Coupling Traditional Monitoring and Citizen Science to Disentangle the Invasion of Halyomorpha halys

The brown marmorated stink bug, Halyomorpha halys Stal (Hemiptera: Pentatomidae), is an invasive pest that has expanded its range outside of its original confinements in Eastern Asia, spreading through the United States, Canada and most of the European and Eurasian countries. The invasiveness of this agricultural and public nuisance pest is facilitated by the availability of an array of suitable hosts, an r-selected life history and the release from natural enemies in the invaded zones. Traditional monitoring methods are usually impeded by the lack of time and resources to sufficiently cover large geographical ranges. Therefore, the citizen science initiative “BugMap” was conceived to complement and assist researchers in breaking down the behavior of this invasive pest via a user-friendly, freely available mobile application. The collected data were employed to forecast its predicted distribution and to identify the areas at risk in Trentino, Northern Italy. Moreover, they permitted the uncovering of the seasonal invasion dynamics of this insect, besides providing insight into its phenological patterns, life cycle and potential management methods. Hence, the outcomes of this work emphasize the need to further integrate citizens in scientific endeavors to resolve ecological complications and reduce the gap between the public and science.

[1]  Eppo EPPO Global Database , 2015 .

[2]  M. Crawley,et al.  Exotic plant invasions and the enemy release hypothesis , 2002 .

[3]  M. Raupp,et al.  Host Plant Use by the Invasive Halyomorpha halys (Stål) on Woody Ornamental Trees and Shrubs , 2016, PloS one.

[4]  R. Venette,et al.  Cold Tolerance of Halyomorpha halys (Hemiptera: Pentatomidae) Across Geographic and Temporal Scales , 2016, Environmental Entomology.

[5]  David N. Bonter,et al.  Citizen Science as an Ecological Research Tool: Challenges and Benefits , 2010 .

[6]  E. Green,et al.  Landscape Factors Facilitating the Invasive Dynamics and Distribution of the Brown Marmorated Stink Bug, Halyomorpha halys (Hemiptera: Pentatomidae), after Arrival in the United States , 2014, PloS one.

[7]  Valerio Mazzoni,et al.  Multiple lines of evidence for reproductive winter diapause in the invasive pest Drosophila suzukii: useful clues for control strategies , 2016, Journal of Pest Science.

[8]  Krista G. Hilchey,et al.  A review of citizen science and community-based environmental monitoring: issues and opportunities , 2011, Environmental monitoring and assessment.

[9]  Harris David,et al.  A statistical explanation of MaxEnt for ecologists , 2013 .

[10]  Neil D. Burgess,et al.  Monitoring Matters: Examining the Potential of Locally-based Approaches , 2005, Biodiversity & Conservation.

[11]  B. Short,et al.  Efficacy of insecticide residues on adult Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) mortality and injury in apple and peach orchards. , 2014, Pest management science.

[12]  C. Kolar,et al.  Progress in invasion biology: predicting invaders. , 2001, Trends in ecology & evolution.

[13]  P. Shearer,et al.  Brown marmorated stink bug [Halyomorpha halys (Stål, 1855)] (Heteroptera: Pentatomidae) in Hungary. , 2014 .

[14]  R. Richards-Kortum,et al.  A comparison of C/B ratios from studies using receiver operating characteristic curve analysis. , 1999, Journal of clinical epidemiology.

[15]  B. Forster,et al.  First records of an invasive bug in Europe: Halyomorpha halys Stål (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? , 2008 .

[16]  L. Dosdall EVIDENCE FOR SUCCESSFUL OVERWINTERING OF DIAMONDBACK MOTH, PLUTELLA XYLOSTELLA (L.) (LEPIDOPTERA: PLUTELLIDAE), IN ALBERTA , 1994, The Canadian Entomologist.

[17]  T. Measham Building Capacity for Environmental Management: local knowledge and rehabilitation on the Gippsland Red Gum Plains , 2007 .

[18]  G. Hamilton,et al.  Use of Black Light Traps to Monitor the Abundance, Spread, and Flight Behavior of Halyomorpha halys (Hemiptera: Pentatomidae) , 2013, Journal of economic entomology.

[19]  J. Silvertown A new dawn for citizen science. , 2009, Trends in ecology & evolution.

[20]  Frederic Bartumeus,et al.  Citizen science provides a reliable and scalable tool to track disease-carrying mosquitoes , 2017, Nature Communications.

[21]  Thomas J. Stohlgren,et al.  Improving and integrating data on invasive species collected by citizen scientists , 2010, Biological Invasions.

[22]  C. Capinha,et al.  Assessing the environmental requirements of invaders using ensembles of distribution models , 2011 .

[23]  Jeremy J. D. Greenwood,et al.  Citizens, science and bird conservation , 2007, Journal of Ornithology.

[24]  Anne L. Nielsen,et al.  Life History of the Invasive Species Halyomorpha halys (Hemiptera: Pentatomidae) in Northeastern United States , 2009 .

[25]  M. Raupp,et al.  Traps and Trap Placement May Affect Location of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) and Increase Injury to Tomato Fruits in Home Gardens , 2014, Environmental entomology.

[26]  Kelly A. Lee,et al.  A role for immunology in invasion biology. , 2004, Trends in ecology & evolution.

[27]  G. Anfora,et al.  Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe , 2014, Journal of Pest Science.

[28]  William R. Morrison,et al.  Establishing the behavioral basis for an attract-and-kill strategy to manage the invasive Halyomorpha halys in apple orchards , 2015, Journal of Pest Science.

[29]  R. Bonney,et al.  Scientific knowledge and attitude change: The impact of a citizen science project , 2005 .

[30]  T. Leskey,et al.  Host Plant Effects on Halyomorpha halys (Hemiptera: Pentatomidae) Nymphal Development and Survivorship , 2016, Environmental Entomology.

[31]  T. Dawson,et al.  Selecting thresholds of occurrence in the prediction of species distributions , 2005 .

[32]  Rainer M. Krug,et al.  Spatially‐explicit sensitivity analysis for conservation management: exploring the influence of decisions in invasive alien plant management , 2010 .

[33]  Victoria P. Skillman,et al.  Phenology of brown marmorated stink bug described using female reproductive development , 2017, Ecology and evolution.

[34]  G. Dively,et al.  Adjacent Habitat Influence on Stink Bug (Hemiptera: Pentatomidae) Densities and the Associated Damage at Field Corn and Soybean Edges , 2014, PloS one.

[35]  B. Blossey,et al.  Evolution of Increased Competitive Ability in Invasive Nonindigenous Plants: A Hypothesis , 1995 .

[36]  I. Radulov,et al.  Geographic information systems (GIS) and entomological research : a review , 2010 .

[37]  Lara Maistrello,et al.  Citizen science and early detection of invasive species: phenology of first occurrences of Halyomorpha halys in Southern Europe , 2016, Biological Invasions.

[38]  D. Inkley Characteristics of Home Invasion by the Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) , 2012 .

[39]  Anne L. Nielsen,et al.  Impact of the Invasive Brown Marmorated Stink Bug in North America and Europe: History, Biology, Ecology, and Management. , 2018, Annual review of entomology.

[40]  Wolfgang Nentwig,et al.  Grasping at the routes of biological invasions: a framework for integrating pathways into policy , 2008 .

[41]  K. Tindall,et al.  Halyomorpha halys (Hemiptera: Pentatomidae): a First Kansas Record , 2012 .

[42]  Steven J. Phillips,et al.  Sample selection bias and presence-only distribution models: implications for background and pseudo-absence data. , 2009, Ecological applications : a publication of the Ecological Society of America.

[43]  P. Shearer,et al.  Electronically Monitored Labial Dabbing and Stylet ‘Probing’ Behaviors of Brown Marmorated Stink Bug, Halyomorpha halys, in Simulated Environments , 2014, PloS one.

[44]  S. V. Joseph,et al.  Characterizing spring emergence of adult Halyomorpha halys using experimental overwintering shelters and commercial pheromone traps , 2017 .

[45]  G. Hamilton,et al.  Exploring the Spread of Brown Marmorated Stink Bug in New Jersey Through the Use of Crowdsourced Reports , 2016 .

[46]  Benoit Gauzens,et al.  Massively Introduced Managed Species and Their Consequences for Plant–Pollinator Interactions , 2017 .

[47]  Robert J Fletcher,et al.  Predicting Species Distributions from Samples Collected along Roadsides , 2012, Conservation biology : the journal of the Society for Conservation Biology.

[48]  Robert P. Anderson,et al.  Maximum entropy modeling of species geographic distributions , 2006 .

[49]  R. Bugiani,et al.  Distribution and damage caused by Halyomorpha halys in Italy , 2016 .

[50]  Matthew J. Smith,et al.  Protected areas network is not adequate to protect a critically endangered East Africa Chelonian: Modelling distribution of pancake tortoise, Malacochersus tornieri under current and future climates , 2013, bioRxiv.

[51]  J. Engler,et al.  Mapping Species Distributions with MAXENT Using a Geographically Biased Sample of Presence Data: A Performance Assessment of Methods for Correcting Sampling Bias , 2014, PloS one.

[52]  Robert P. Anderson,et al.  Evaluating predictive models of species’ distributions: criteria for selecting optimal models , 2003 .

[53]  J. Cooley The Distribution of Periodical Cicada (Magicicada) Brood I in 2012 with Previously Unreported Disjunct Populations (Hemiptera: Cicadidae, Magicicada) , 2015 .

[54]  R. Guidetti,et al.  Genetic diversity of the brown marmorated stink bug Halyomorpha halys in the invaded territories of Europe and its patterns of diffusion in Italy , 2018, Biological Invasions.

[55]  E. Kistner Climate Change Impacts on the Potential Distribution and Abundance of the Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) With Special Reference to North America and Europe , 2017, Environmental Entomology.

[56]  Christopher A. Lepczyk,et al.  Integrating published data and citizen science to describe bird diversity across a landscape , 2005 .

[57]  S. Graff,et al.  First records of the invasive pest, Halyomorpha halys (Hemiptera: Pentatomidae), in Ontario and Quebec. , 2011 .

[58]  T. Haye,et al.  Phenology, life table analysis and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe , 2014, Journal of Pest Science.

[59]  J. Overpeck,et al.  Responses of plant populations and communities to environmental changes of the late Quaternary , 2000, Paleobiology.

[60]  G. Zhu,et al.  Potential Geographic Distribution of Brown Marmorated Stink Bug Invasion (Halyomorpha halys) , 2012, PloS one.