other unanticipated invaders (Bishop and Hutchings 2011). The reasoning is based, in part, on the consequences of screening only the taxa that look morphologically similar to the target pest. When by-catch has been analyzed, new invasive species Table 1. By-catch was collected from 90 bucket traps every two weeks from June to September Traps were placed in alfalfa and corn fields. On average, 2,215 non-target moths, 126 pollinators and natural enemies, belonging to at least 20 species, were collected per sampling event. Overall, 15,496 non-target moths, 5,999 pollinators and natural enemies, and at least 82 species were collected (note: some specimens were sorted only to genus and therefore were not included in this estimate). Species represented by more than 100 individuals are listed below. Species Total # Captured Natural Enemies Coccinella septempunctata 159 Coccinella transversoguttata 125 Hippodamia convergens 605 Pollinators Agapostemon angelicus/texanus 742 Apis mellifera 1063 Bombus bifarius 217 B. fervidus 283 B. huntii 110 B. nevadensis 149 B. rufocinctus 201 Eucera edwardsii 115 Melissodes agilis 279 Non-Target Moths Anarta decepta 385 Chrysoteuchia topiaria 894 Euxoa septentrionalis 140 Helicoverpa zea 5673 Plagiomimicus spumosum American Entomologist Fall 2015

4 have been detected, some of which have no close relation to the target species (e.g., Dodds et al. 2010; Haack et al. 2009; Jendek and Grebennikov 2009; Kelly et al. 2013; Looney et al. 2012; Rabaglia et al. 2008; Skvarla and Holland 2011). If the primary goal of early detection surveys is to detect invasive species before they become established and cause major impacts on agricultural production, natural resources, and the environment, then monitoring efforts may need to be expanded to include the screening of all collected specimens. Insect by-catch as value-added collections. Other advantages for analyzing by-catch that are relevant to entomology and ecology more generally include providing insight into patterns of insect abundance, distribution, and diversity (Buchholz et al. 2011). Indeed, the value of using by-catch for addressing questions of ecological relevance has already been recognized. Strange et al. (2011) obtained by-catch from Japanese beetle traps to examine the expansion potential of the wool carder bee (Anthidium manicatum L.), an exotic species that is not targeted by pest detection programs, but has the potential to adversely affect native bee species. They found that A. manicatum s potential distribution across the rest of the country is much broader than first suspected, suggesting that this species has the ability to overcome limiting environmental conditions. Hatten et al. (2013) examined two years of bumble bee by-catch collected from pitfall traps from the Palouse Prairie and found differences in historical vs. observed species presence, yearly changes in abundances and caste proportions, and effects of landscape cover. Gibson et al. (2012) used insect by-catch collected by the National Ecological Observatory Network (NEON) to validate species identifications using DNA barcoding. These data are publicly available through the Barcode of Life Datasystem ( so that other researchers can learn more about changes in insect populations over time, among other research possibilities (Hoekman et al. 2012). Today, more integrative and interdisciplinary approaches to ecology are being explored, and in response, ecology is becoming more reliant on large data sets and meta-analysis of multiple data sets (Fattorini 2013; Hampton et al. 2013). Additionally, demands for data Fig. 4. Map of U.S. survey locations (at the county level) for Japanese beetle (P. japonica) traps (NAPIS 2014). Fig. 5. Map of U.S. survey locations (at the county level) for old world bollworm (Helicoverpa armigera) traps (NAPIS 2014). sharing and reuse have increased and data collection interfaces have been created to make this sharing easier (White et al. 2013). Big data refers to the use of compilation datasets to address some of the most pressing issues in ecology (such as biodiversity and the impacts of climate change, land management, and land use) issues that require researchers to work at scales beyond those possible by most scientific endeavors (Hoekman et al. 2012). By-catch, especially those captured from invasive species surveys, could act as an important and consistent source of big data in the future because many of these surveys are carried out nearly nationwide (Figs. 4-5) and some of the surveys have Legend Established by Consensus Established by Survey Being Eradicated Eradicated Found Not Found Survey in Progress No Survey Legend Established by Consensus Established by Survey Being Eradicated Eradicated Found Not Found Survey in Progress No Survey been conducted annually for decades. Further, the CAPS program in particular has been continuously funded (albeit at ever decreasing levels) by USDA since 1982; therefore, these surveys will likely continue for decades to come. It is these aspects that make the by-catch from pest detection surveys incredibly promising and more relevant for big data analytics than by-catch collected during other ecological field studies involving invertebrates (Buchholz et al. 2011). There is an unprecedented wealth of data available to us, but unfortunately our collective ignorance has distracted and diverted us from effectively processing it and actually using it. American Entomologist Volume 61, Number 3 171

5 Finally, by-catch can also assist with building insect reference collections that are essential for making progress in many aspects of entomology (e.g., taxonomy, systematics, and diagnostics) and are a valuable resource for both current and future researchers. For example, insect by-catch can provide training for taxonomists and identifiers, making them better able to recognize peculiar specimens and thus raising the possibility of early detection (C. Looney, personal communication). Likewise, insect collections made from by-catch species can serve as important outreach tools for master gardeners and county extension agents, and training for undergraduate students. We recently recruited students to assist with processing of by-catch and, as a result, our students have been given broad exposure to entomological research and have gained practical curatorial and taxonomic experience. Logistics and Strategies for Increasing By-Catch Usage Why a shortage of insect by-catch usage? We suspect that one major reason few studies examine by-catch is the costs associated with sorting, preparing, mounting, labeling, identifying, and storing specimens. It is worth highlighting, however, that there are benefits associated with analyzing data that have already been collected, including capturing more value from time and money already spent (C. Looney, personal communication) and the saving of time, effort, and funds that would otherwise be taken up by fieldwork (Buchholz et al. 2011), especially if DNA barcoding can be used to minimize the amount of time processing specimens in the lab (dewaard et al. 2009) Other reasons for infrequent by-catch usage may include a lack of interest in research that does not directly support an investigator s primary research interests and a shortage of investigators with the level of taxonomic expertise required for analysis of this large a dataset (Buchholz et al. 2011). However, if survey coordinators are not interested in analyzing by-catch or do not have the taxonomic experience, their colleagues (within or across teams) may have an interest in, and be qualified to examine, these data. Strange et al. (2011) obtained by-catch after specimens were sorted through and inspected for target species by Utah s State Department of Agriculture. Similarly, data analyzed by Gibson et al. (2012) and made available online have already been used by others (e.g., Namin et al. 2014). By-catch funding. Due to the nature of early detection surveys, basic principles of experimental design cannot always be followed and perhaps this does not lend itself to favorable support from granting agencies. Articles that were uncovered during our literature review (see By-Catch in the Primary Literature) were funded by various federal, state, and local agencies, such as the National Science Foundation, the Environmental Protection Agency, United States Department of Agriculture (oftentimes through the CAPS program), local departments of agriculture, and universities, but none of these projects appear to have been directly funded to analyze by-catch specifically. In fact, many studies never even mentioned their funding source. Seemingly, researchers are leveraging their time and resources to complete these side projects. Funding for research is ever decreasing, but if collaborations and networks can be created, this could help connect those who have collected by-catch with those who want particular specimens. Collaborative networks of researchers will increase by-catch usage and may even make future grant proposals more competitive. Indeed, at least two different networks of by-catch have already been put into place (see Buchholz et al. 2011), but they are mostly international in scope and therefore do not include insects collected during early detection surveys in the U.S. Other sources of funding may include internal grants, such as cooperative extension, departmental, and undergraduate research awards. For instance, Utah State University Extension supported a project to pair by-catch with environmental data to understand insect activity patterns that may be useful for Utah s clientele. Skvarla and Holland (2011) received funding to examine non-target insects caught on emerald ash borer traps from the Purdue University College of Agriculture and Department of Entomology. Collaborations and networks. Online databases have become a valuable addition to scientific research in recent years. Databases provide a venue for recording and accessing data and help to facilitate communication among the scientific community, including exchanging of information and updates of ongoing efforts. For example, the Bee Database project (research.amnh.org/iz/bee-database-project) was created in 2003 with the goal of capturing information from bees being held at the American Museum of Natural History. These data have helped to document bumble bee declines and are currently being used to document changes in bee communities across space and time. Similarly, the Lost Ladybug Project ( encourages citizen scientists to submit lady beetle findings, and documents rare lady beetles to help prevent the decline of native species. As mentioned previously, NEON has put together a database ( org) of terrestrial insects, focusing mostly on mosquitoes and ground beetles, some of which were collected as by-catch (Gibson et al. 2012). A database would be useful for documenting insect by-catch from nationwide surveys as well. However, foreseeable challenges of setting up a database of this kind include funding for analyzing by-catch, getting data entered into the system, ensuring that all of the necessary information is included (e.g., GPS-based location data, null events), and getting the scientific community to accept and utilize these data (Buchholz et al. 2011). A successful database would also have in place tools (e.g., a checklist of species that are expected to occur in an area) to minimize reporting errors and improve data quality. While further discussion of these issues is beyond the scope of this paper (but see Buchholz et al. 2011), it is at least worth noting here that a centralized database would help facilitate the process of using by-catch to improve our understanding of biological systems. Conclusions New invasive species will continue to arrive to the U.S., despite our best efforts to stop them. In addition to these discoveries, large amounts of insect by-catch will be collected nationwide, and some of the by-catch will be of economic or environmental importance. Rather than discarding these data, it is clear that insect by-catch can be a valuable resource for many reasons. These include detecting new non-target species, expanding our knowledge of insect ecology more generally, and providing important outreach and training opportunities for extension personnel and current and future scientists. Indeed, the potential ways in which by-catch can be used are not exhaustively 172 American Entomologist Fall 2015

6 described here. Given that by-catch is being used, albeit at a low level, we are encouraged that more of our colleagues will come up with novel ways to utilize by-catch. By-catch usage appears to be a worthwhile research and outreach endeavor that should get another look from the scientific community, given its potential to generate new knowledge and ultimately increase our entomological and ecological output. For this to happen, the building of a collaborative network to connect scientists with relevant unprocessed collections within the U.S. should be among the list of starting points. Acknowledgements We thank Chris Looney and Carol Anelli for reviewing an earlier version of this manuscript, Chris Looney for identifying moth specimens, Terry Griswold, Harold Ikerd, Jonathan Koch, and Jamie Strange for identifying bee specimens, Anna Fabiszak for assisting with the literature review, and DaShell Burnham, Jaci Larson, and Breanne Garrard for spending countless hours in the lab processing by-catch. Funding came from a Utah State University Extension mini-grant and a USDA CAPS grant: Alfalfa and Corn Commodity Survey (# CA). References Cited Bishop, M.J., and P.A. Hutchings How useful are port surveys focused on target pest identification for exotic species management? Marine Pollution Bulletin 62: Buchholz, S., M. Kreuels, A. Krongshage, H. Terlutter, and O. Finch Bycatches of ecological field studies: bothersome or valuable? Methods in Ecology and Evolution 2: CAPS (Cooperative Agricultural Pest Survey (CAPS) Cooperative agricultural pest survey (CAPS) 2013 national survey guidelines April 22, Cranshaw, W Recently recognized range extensions of the walnut twig beetle, Pityophthorus juglandis Blackman (Coleoptera: Curculionidae: Scolytinae), in the Western United States. The Coleopterists Bulletin 65: dewaard, J.R., J.-F. Landry, B.C. Schmidt, J. Derhousoff, J.A. McLean, L.M. Humble In the dark in a large urban park: DNA barcodes illuminate cryptic and introduced moth species. Biodiversity and Conservation 18: Dodds, K.J., G.D. Dubois, and E.R. Hoebeke Trap type, lure placement, and habitat effects on Cerambycidae and Scolytinae (Coleoptera) catches in the Northeastern United States. Journal of Economic Entomology 103: Fattorini, S Regional insect inventories require long time, extensive spatial sampling and good will. PLoS ONE 8: e Fleischer, S.J., C.L. Harding, P.E. Blom, J. White, and J. Grehan Spodoptera frugiperda pheromone lures to avoid non-target captures of Leucania phragmatidicola. Journal of Economic Entomology 98: Gibson, C.M., R.H. Kao, K.K. Blevins, and P.D. Travers Integrative taxonomy for continental-scale terrestrial insect observations. PLoS ONE 7: e Haack, R.A., T.R. Petrice, and J.E. Zablotny First report of the European oak borer, Agrilus sulcicollis (Coleoptera: Buprestidae) in the United States. The Great Lakes Entomologist 42: 1-7. Hamilton, D.W., P. Schwartz, B.G. Townsend, and C.W. Jester Effect of color and design of traps on captures of Japanese beetles and bumblebees. Journal of Economic Entomology 64: Hampton, S.E., C.A. Strasser, J.J. Tewksbury, W.K. Gram, A.E. Budden, A.L. Batcheller, C.S. Duke, and J.H. Porter Big data and the future of ecology. Frontiers in Ecology and the Environment 11: Hatten, T.D., C. Looney, J.P. Strange, and N.A. Bosque-Perez Bumble bee fauna of Palouse Prairie: survey of native bee pollinators in a fragmented ecosystem. Journal of Insect Science 13: Hoekman, D., C. Gibson, and K. Blevins DNA barcodes for NEON s terrestrial insects: short- and long-term development and applications. Barcode Bulletin 3. Available at: Jendek, E., and V.V. Grebennikov Agrilus sulcicollis (Coleoptera: Buprestidae), a new alien species in North America. Canadian Entomologist 141: Kelly, J.A., T.S. Avery, D.T. Stewart, G.C. Cutler, S.O. Gaul, K.E. MacKenzie, and N.K. Hillier Non-target Gelechiidae and Noctuidae attraction to Aroga trialbamaculella (Lepidoptera: Gelechiidae) pheromone-based trapping systems. Canadian Entomologist 145: Lewison, R.L Global patterns of marine mammal, seabird, and sea turtle bycatch reveal taxa-specific and cumulative megafauna hotspots. PNAS 111: Looney, C., E. LaGasa, and S. 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The Canadian Entomologist 146: National Agricultural Pest Information System (NAPIS) Purdue University. Accessed: 12/11/ purdue.edu Panzavolta, T., M. Bracalini, L. Bonuomo, F. Croci, and R. Tiberi Field response of non-target beetles to Ips sexdentatus aggregation pheromone and pine volatiles. Journal of Applied Entomology 138: Rabaglia, R., D. Duerr, R. Acciavatti, and I. Ragenovich Early detection and rapid response for non-native bark and ambrosia beetles. USDA Forest Service, Forest Health Protection, Read, A.J., P. Drinker, and S. Northridge Bycatch of marine mammals in U.S. and global fisheries. Conservation Biology 20: Skvarla, M.J., and J.D. Holland Nontarget insects caught on emerald ash borer purple monitoring traps in western Pennsylvania. Northern Journal of Applied Forestry 28: Soykan, C.U., J.E. Moore, R. Žydelis, L.B. Crowder, C. Safina, and R.L. Lewison Why study bycatch? An introduction to the theme section on fisheries bycatch. Endangered Species Research 5: Strange, J.P., J.B. Koch, V.H. Gonzalez, L. Nemelka, and T. Griswold Global invasion by Anthidium manicatum (Linnaeus) (Hymenoptera: Megachilidae): assessing potential distribution in North America and beyond. Biological Invasions 13: White, E.P., E. Baldridge, Z.T. Brym, K.J. Locey, D.J. McGlinn, and S.R. Supp Nine simple ways to make it easier to (re) use your data. Ideas in Ecology and Evolution 6: Lori Spears is the Utah State University coordinator of the Utah Cooperative Agricultural Pest Survey (CAPS) program, which monitors invasive pests entering the state. Ricardo Ramirez is assistant professor and extension entomologist of the Department of Biology at Utah State University. DOI: /ae/tmv046 American Entomologist Volume 61, Number 3 173