The Great Lakes Entomologist
Volume 50 Numbers 3 & 4 -- Fall/Winter 2017 Numbers 3 & Article 6 4 -- Fall/Winter 2017
December 2017
TGLE Vol 50 nos. 3 & 4 full issue
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Vol. 50, Nos. 3 & 4 Fall/Winter 2017
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THE MICHIGAN ENTOMOLOGICAL SOCIETY 2017–18 OFFICERS President Matthew Douglas President Elect Elly Maxwell Immediate Pate President Robert Haack Secretary Adrienne O’Brien Treasurer Angie Pytel Member-at-Large (2017-2019) James Dunn Member-at-Large (2017-2019) Toby Petrice Member-at-Large (2016-2018) John Douglass Member-at-Large (2016-2018) Martin Andree Lead Journal Scientific Editor Kristi Bugajski Lead Journal Production Editor Alicia Bray Associate Journal Editor Anthony Cognato Associate Journal Editor Julie Craves Associate Journal Editor David Houghton Associate Journal Editor William Ruesink Associate Journal Editor William Scharf Associate Journal Editor Daniel Swanson Newsletter Editor Mark O’Brien Webmaster Mark O’Brien The Michigan Entomological Society traces its origins to the old Detroit Entomological Society and was organized on 4 November 1954 to “. . . promote the science of entomology in all its branches and by all feasible means, and to advance cooperation and good fellowship among persons interested in entomology.” The Society attempts to facilitate the exchange of ideas and information in both amateur and professional circles, and encourages the study of insects by youth. Membership in the Society, which serves the North Central States and adjacent Canada, is open to all persons interested in entomology. There are five paying classes of membership: Active—annual dues $25.00 Student (to 12th grade)—annual dues $12.00 Institutional—annual dues $45.00 Sustaining—annual contribution $35.00 or more Life—$500.00 Dues are paid on a calendar year basis (Jan. 1-Dec. 31). Memberships accepted before July 1 shall begin on the preceding January 1; memberships accepted at a later date shall begin the following January 1 unless the earlier date is requested and the required dues are paid. All members in good standing receive the Newsletter of the Society. All active and sustaining members may vote in Society affairs. All dues and contributions to the Society are deductible for Federal income tax purposes. SUBSCRIPTION INFORMATION The journal is published online and open access, there is no subscription needed. Articles are avail- able in pdf format and can be printed from the website, free of charge. To view current and past volumes, please visit http://scholar.valpo.edu/tgle/ .
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New Species Records for Wisconsin False Click Beetles (Coleoptera: Eucnemidae), with a Checklist of the Wisconsin Eucnemid Fauna Robert L. Otto1* and Daniel K. Young2** 1W4806 Chrissie Circle, Shawano, Wisconsin 54166, U.S.A. 2Department of Entomology, University of Wisconsin, Madison, Wisconsin 53706, U.S.A.
Abstract In Wisconsin, Microrhagus opacus Otto, Euryptychus ulkei (Horn) and Fornax bicolor (Melsheimer) are recorded for the first time. Records for these three species are based on nine specimens, most of which were taken since 2008. Two specimens of M. opacus taken from a Grant County Malaise trap in the late 1970’s as part of a statewide gypsy moth parasitoid recovery project, were previously identified as Microrhagus audax Horn. Most of the specimens reported herein were taken late in the collecting season, primarily during August. A checklist of the 20 genera and 41 species of Wisconsin Eucnemidae is also included.
Eucnemidae is a globally distributed, especially in tropical regions (Muona 2000; moderately sized elateroid family comprising Otto 2016). Species of Eucnemidae are also approximately 1900 species in 200 genera good indicators of diverse forest composition (Otto 2016). Eucnemidae is most diverse in (Muona 2000). the subtropical and tropical regions of the world, with numerous radiations into tem- Materials and Methods perate and boreal regions. In the Nearctic region, the family is comprised of 37 genera Specimen Data and Specimens. and nearly 100 species, including a number Specimens were examined under ACE® of new species to be described by the senior Modulamp® unit with gooseneck fiber-optic author (RLO) in forthcoming publications. illumination, through a Wild M3C 6.4–40x Forty-one eucnemid species in 20 genera zoom stereo binocular microscope with 20x are currently known from Wisconsin, in- oculars. cluding the three species reported herein. All specimens of Microrhagus opacus Five additional, yet unconfirmed, species of Otto and most specimens of Fornax bicolor Eucnemidae may also be present in the state (Melsheimer) reported herein are vouchered based on collection records from neighboring in the Insect research Collection (WIRC) of or nearly adjacent states. the Department of Entomology, University The common name, “false-click bee- of Wisconsin-Madison. A single specimen of tles,” has been referred to a belief that Euryptychus ulkei (Horn) and one specimen of F. bicolor are deposited in the collection beetles in the family lack the functional of the Global Eucnemid Research Project “clicking” mechanism common in adults of (GERP) also at the Department of Entomol- Elateridae (Muona 2000). However, many ogy, University of Wisconsin-Madison and eucnemid species have the ability to click under the current supervision of RLO. and in doing so produce a series of audible sounds, possibly forming a defensive strategy Label data are presented verbatim, to startle any would-be predators (Muona with text for each individual label placed 1993). The common name is still in use, but inside quotation marks and separated from Eucnemidae is readily distinguished from an underlying label by a slash (/). Each Elateridae by the subterminal attachment of specimen deposited in the collection of the the antennal pedicel to the scape (terminal Global Eucnemid Research Project bears a in Elateridae). green framed white label, “Collection of the Global Eucnemid Research Project, (Robert Associations with fungi present in L. Otto)”. coarse woody debris and dead trees within forested ecosystems are important factors in Figures. Habitus images were cap- the family’s role in forest ecosystem services, tured by the RLO as TIFF files taken with a JVC KY-F75U digital camera attached to a Leica® Z16 APO dissecting microscope with *Corresponding author: ([email protected]) apochromatic zoom objective and motor focus **Corresponding author: (young@entomology. drive, using a Synchroscopy Auto-Montage® wisc.edu) Pro System and software version 5.01.0005,
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Figures 1–3. Figure 1. Microrhagus opacus Otto: habitus, dorsal view; Figure 2. Euryptychus ulkei (Horn): habitus, dorsal view; Figure 3. Fornax bicolor (Melsheimer): habitus, dorsal view (Scale bar = 1.0 mm). Digital images: RLO.
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resulting image stacks were processed using –89.88363°W, Geodetic datum: WGS84, 26 CombineZP®. Each image was modified July–1 August 2011, collector: Daniel K. through Photoshop Elements 10® (Adobe Young / ex. Malaise in Populus, grandidenta- Systems Inc.) software on a Toshiba Sat- ta blow (1, GERP; 2, WIRC)]. Two additional ellite® C55 series laptop computer and all specimens were taken from Jackson County were collated into plates through the com- [USA: WI: Jackson County, NE of Black puter’s paint program. River Falls, near Levis Creek [WGS84], 44.31134°N, –90.82335°W, 26 July–02 Results and Discussion August 2011, collector: Daniel K. Young / Muona (2000) identified two specimens ex. Malaise trap in, Quercus-Pinus forest from the WIRC as Microrhagus audax Horn (1, WIRC)]; [USA: WI: Jackson County, taken from Malaise trap residues associated NE of Black River Falls, near Levis Creek with a statewide survey to recover potential [WGS84], 44.31134°N, –90.82335°W, 02–09 gypsy moth parasitoids. These specimens August 2011, collector: Daniel K. Young / were recently re-evaluated by RLO and ex. Malaise trap in, Quercus-Pinus forest (1, determined to represent M. opacus (Fig. 1), WIRC)]. Fornax bicolor is an eastern North previously recorded from Alabama, Florida, American species previously known from Georgia, Indiana, Kansas, and New York Quebec, Alabama, Arkansas, Florida, Geor- (Otto 2015). One specimen was taken at a gia, Illinois, Indiana, Louisiana, Missouri, Malaise trap in the Lower Wisconsin River New York, North Carolina, Pennsylvania, valley in southwestern Wisconsin [WI: Grant Co., T6N R6W sec. 17, 26 VII–9 VIII 1976, South Carolina, and Virginia (Muona 2000). Gypsy Moth-MT (WIRC)]. A second specimen The Wisconsin records reset the known was taken from a same locale a year later northwestern distributional range boundary [WI: Grant Co., T6N R6W sec. 17, 15–22 VI of this widespread but uncommonly encoun- 1977, Gypsy Moth-MT (WIRC)]. Thirty-one tered species. years later, a third specimen of M. opacus Despite relatively intensive collecting was recovered by the junior author (DKY) efforts across Wisconsin for Eucnemidae from a barrier pitfall trap placed in an oak and other Coleoptera in recent years, new savanna restoration in southcentral Wiscon- sin, west of the village of Cross Plains [USA: records continue to be relatively easy to WI: Dane County, Swamp Lover’s Incorp., document, as evidenced by the current con- 43° 08’13”N, –89° 39’47”W, WGS84, 22–28 tribution which represents an 8% increase July 2008, coll: Daniel K. Young] / [barrier in the known eucnemid fauna of the state. pitfall trap, upland savanna (WIRC)]. Such revelations provide clear evidence that we are nowhere near approaching any The new record for a single specimen of E. ulkei (Fig. 2) comes from a purple prism hypothetical upper asymptote with respect trap (Synergy Semiochemicals Inc., Vancou- to most of our regional insect species accu- ver, British Columbia, Canada) deployed in mulation curves. This is not at all reassuring southwestern Wisconsin while monitoring given the rates of habitat fragmentation and for the adventive emerald ash borer, Agri- loss, climate change, and impacts of invasive lus planipennis Fairemaire [WI: Richland species. It does, however, vividly illustrate Co., along McCarthy Lane, N43.374134°, that the need for even the most basic of biotic W-090.406902°, EABT103909B, 28 July surveys and inventories—particularly with 2011, Andy Anderson / Taken from EAB, respect to insect species—is far from having prism trap baited, with Manuka oil, & Z3- been met. And without such baseline species Hexen-1-ol (GERP)]. Euryptychus ulkei has inventories and collection event data, we re- previously been confirmed from Georgia, main far from being able to provide the kinds Mississippi, Ohio, Pennsylvania and Virgin- of evidence requisite to feed into predictive ia (Muona 2000; Hoffman et al 2009), thus the Wisconsin record represents a consider- ecological modeling, or even common sense able northwestern range extension. strategies, essential to the land managers and stewards of our precious and vanishing The new records for F. bicolor (Fig. 3) natural areas. come from three collection events by DKY using Malaise traps. The first is from cen- The complete checklist of false click tral Wisconsin [USA: WI: Adams County, beetles known to occur in Wisconsin includes Quincy Bluff Preserve, TNC, 43.86627°N, the following:
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EUCNEMIDAE OF WISCONSIN SUBFAMILY PSEUDOMENINAE Muona, 1993 Tribe Schizophilini Muona, 1993 Schizophilus subrufus (Randall, 1838)
SUBFAMILY MELASINAE Fleming, 1821 Tribe Melasini Fleming, 1821 Isorhipis obliqua (Say, 1836) Isorhipis ruficornis (Say, 1823) Tribe Xylobiini Reitter, 1911 Xylophilus crassicornis Muona, 2000 Xylophilus cylindriformis (Horn, 1871) Tribe Epiphanini Muona, 1993 Epiphanis cornutus Eschscholtz, 1829 Hylis frontosus (Say, 1836) Hylis terminalis (LeConte, 1866) Tribe Dirhagini Reitter 1911 Dirrhagofarsus ernae Otto, Muona & McClarin, 2014 Dirrhagofarsus lewisi (Fleutiaux, 1900) Microrhagus audax Horn, 1886 Microrhagus breviangularis Otto, 2015 Microrhagus brunneus Otto, 2013 Microrhagus carinicollis Otto, 2015 Microrhagus lecontei Otto, 2015 Microrhagus opacus Otto, 2015 Microrhagus pectinatus LeConte, 1866 Microrhagus subsinuatus LeConte, 1852 Microrhagus triangularis (Say, 1823) Entomophthalmus rufiolus (LeConte, 1866) Rhagomicrus bonvouloiri (Horn, 1886) Rhagomicrus humeralis (Say, 1836) Sarpedon scabrosus Bonvouloir, 1875
SUBFAMILY EUCNEMINAE Eschscholtz, 1829 Tribe Mesogenini Muona, 1993 Stethon pectorosus LeConte, 1866 Tribe Eucnemini Eschscholtz, 1829 Eucnemis americana Horn, 1886
SUBFAMILY MACRAULACINAE Fleutiaux, 1922 Tribe Euryptychini Mamaev, 1976 Euryptychus heterocerus (Say, 1836) Euryptychus ulkei (Horn, 1886) Tribe Macraulacini Fleutiaux, 1922 Onichodon canadensis (Brown, 1940) Onichodon downiei Muona, 2000 Onichodon orchesides Newman, 1838 Onichodon rugicollis (Fall, 1925) Fornax bicolor (Melsheimer, 1844) Isarthrus calceatus (Say, 1836) Isarthrus rufipes (Melsheimer, 1844) Dromaeolus badius (Melsheimer, 1844) Dromaeolus cylindricollis (Say, 1836) Dromaeolus harringtoni Horn, 1886 Dromaeolus striatus (LeConte, 1852) Thambus horni Muona, 2000 Deltometopus amoenicornis (Say, 1836) Tribe Nematodini Leiler, 1976 Nematodes penetrans (LeConte, 1852)
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Acknowledgments Literature Cited We are grateful to Dr. Craig Brabant, Hoffman, R. L., R. L. Otto & R. Vigneault. curator of the WIRC, for his cooperation and 2009. An annotated list of the false click assistance with this project. The long-stand- beetles of Virginia (Coleoptera: Eucnemidae). ing permitting support to DKY by the Wis- Banisteria 34: 25–32. consin Department of Natural Resources, Muona, J. 1993. Review of the Phylogeny, Classi- Bureau of Natural Heritage Conservation, fication and Biology of theFamily Eucnemi- State Natural Areas Program (Thomas Mey- dae (Coleoptera). Entomologica Scandinavica er) and the Wisconsin Chapter of The Nature Supplement 44: 133 pp. Conservancy (Nick Miller) is also gratefully acknowledged. Permission to sample at Muona, J. 2000. A revision of the Nearctic Euc- Swamp Lover’s Incorporated was granted nemidae. Acta Zoologica Fennica 212: 1–106. to DKY by Swamp Lovers Foundation presi- Otto, R. L. 2015. Eucnemid larvae of the Nearctic dent, Gerry Goth. Partial funding support for region. Part V: Fifth instar larval descrip- this and related Wisconsin beetle inventory tions for eight species of Microrhagus Dejean, projects (to DKY and the WIRC) was made 1833 (Coleoptera: Eucnemidae: Melasinae: available by the University of Wisconsin Dirhagini), with descriptions of four new Natural History Museums Council Block species and notes on their biology. Insecta Grants Program. Thanks are extended for Mundi 0421: 1–46. this support. Otto, R. L. 2016. The False Click Beetles (Cole- optera: Eucnemidae) of Laos. Entomologica Basiliensia et Collectionis Frey 35: 181–427.
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The Effects of Soil Moisture, Soil Texture, and Host Orientation on the Ability of Heterorhabditis bacteriophora (Rhabditida:Heterorhabditidae) to Infect Galleria mellonella (Lepidoptera:Pyralidae) Suzanne M. Hartley1,2* and John R. Wallace1* 1Department of Biology, Millersville University, Millersville, Pennsylvania 17551. 2Department of Forestry and Environmental Resources, North Carolina State University, 2800 Facuette Drive, Raleigh, North Carolina 27607.
Abstract Entomopathogenic nematodes (EPN) demonstrate potential as a biological control for soil dwelling insects. However, edaphic factors, such as soil moisture and texture impact the ability of EPN to find host. The objectives of this study were to examine the effects of soil texture and moisture on 1) the infection rate of Galleria mellonella L. by EPN and; 2) the ability of Heterorhabditidae bacteriophora (Poinar) to move through the soil to find a host at different orientations. Soil textures consisted of sand, a sand/silt/peat mixture, and a silt/ peat mixture at 50% and 100% moisture. An ANOVA was used to evaluate infection rates and EPN movement. Both soil moisture (p < 0.05) and texture (p < 0.05) had significant effects on nematodes infection rates of G. mellonella. Texture, moisture, and host orientation did not significantly affect (p > 0.05) the ability of EPN to find a host. While EPN were able to find a host within a variety of soil types, soils that held more water had higher infection rates than soils that held less water, suggesting that moisture may be a key component in facilitating infection by EPN. By understanding the factors that influence the ability of EPN to find and infect a host, improved bio-control programs using EPN may be developed. Keywords: Soil moisture, soil texture, host orientation, nematode infection, Galleria mellonella
Insect pests are the largest contributor and Castane 1998). With more than 90% to crop loss and account for 15% reduction of extant insect species having life history in potential crop yields on the world’s eight stages in the soil, entomopathogenic nema- major crops (Yudelman et al. 1998). Losey todes show potential for biological control in and Vaughan (2006) estimate these losses to agricultural systems (Hominick 2002). be more than $18.7 billion dollars annually. Entomopathogenic nematodes (EPN) Despite an increased use of pesticides, the are found on every continent, except for number of crops lost to pest damage has Antarctica and have been used as biological increased since 1965. This phenomenon has controls for numerous soil dwelling agricul- led to an increased interest in identifying bio- logical control agents to add to the arsenal of tural pests and invasive species (Peters and tools utilized in integrated pest management Ehlers 1994, Hominick 2002, Lewis et al. (Yudelman et al. 1998). Natural enemies, 2006, Campos-Herrera et al. 2007). Previous like entomopathogenic nematodes, can con- studies have shown that EPN show promise trol pest populations through parasitism for suppressing Dipteran, Coleopteran, and thus regulating the spread and impact of Lepidopteran agricultural pests (Peters and pest species (Hajek 2004). However, in the Ehlers 1994; Lacey and Unruh 1998, Lo- case of invasive agricultural pest species in la-Luz et al. 2005). EPN infect a host during novel environments, natural enemies may a free-living infective juvenile (dauer) stage be absent or scarce (Lockwood et al. 2007). when they crawl into a host via any possible Identifying the potential biological control opening such as the mouth, anus, spira- agents, as well as their presence, abundance, cles, and even intersegmental membranes and effectiveness, becomes necessary when (Bedding and Molyneux 1982, Kaya et al. considering integrated pest management 1993). Once inside, the infected juveniles for invasive agricultural pests (Riudavets release symbiotic enteric bacteria, and the larval host dies via septicemia within 24–48 hours (Molyneux and Bedding 1984, Ansari *Corresponding authors: (e-mail: smhartle@ncsu. and Butt 2011). EPN reproduce inside the edu and [email protected]) cadaver for two to three generations before
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leaving the cadaver en masse to seek a new Glazer 2015). This downward movement host (Shapiro-Ilan et al. 2006). However, the toward soil moisture could impact the ability effectiveness of EPN has varied dramatically H. bacteriophora to successfully find a host, from study to study depending on soil charac- depending on the soil texture, moisture, and teristics, species, agricultural management, host orientation. and competition with native EPN (Georgis The purpose of this study was to iden- et al. 2006, Campos-Herrera et al. 2008). tify the optimum conditions of soil texture, One approach to understanding how EPN soil moisture, time, and host orientation can be utilized to manage soil dwelling pests in which H. bacteriophora and its associ- is to fully investigate the influence of soil ated enteric bacteria (Photorhabdus spp.) conditions and host orientation on the host causes the greatest mortality on Galleria seeking success of EPN. mellonella L. (Lepidoptera: Pyralidae). This Soil moisture, texture, pH, organic study was part of a larger study examining matter, and bulk density may affect the the potential use of EPN for regulating an survival and host seeking success of EPN invasive agricultural pest, Tipula paludosa (Gruner et al. 2007). EPN require a thin film Meigan. Since the invasive pest could not of water to navigate through the soil to find be obtained, G. mellonella was used as a a host. The relationship of soil texture and model for control of invasive agricultural organic matter in determining the porosity pests. Galleria mellonella have been used and water-holding capacity of a soil is crucial as a host in numerous EPN studies since to the survival and efficacy of EPN. If the soil they are easily raised in captivity and are is too dry, there may not be a continuous film very susceptible to dauers (Woodring and of water to allow for nematode movement Kaya 1988). There were two experiments (Koppenhöfer and Fuzy 2006, Lewis et al. conducted to address the purpose of this 2006). Concomitantly, interstitial space, the study. The first experiment examined the space between soil particles, is essential for effects of soil texture and moisture on EPN providing oxygen and allowing EPN to move location and infection of G. Mellonella, and through soil (Kung et al. 1990, Koppenhöfer the second experiment examined the effects et al. 1995) For example, sand provides of soil texture, moisture, time, and host ori- interstitial space for movement and oxygen entation on the rate EPN move through the but lacks water retention. On the other soil and infect a host. hand, clay lacks interstitial space and can easily become anoxic, but has a high capac- Methods ity for retaining water (Meats 1972, Thien and Graveel 1997). Therefore, it is possible Experimental Design. Two labora- that a tradeoff between soil texture and soil tory experiments were conducted to under- moisture level may create the ideal sub- stand the role of soil texture, soil moisture, strate for EPN movement and host seeking and host orientation on host infection by H. success. While other studies have examined bacteriophora. In both experiments, three the effects of different soil textures at the different soil textures at two soil moisture same moisture level, few have compared soil levels were used to form a total of six soil textures at different moisture levels with treatments. For the three soil texture treat- regards to host seeking success (Molyneux ments, soil was collected near a stream and Bedding 1984, Kung and Gaugler 1991, using a shovel in Millersville, PA on 19 Koppenhöfer and Fuzy 2006). February 2013. Play sand was purchased Foraging strategies of EPN exist on a at a local hardware store. The sand and soil continuum from ambush to cruising foragers were transported to the laboratory where (Salame and Glazer 2015). Heterorhabaditis both were dried in an oven at 93ºC, ground bacteriophora (Poinar) is a cruiser species through a two-millimeter sieve, and auto- of EPN that currently can be purchased claved for 40 minutes at 121ºC. Soil texture commercially as biological control agent was determined by using the hydrometer (Shapiro-Ilan et al. 2002). Compared to oth- method as described by California Depart- er EPN species, H. bacteriophora is better ment of Pesticide Regulation (2005). Fifty adapted to finding more sedentary insects grams of soil were mixed with 250 mL of that live deep in the soil profile where the distilled water and 100 mL of sodium hex- soil is moist (Campbell et al. 1996, Salame ametaphosphate and allowed to soak for 24 and Glazer 2015). However, Heterorhabditid hours. The soil mixture was homogenated populations have also demonstrated poor with a “blend” setting on a blender (Hamilton desiccation tolerance when compared to Beach Blendmaster®, Glen Allen, Virginia) Steinernematids, the second major family for one minute before being poured into a of EPN (Surrey and Wharton 1995, Liu and 1000mL sedimentation cylinder. Distilled Glazer 2000). To escape desiccation in drier water was added to bring the volume to one soils, H. bacteriophora has been found to liter. The homegenated soil was mixed vig- migrate deeper into the soil (Salame and orously with a plunger for one minute and a
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Figure 1. Assembly of experimental chambers A) Parafilm®, B) fiberglass screening, C) piece of PVC, D) Galleria mellonella larva, E) PVC portion containing G. mellonella, F) PVC portions containing G. mellonella and soil, G) assembled chamber.
hydrometer reading was taken 30 seconds, for peat/silty loam (Fig. 1). On one end of 60 seconds, 90 minutes, and 24 hours after the pipe, a cotton cloth was secured to keep mixing. Using a set of equations as described the soil within the tube and distilled water by the California Department of Regulation was added until water was seen dripping in their standard operating procedure for from the tube. The soil was allowed to drain using a soil hydrometer, the soil texture for 24 hours before weighing to determine was determined to be a silty loam, 64% silt, the water volume by weight. The amount 26% clay, 10% sand (California Department of water the soil contained after 24 hours of Regulation 2005). Sphagnum peat moss, was used to determine field capacity or the a common horticultural potting media, was amount of water the soil can hold after any added to the silty loam as proxy for organic excess water has been drained (Thien and matter in a 1:1 ratio to create a silt/peat soil Graveel 1997). Henceforth, in this study mixture (Ansari and Butt 2011). Several we define soil at field capacity to be 100% other studies have also used peat as a me- saturation. For the following experiments, dium when examining the efficacy of EPNs the necessary amount of water was added to (Lola-Luz et al. 2005, Lola-Luz and Downes each soil texture type to create two moisture 2007, Ansari et al. 2008, Ansari et al. 2010, levels: 100% and 50% saturation. Ansari and Butt 2011). For a second soil tex- Forty-five mL of soil was placed in ture, sand, silty loam, and peat were added 100 mm×15 mm petri dishes and replicated in a 1:1:1 ratio to create a sand/silt/peat soil three times for each soil texture and mois- mixture. Finally, the third soil texture was ture level. EPN purchased from ARBICO 100% sand obtained from a garden store. Organics were introduced into the petri To determine soil moisture, a 15cm dishes by applying 2 mL of water contain- long PVC pipe with a 5cm diameter was ing approximately 45,000 individuals of H. filled vertically with a known weight of bacteriophora to the surface of the soil. The dried soil; 450 grams for sand, 250 grams resulting dauer density was approximately for sand/peat/silty loam, and 150 grams 1,000 dauers per cm3 of soil. To estimate the
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number of dauers, a solution of EPN was each time period, G. mellonella were checked placed into distilled water and stirred on a for infection. Galleria mellonella larvae that stirring plate. Two microliters of the solution were still alive at the end of the time period were subsampled and the nematodes were were rinsed with distilled water and quar- counted under a dissecting microscope. This antined for three days to confirm whether step was repeated an additional two times or not the larvae had been infected by EPN. and the three counts of nematodes were Statistical Analysis. The statistical averaged to estimate the concentration of significance of the two experiments was the nematodes in the solution. After EPN determined by two separate ANOVAs in application, 10 sixth instar G. mellonella Minitab (Minitab 17 Statistical Software were placed with forceps into the petri dish- 2010). Differences were considered signifi- es and replicated three times for every soil cant at p ≤ 0.05. treatment. G. mellonella in Petri dishes were checked daily for nematode infection and Results infected individuals were removed. Cadavers infected by H. bacteriophora were identified In the first laboratory experiment by the red color and flaccid body caused by examining the effects of soil texture and H. bacteriophora’s symbiotic enteric bacte- moisture on infection rate of G. mellonella ria (Koppenhöfer 2008). Any G. mellonella by H. bacteriophora, a general linear model larvae that died of causes other than H. showed that there was a significant differ- bacteriophora infection were removed and ence between soil texture and soil moisture replaced by live G. mellonella larvae. on the number of G. mellonella larvae in- A second laboratory experiment was fected by H. bacteriophora. After six days, conducted to determine the rate that EPN G. mellonella larvae in silt/peat soil had a moved through the soil types to find a host suffered higher mortality (Fs = 15.50; df = 2; at different orientations, soil moistures and P < 0.05) than larvae in sand/silt/peat soils soil textures. Each treatment of host orien- or pure sand soils. Soil moisture also had a tation, soil moisture, soil texture and time significant effect (Fs = 5.54; df = 1; P < 0.05) there was replicated five times. The three soil effect G. mellonella mortality. Soils that types described above were mixed with the were at 100% moisture had more infected G. distilled water to create the two saturation mellonella larvae than sites with 50 % soil levels (50% and 100%) and placed into PVC moisture (Fig. 2). There was no significant tubes like those created by Ansari and Butt interaction between soil moisture and soil (2011). PVC pipe (approximately 1.25 cm in texture (Fs = 1.50; df = 2; P > 0.05). diameter) was cut into two-centimeter long In the second experiment evaluating segments. At one end of the PVC segment, the effects of time, host orientation, soil 1.5 mm×1.5 mm fiberglass screening was texture and moisture, a general linear model installed to keep the G. mellonella larva showed that only time had a significant (Fs from moving through the length of the tube = 4.64; df = 2; P < 0.05) effect on the number (Fig. 1). Each end was sealed with a double of G. mellonella killed by H. bacteriophora. ® layer of perforated Parafilm to prevent the At 24 hours, infective juveniles were able to nematodes from escaping but to allow for air move the length of the tube (2 cm) to find and exchange (Ansari and Butt 2011). The PVC infect the 17% of the G. mellonella larvae, at tube was filled with approximately 10 cm3 of 72 hours 33% of the larvae were infected, and moistened soil and placed at approximate 23º at 96 hours 78% of the larvae were infected C for 24 hours to allow a gradient of host cues (Fig. 3). Variations in host orientation (Fs (i.e., carbon dioxide) to accumulate (Lewis = 0.33; df = 2; P > 0.05), soil texture (Fs = 2002). Heterorhabditis bacteriophora are 1.77; df = 2, P > 0.05), and soil moisture (Fs = mobile active cruisers with a strong response 0.43; df = 1; P > 0.05) did not have significant to host cues (Kaya and Gaugler 1993). Heter- effects on the movement of EPN through the orhabditis bacteriophora infective juveniles soil to infect a host. were mixed in distilled water to create a concentration of 5 infective juveniles/µL. Discussion One hundred microliters of the nematode solution (approximately 500 nematodes) In order for EPN to move through the was applied to the soil surface with a 1000 soil and find a host, they require oxygen and µL micropipette. The approximate density a thin film of water (Ansari and Butt 2011). of injective juveniles was 50 dauers per cm3 While sand may provide greater interstitial of soil. The tubes were allowed to sit for 24, space for EPN to move than silt, sand has 72, and 96 hours to allow for nematode move- a lower water holding capacity than silt or ment. Tubes were placed in three different clay soils (Saxton and Rawls 2006). In our orientations; horizontal, vertical with the G. first experiment, the addition of peat moss, mellonella larvae on top, and vertical with which is characterized by large pieces of the G. mellonella larvae on the bottom. After organic debris, may have increased both
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Figure 2. Average number of Galleria mellonella larvae infected by Heterorhabditis bacteriophora after six days across three types of soil mixture.
interstitial space and water holding capac- soil pores to facilitate the movement of H. ity (Portillo-Aguilar et al. 1999). Soils rich bacteriophora through the soil. Future work in organic matter retain more moisture will involve the measurement of interstitial compared to soils lower in organic matter spaces within different soil types. (Saxton and Rawls 2006). The soils con- Given the results of our first exper- taining peat (peat/silty and sand/peat/silty iment, we would have expected to see a loam) had significantly higherG. mellonella significant difference in soil moisture and infection rates than pure sand. Unlike most texture on the ability of nematodes to find other studies that have shown that EPN a host; instead soil moisture and texture efficacy was higher in sandier soils (Kung were not significant. One explanation for et al.1990, Campos-Herrera et al. 2008), this these contradicting results could be the dif- study demonstrated that EPN were more ference in EPN concentration between the easily infected in soils with higher clay and two experiments. In the first experiment, organic material contents. Similar to our there were 1,000 dauers/cm3, whereas, in findings, Toledo et al. (2009) found improved the second experiment there were 50 dauers/ efficacy of EPN in sand-clay soils rather cm3. A second explanation for the difference than in pure sand. Our study also found between the two experiments is the effect of that soils with 100% moisture had greater time. EPN were given six days to find a host G. mellonella larvae infection rate than soils in the first experiment, while the maximum at 50% moisture, which may suggest that time in the second experiment was four days. soil moisture may be more important than It could be that the lower density of EPN and soil texture alone. Molyneux and Bedding the shorter time frame of experiment masked (1984) also demonstrated that moisture to difference is soil texture and soil moisture. be the most important factor in their study A third explanation for the difference comparing soil textures and moisture. How- between the two experiments could be soil ever, tradeoffs between interstitial space and compaction (bulk density). In the first -ex soil moisture may still exist. A soil with high periment, the soil was scooped into the petri organic matter, such as peat, and high field dish and very little compaction occurred. capacity may have more interstitial space However, in the second experiment, the soil required for successful host encounters for had to be stuffed into the PVC tube. The EPN. Peat moss also lowers bulk density (a process of filling the tube could have led to a measure of compaction) to allow for larger higher bulk density which lowered intersti-
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Figure 3. Average number of Galleria mellonella killed when nematodes traveled 2 cm to find a host at three different time intervals (24, 72, 96h).
tial space resulting in poorer efficacy of the time, a more holistic approach in evaluating nematodes. A study by Portillo-Aguilar et the effects of soil texture, moisture, bulk al. (1999) found that EPN in silty clay loam density, pH, and temperature is needed soil at a high bulk density were less effective determine the interactions between these at moving through 8 cm of soil to infect G. parameters and their impact on each EPN mellonella larvae. Wallace (1958) found that species’ efficacy. nematodes moved best when the size of the In order for H. bacteriophora to func- pores (interstitial space) found within the tion as an effective biocontrol agent for soil was approximately equal to the size of agricultural pests, it is important that they their body. Soils with higher bulk density are able to quickly find, kill, and reproduce may have pores that are smaller than the inside the host (Peters and Ehlers 1994). size of the EPN. While we did not measure The second laboratory experiment indicated bulk density, we speculate that the process that within 24 hours it was possible for H. of packing the soil into the tubes for the bacteriophora infective juveniles to travel second experiment reduced the size of the two centimeters to find and infect a host. interstitial space relative to experiment and However, our study found at 48 and 96 hours, prevented H. bacteriophora dauers (diameter significantly more of theG. mellonella hosts 25µm) from moving freely through the soil had been infected by H. bacteriophora than (Portillo-Augilar et al. 1999, Klingen and at 24 hours. Hence, as more time passed, a Haukeland 2006). We speculate that the higher rate of G. mellonella infection by H. difference between the two experiments may bacteriophora occurred. While H. bacterio- provide new information as to how minor phora were able to reach G. mellonella larvae changes in the environmental conditions can 2 cm within 24 hours, a larger proportion influence the success of entomopathogenic of the G. mellonella were infected after 96 nematodes to move through the soil to find hours. Several factors may be contributing a host. Koppenhöfer and Fuzy (2006) also to this difference, a 96 hour interval did pro- found that it was difficult to make conclu- vide more time for host cues to accumulate sions when comparing different soils due for the EPN to detect and pursue, it may to the conglomeration of parameters within also allow for more EPN to enter the host each soil type. While previous studies have and more time for the bacteria to kill the attempted to address one soil parameter at a host via septicemia. Previous research has
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indicated that small amounts of nitrogen Literature Cited (<0.16mg) released from H. bacteriopho- ra-infected hosts during the early stages of Ansari, M.A., F.S. Shah, and T.M. Butt. 2008. infection can attract conspecific dauers to the Combined use of entomopathogenic nema- host. However, when nitrogen is released at todes and Metarhizium anisopliae as a new higher levels (>0.16mg), it leads to repulsion approach for black vine weevil Otiorhynchus of nematodes away from the infected host sulcatus (coleopteran: Curculionidae) control. Entomologia Experimentalis et Applicata (Shapiro et al. 2000). Our finding empha- 129:340–347. sizes the importance of applying EPN in the appropriate quantities and during the Ansari, M.A., F.S. Shah, and T.M. Butt. 2010. ideal environmental conditions (i.e., mois- The cold tolerant entomopathogenic nema- ture, temperature, pH, bulk density, and tode Steinernema kraussei and Metarhizium texture) to control pest hosts. Given the right anisopliae work synergistically in controlling parameters, we found that H. bacteriophora overwintering larvae of the black vine nematodes were able to survive for 96 hours weevil. Journal of Ecological Entomology to infect a host at least 2 cm away (in any 98:1884–1889. direction vertical or horizontal). Ansari, M.A. and T.M. Butt. 2011. Effect of potting media on the efficacy and dispersal of We hypothesized that orientation of entomopathogenic nematodes for the control EPN in respect to the host could influence of black vine weevil, Otiorhynchus sulcatus their ability to find a host. Previous studies (Coleoptera: Curculionidae). Biological Con- have examined the ability of EPN to move trol 58:310–318. vertically or horizontally to find a host crawl- ing on the soil surface (Toledo et al. 2009, Bedding, R. and A. Molyneux. 1982. Penetra- Ansari and Butt 2011), but none compared tion of insect cuticle by infective juveniles of Heterorhabditis spp. (Heterorhabditidae: the effects of host orientation on EPN infec- Nematoda). Nematologica 28:354–359. tions. However, this study found that there was no significant difference in the infection California Department of Pesticide Regula- rate when EPN move horizontally, vertically tion. 2005. Standard Operating Procedure: (downwards), and vertically (upwards) to Procedure for determining soil particle size find a host. These results suggest H. bacte- using the hydrometer method. Available from riophora were able to seek out their host in http://www.cdpr.ca.gov/docs/emon/pubs/sops/ any direction within the soil. meth004.pdf (accessed May 2013). To be an effective biological control Campbell, J.F., E. Lewis, and F. Yoder. 1996. Entomopathogenic nematode (Heterorhabdit- agent, it is imperative to know the environ- idae and Steinernematidae) spatial distribu- mental conditions wherein H. bacteriophora tion in turfgrass. Parasitology 113:473–82. are most successful in finding and infecting the host. Our results are consistent with Campos-Herrera, R., M. Escuer, S. Laber- other studies that suggest EPN are most ador, L. Roberson, L. Barrios, and C. effective at finding and infecting hosts in Gutiérrez. 2007. Distribution of the en- soils that are high in water holding capacity, tomopathogenic nematodes from La Rioja such as soils with high organic material and (Northern Spain). Journal of Invertebrate clay content (Molyneux and Bedding 1984). Pathology 95:125–139. Further studies, in the field and laboratory, Campos-Herrera, R., J.M. Gómez-Ros, M. are needed to more closely evaluate the Escuer, L. Cuadra, L. Barrios, and C. complex interactions that maybe occurring Gutiérrez. 2008. Diversity, occurrence, and across multiple soil parameters to impact life characteristics of natural entomopatho- the efficacy ofH. bacteriophora. genic nematode populations from La Rioja (Northern Spain) under different agricultural management and their relationships with Acknowledgments soil factors. Soil Biology and Biochemistry This research would not have been 40:1474–1484. possible without our introduction to ento- Georgis, R., A.M. Koppenhöfer, L.A. Lacey, mopathogenic nematodes through Dr. Mat- G. Belair, L.W. Duncan, P.S. Grewal, M. thew J. Petersen and Cornell University’s Samish, L. Tan, P. Torr, and R.W.H.M. Summer Scholar program in Entomology. VanTol. 2006. Successes and failures in the The funding for this research came from use of parasitic nematodes for pest control. Millersville University’s Neimeyer Hodgson Biological Control 38:103–123. and Biology Student Investigator grants. We Gruner, D.S., K. Ram, and D.R. Strong. 2007. also thank Dr. Daniel Yocom for the use of Soil mediates the interaction of coexisting laboratory equipment and space. entomopathogenic nematodes with an in-
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sect host. Journal of Invertebrate Pathology genic Nematology. CABI Publishing, New 94:12–19. York, NY. Hajek, A.E. 2004. Natural enemies: an intro- Lewis, E.E., J. Campbell, C. Griffin, H. Kaya, duction to biological control. Cambridge and A. Peters. 2006. Behavioral ecology University Press, Cambridge, UK. of entomopathogenic nematodes. Biological Control 38:66–79. Hominick, W.M. 2002. Biogeography. pp. 115–145. In R. Gaugler (ed), Entomopatho- Liu, Q.-Z. and I. Glazer. 2000. Factors affecting genic Nematology. CABI Publishing, New desiccation survival of the entomopathogenic York, NY. nematodes, Heterorhabditis bacteriophora HP88. Phytoparasitica 28:331–340. Kaya, H.K., R.A. Bedding, and R.J. Akurst. 1993. An overview of insect-parasitic and Lockwood, J.L., M.F. Hoopes, and M.P. Mar- entompathogenic nematodes. pp. 1–10. In chetti. 2007. An introduction to invasion R. Bedding, R, Akhust, and H. Kaya (Eds.), ecology. pp. 1–18. In J.L. Lockwood, M.F. Nematodes and the Bioloigcal Control of Hoopes, and M.P. Marchetti (eds.) Invasion Insect Pests. CSIRO, East Melbourne, Aus- Ecology. Blackwell, Malden, MA. tralia. Lola-Luz, T., M. Downes, and R. Dunne. 2005. Kaya, H.K. and R. Gaugler. 1993. Entomo- Control of black vine weevil Otiorhynchus pathogenic Nematodes. Annual Review of sulcatus (Fabricus) (Coleoptera: Curculioni- Entomology 38:181–206. dae) in grow bags outdoors with neamtodes. Agricultural Forest Entomology 7:121–126. Klingen, I. and S. Haukeland. 2006. The soil as a reservoir for natural enemies of pest Lola-Luz, T. and M. Downes. 2007. Biological insects and mites with emphasis on fungi control of black vine weevil Otiorhynchus and nematodes. pp. 145–211. In J. Eilenberg sulcatus in Ireland using Heterorhabditis and H.M.T. Hokkanen (eds), An ecological megidis. Biological Control 40:314–319. and societal approach to biological control. Losey, J.E. and M. Vaughn. 2006. The economic Springer, Dordrecht, The Netherlands. value of ecological services provided by in- Koppenhöfer, A.M., H.K. Kaya, and S.P. sects. Bioscience 56: 311–323. Taormino. 1995. Infectivity of entomopatho- Meats, A. 1972. The effect of soil flooding on genic nematodes (Rhabditida:Sternematidae) the survival and development of the eggs of at different depths and moistures. Journal of Tipula oleracea L. and T. paludosa Meigen Invertebrate Pathology 65:193–199. (Diptera: Tipulidae). Journal of Entomology Koppenhöfer, A.M. and E.M. Fuzy. 2006. Effect Series A, General Entomology 46:99–102. of soil type on infectivity and persistence of Minitab 17 Statistical Software. 2010. Quality the entomopathogenic nematodes Steiner- Companion 3 by Minitab. Minitab, Inc., State nema scarabaei and Heterorhabditis bacte- College, PA www.minitab.com riophora. Journal of Invertebrate Pathology Molyneux, A.S. and R.A. Bedding. 1984. In- 92:11–22. fluence of soil texture and moisture on the Koppenhöfer, A.M. 2008. Microbial control infectivity of Heterorhabditis sp. and Steiner- of turfgrass Insects, pp. 281–298. In M. nema glaseri for larvae of the sheep blowfly, Pessarakli (ed.) Handbook of turfgrass man- Lucilia cuprina. Nematologica 30:358–365. agement and physiology. CRC Press, Boca Peters, A. and R.U. Ehlers. 1994. Susceptibility Raton, FL. of leatherjackets (Tipula plaudosa and Tip- Kung, S.P., R, Gaugler, and H.K. Kaya. 1990. ula oleracea; Tipulidae; Nematocera) to the Soil type and entomopathogenic nematode entomopathogenic nematode Steinernema persistence. Journal Invertebrate Pathology feltiae. Journal of Invertebrate Pathology 55:401–406. 63:163–171. Kung, S.P. and R. Gaugler. 1991. Effects of Portillo-Aguliar, C., M.G Villani, M.J. Tau- soil temperature, moisture, and relative ber, C.A. Tauber, and J.P. Nyrop. 1999. humidity on entomopathogenic nematode Entomopathogenic nematode (Rhabditidia: persistence. Journal of Invertebrate Pathol- Heterorhabditidae and Steinernematidae) ogy 57:242–249. response to soil texture and bulk density. Lacey, L.A. and T.R. Unruh. 1998. Entomo- Population Ecology 28:1021–1035. pathogenic nematodes for control of codling Riudavets, J. and C. Castane. 1998. Identifi- moth,Cydia pomonella (Lepidoptera: Tortri- cation and evaluation of native predators of cidae): effect of nematode species, concentra- Frankliniella occidentalis (Thysanoptera: tion, temperature, and humidity. Biological Thripidae) in the Mediterranean. Environ- Control 13:190–197. mental Entomology 21:86–93. Lewis, E.E. 2002. Behavioral Ecology, pp. Salame, L. and I. Glazer. 2015. Stress avoid- 205–220. In R. Gaugler (ed.) Entomopatho- ance: vertical movement of entomopathogenic
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nematodes in response to soil moisture gra- Thien, S.J. and J.G. Graveel. 1997. Laboratory dient. Phytoparasitica 43:647–655. manual for soil science: agricultural and Saxton, K.E. and W.J. Rawls. 2006. Soil wa- environmental principles. McGraw-Hill, ter characteristic estimates by texture and Boston, MA. organic matter for hydrologic solutions. Toledo, J., T. Williams, P. Concepción, P. Soil Science Society of America Journal Liedo, J.F. Valle, and J.E. Ibarra. 2009. 70:1569–1578. Abiotic factors affecting the infectivity to Shapiro, D.I., E.E. Lewis, S. Paramasivam, Steinernema carpcapsae (Rahbditida: Stein- and C.W.McCoy. 2000. Nitrogen parti- ernematidae) on larvae of Anastrepha oblique tioning in Heterorhabditis bacteriophora– (Diptera: Tephritidae). Biocontrol Science infected hosts and the effects of nitrogen on and Technology 19:887–898. attraction/repulsion. Journal of Invertebrate Pathology 76:43–48. Wallace, H.R. 1958. Movements of eelworms II, a comparative study of the movement in Shapiro-Ilan, D.I., D.H. Gouge, and A.M. soil of Heterodera schachlii Schmidt and of Koppenhöfer. 2002. Factors affecting Ditylenchus dipsaci (Kuhn) Filipjev. Annuals commercial success: case studies in cotton, of Applied Biology 46: 86–94. turf and citrus. In R. Gaugler (ed.) Entomo- pathogenic Nematology. CABI Publishing, Woodring, J.L. and H.K. Kaya. 1988. Stein- New York, NY. ernematid and Heterorhabditid nematodes: a handbook of biology and techniques. Shapiro-Ilan, D.L., RJ. Stuart, and CW. McCoy. 2006. A comparison of entomo- Southern Cooperative Bulletin 331, Arkan- pathogenic nematode longevity in soil under sas Agricultural Experimental Stations. laboratory conditions. Journal of Nemotology Fayetteville, AR. 38:119–129. Yudelman, M., A. Rattam, and D. Nygaard. Surrey, M.R. and D.A. Wharton. 1995. Desic- 1998. Pest Management and Food Produc- cation survival of the infective larvae of the tion: Looking to the Future. Washington insect parasitic nematode, Heterorhabditis (DC): International Food Policy Research In- zealandica Poinar. International Journal of stitute. Food.Agriculture, and Environment Parasitiology 25:407–412. Discussion Paper 25.
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Insect (Arthropoda: Insecta) Composition in the Diet of Ornate Box Turtles (Terrapene ornata ornata) in Two Western Illinois Sand Prairies, with a New State Record for Cyclocephala (Coleoptera: Scarabaeidae) Reese J. Worthington1*, E. R. Sievers2, D. B. Ligon2, and P. K. Lago1 1Department of Biology, University of Mississippi, University, MS 38677 2Department of Biology, Missouri State University, Springfield, MO 65897
Abstract A study of fecal samples collected over a two-year period from juvenile ornate box turtles (Terrapene ornata ornata Agassiz) revealed diets consisting of six orders of insects representing 19 families. Turtles were reared in captivity from eggs harvested from local, wild populations, and released at two remnant prairies. Identifiable insect fragments were found in 94% of samples in 2013 (n = 33) and 96% in 2014 (n = 25). Frequency of occurrence of insects in turtle feces is similar to results reported in previous studies of midwestern Terrapene species. A comparison of insect composition presented no significant difference between release sites. There is no significant difference in consumed insect species between turtles released into or outside of a fenced enclosure at the same site. Specimens of Cyclo- cephala longula LeConte collected during this study represent a new state record for Illinois. Keywords: Ornate box turtle, head-starting, conservation, feces, Cyclocephala longula
The ornate box turtle, Terrapene or- Lovich 2009). Insects make up an important nata ornata Agassiz, is a prairie-dwelling portion of Terrapene carolina carolina L. diet species that has experienced population in Illinois and Pennsylvania, ranging from 60 declines, especially near the northern edge to 92% frequency of occurrence in digestive of its range in Wisconsin and Illinois (Levell tract examinations (Surface 1908, Klimstra 1997, Conant and Collins 1998, Dodd 2001, and Newsome 1960). Whereas Terrapene car- Redder et al. 2006, Strickland et al. 2013). olina bauri Taylor fecal remnants from the Habitat loss and fragmentation appear to be Florida Keys had an invertebrate occurrence leading causes of T. ornata ornata decline, of 10.4% (Platt et al. 2009), a study of T. especially in the midwestern United States, where agricultural expansion and land de- ornata ornata from Kansas found insects in velopment have left less than 0.01% of the 100% of 23 turtle stomachs examined (Leg- native prairie habitat (White 1978, Samson ler 1960), and a study of Terrapene ornata and Knopf 1994, Corbett and Anderson luteola H.M. Smith & Ramsey from Texas 2006). Species extirpation due to the loss found insects in 100% of 14 turtles sampled of prairie habitat continues to be a major (Platt et al. 2012). However, such ubiquitous concern. Currently, 55 grassland species consumption of insects may vary seasonally are threatened or endangered in the United or geographically; the stomach contents of States (Samson and Knopf 1994). Ornate five T. ornata ornata collected in Illinois box turtles were listed in Appendix II of the contained partially digested plant material Convention on International Trade of En- but no insect or other animal material (Cahn dangered Species of Wild Flora and Fauna 1937). A dietary analysis of insect fragments in 1994 still remaining on the list to-date in fecal samples of ornate box turtles was (USFWS 1995, CITES 2017), and are pro- conducted in this study to ascertain if, in tected in Colorado, Illinois, Iowa, Indiana, addition to habitat loss, limited diversity in Nebraska, Kansas, Wisconsin (Redder et al. their diet could be exacerbating population 2006), and now South Dakota and Wyoming. declines in Illinois. Diet studies are essential Terrapene spp. are dietary generalists to understanding the ecology of an organism and frequently consume insects and other (Rosenburg and Cooper 1990) and help to invertebrates, carrion, vertebrates, and a inform reintroduction efforts as turtle diet wide range of plants and fungi (Ernst and directly affects energy allotment, which in turn influences reproductive rates, growth, and survival (Sloan et al. 1996, Ford and *Corresponding author: ([email protected]) Moll 2004, Platt et al. 2009).
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This research occurred in conjunction prickly pear cactus (Opuntia humifusa Raf.), with an on-going T. ornata ornata rein- aromatic sumac (Rhus aromatica Ait.), and troduction effort conducted by the Upper spiderwort (Tradescantia ohiensis Raf.). A Mississippi River National Wildlife and Fish strip approximately 10 m wide immediately Refuge. In 2008, the United States Fish and bordering the river is dominated by a variety Wildlife Service (USFWS) initiated efforts to of deciduous trees, black raspberry (Rubus reestablish a viable population of ornate box occidentalis L.), and poison ivy (Toxicoden- turtles on a patch of remnant prairie located dron radicans L.). Isolated raspberry patches at a former army depot that was decommis- and eastern red cedar (Juniperus virginiana sioned in 2000. The project used juveniles L.) are scattered throughout the study site that were hatched from eggs collected from (Bowen et al. 2004, Refsnider et al. 2012, Thomson Sand Prairie, a nearby prairie also Strickland et al. 2013). The site is bordered managed by USFWS, and reared in captivity by the Mississippi River to the west, a rail- prior to reintroduction, a method termed road right-of-way containing remnant prairie head-starting. In 2010, a population viability to the east, a residential development to the study concluded that the ornate box turtle north, and a pine plantation to the south, population at Thomson Sand Prairie could which separates Thomson Sand Prairie from sustain the harvest of eggs for a head-start another remnant sand prairie, Thomson Ful- program to repopulate Lost Mound Sand ton Sand Prairie. A narrow corridor of prairie Prairie (Strickland et al. 2013). However, to associated with the railroad right-of-way and ameliorate the potential negative impact of a public bike path connects Thomson Sand removing eggs, a subset of hatchlings was Prairie and Thomson Fulton Sand Prairie. released at Thomson Sand Prairie annual- Lost Mound Sand Prairie (LMSP) is a ly. Like those at Lost Mound Sand Prairie, 1,619-ha unit in northwestern Carroll and these turtles were radio transmittered and southwestern Jo Daviess counties on the for- monitored throughout their active season. mer Savanna Army Depot, and is the largest A dietary analysis of insects recovered remnant sand prairie in Illinois (Ebinger et from fecal samples of reintroduced turtles al. 2006, Strickland et al. 2013). The area was conducted. This is the first dietary is bordered on the west by the Mississippi analysis of T. ornata ornata using non-lethal River, on the east by railroad tracks, on the methods, which is essential for determining north by a campground and day use area dietary and ecological demands in species managed by the U.S. Army Corps of Engi- of conservation concern. The class Insecta neers, and on the south by privately owned served as the focus of this analysis and was semi-developed sand prairie. Ornate box tur- selected due to the indigestible nature of tles were once common at LMSP, but decades the chitinous exoskeleton, which enabled of military activity nearly extirpated them identification of organisms via fragmented from the area (McCallum and Moll 1994). remains. The goal of this dietary analysis LMSP is jointly managed by the USFWS and was tripartite: 1) to determine if head-start- Illinois Department of Natural Resources ed turtles displayed different insect dietary and contains sand prairie, sand dune, sand composition compared to results shown in savanna, and blowout communities dominat- previous studies of wild-caught terrestrial ed by prairie junegrass (Koeleria macrantha Terrapene species, 2) identification of insect (Ledeb.) Schult.) and little bluestem with fragments to compare species composition interspersed patches of prickly pear cactus, between reintroduction sites, and 3) to deter- aromatic sumac, prairie redroot (Ceanothus mine if soft-release enclosure reintroductions herbaceous Raf.), and spiderwort. had a similar diet composition to turtles hard-released without a protective fenced Methods. Seventeen ten-month-old enclosure at Lost Mound Sand Prairie. head-started turtles were released in June 2013: five were released at the TSP donor site, six were released inside of the soft- Materials and Methods release enclosure at LMSP (LM IN), and Study Site. Research was conducted six were released outside the enclosure (LM at two units of the Upper Mississippi River OUT). Nine additional head-started turtles National Wildlife and Fish Refuge, both of from the 2013 cohort were released in June which are located on the eastern bank of the 2014, with three added to each treatment. Mississippi River. Thomson Sand Prairie Two fecal samples were collected from (TSP) is a 146-ha unit in Carroll County, each turtle annually (2013–2014), when Illinois, that includes both remnant and possible, from each of the head-started reestablished sand prairie. The site contains turtles to identify key dietary components. sand prairie, sand dune, and blowout com- One turtle went undetected for a portion of munities dominated by needlegrass (Stipa the 2013 survey season and was not located spp.) and little bluestem (Schizachyrium sco- for the second fecal collection. Seven 2013 parium Michx.), with interspersed patches of reintroductions died prior to the 2014 fecal
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Figure 1. Single sample of insect specimens to be identified after fecal sample collection and sorting. Samples were collected from head-started ornate box turtles at Thomson Sand Prairie and Lost Mound Sand Prairie in northwestern Illinois.
analysis sampling, while two additional in- dissecting scope with Fisher Scientific LED dividuals succumbed to illness and predation gooseneck illuminator. All measurements during the 2014 surveying season prior to were made using a Wild M5 stereomicro- obtaining second fecal samples. Sampling scope with a Wild MMS235 digital length times occurred during the active season and measuring set. The quantification of insects were spaced approximately one month apart in each sample was often not feasible due to to account for seasonal variation in available the majority of material being extensively resources. Upon capture, each turtle was thoroughly rinsed to remove externally ad- fragmented (Fig. 1). Historically, quantifica- hered particles that could contaminate the tion of identified material has been presented fecal sample and then retained overnight in as frequency of occurrence across the total a 19-L bucket containing 1–2 cm of water. number of turtles sampled (Surface 1908, All turtles defecated during the allotted time. Klimstra & Newsome 1960, Legler 1960). The following morning, the contents of the Platt et al. (2009) presented their findings as bucket were filtered through a 250-μm wire percent occurrence, which they considered a sieve and stored in 70% alcohol for later more appropriate calculation when individu- identification. Arthropods collected, concur- al food item quantification was not feasible. rently, from pitfall traps served as reference We have elected to quantify insect presence samples to aid in identification of arthropod as the number of samples in which the food remains from fecal material. Pitfall traps item occurred divided by the total number consisted of 85-mL plastic cups containing propylene glycol. Each cup was buried with of samples (n). the rim flush with the ground surface. Ten A two-way ANOVA was conducted to traps were placed in a transect and spaced examine relationships between diversity of 50 m apart at each release site. species consumed, years, and three release Insect fragments from fecal samples locations. The statistical computing program were examined using a Nikon SMZ645 R (2013) was used for data analysis.
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Figure 2. Frequency of occurrence in 2013 (n=31) and 2014 (n=24) of insects found in fecal samples of reintroduced ornate box turtles at Thomson Sand Prairie and Lost Mound Sand Prairie.
Results which occurred in 73% of samples in 2013 and 48% of samples in 2014. Aphaenogaster Insects were found in 31 of 33 (94%) treatae Forel (Formicidae) was commonly fecal samples collected in 2013, and 24 of collected in both Lost Mound sites, but was 25 (96%) in 2014. Coleoptera were recovered entirely absent from Thomson Sand Prairie. from 27 of 31 fecal samples, Orthoptera in Formicidae had the greatest diversity with 9 of 31 samples, Hymenoptera in 13 of 31 samples, and Hemiptera in 6 of 31 samples six species across four genera; Scarabaeidae, in 2013. In 2014, Coleoptera were found in also represented by four genera, was limited 19 of 24 fecal samples, Orthoptera in 13 to only four species. Eight families of Cole- of 24 samples, Hymenoptera in 10 of 24 optera were represented in the samples, the samples, and Hemiptera in 13 of 24 sam- greatest familial diversity of the six sampled ples. In 2013, the orders Lepidoptera and orders. Thysanoptera were each represented in Turtles released into the LM IN enclo- single samples. Acrididae, Curculionidae, sure had insect remnants in 7 of 9 samples in and Formicidae were recovered from sam- 2013, while insect fragments were present in ples in both years from all three sites. Six 13 of 13 samples from LM OUT. There was families occurred once each in fecal samples: no significant difference in the number of Histeridae (Atholus falli (Bickhardt)), Mutil- lidae (Dasymutilla sp.), Apidae, Lucanidae species consumed between the three release (Lucanus placidus Say), Alydidae (Alydus sites (F = 1.6044, df = 2, 49, P = 0.2114). No pilosulus Herrich-Schäffer), and Caliscel- significant difference in the number of spe- idae (Bruchomorpha pallidipes Stål) (Fig. cies consumed between the two years was 2). Otiorhynchus ovatus (Linnaeus) and apparent (F = 2.2246, df = 1, 49, P = 0.1422). Melanoplus sanguinipes (Fabricius) were the No significant interaction of site and year only two species that occurred at all three for number of species recovered from fecal sites in both years of the study. The insect material was apparent (F = 2.0350, df = 2, most commonly encountered was O. ovatus, 49, P = 0.1416).
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Insect composition was the focus of concern, future studies may assess whether this study, although identifiable plants, enclosures significantly impact patterns of fungi, and other invertebrates were record- turtle foraging on plants and fungi. While ed. Gastropod shells were recorded in three insect consumption appears unaffected total samples from 2013 and 2014. Fungi by enclosures, additional factors such as were recorded in two samples in 2014 and predation, access to suitable overwintering one sample from 2013. Plant matter was sites, and limited breeding potential should found in 27 of the 33 samples collected in be measured to determine the benefits and 2013, and 24 of the 25 samples in 2014. The efficacy of using soft-release enclosures. majority of plant material was unidentifi- Diet was similarly diverse among all able, although seeds, stems, glochidia, and three treatments. Insect prey selection by inflorescences were used to identify several T. ornata ornata appears indiscriminate. plants. Equisetum L., Acer L., Rhamnus L., The classification of T. ornata ornata as an Carex L., Selaginella P. Beauv., Celtis occi- opportunistic omnivore is supported by a dentalis L., Rubus L., O. humifusa, Callirhoe wide diversity of insect fragments recovered Nutt., Bryophyta, Lithospermum canescens from fecal material. (Michx.) Lehm., and Morus rubra L. were recovered from turtle fecal samples during Diverse invertebrate populations are this study. likely an important continuous food source, as insects were a key dietary element at all Discussion three release sites. The abundance of the flightless weevil,O. ovatus, seen in over half Head-starting conservation programs of the samples, is likely attributable to the have brought concerns and criticism regard- high density of its host, Rubus L., at all three ing the spread of disease to wild populations, sites. Ingested food items that lack rigid loss of fear to potentially harmful organisms structures, such as earthworms and caterpil- and, important to this study, the adjustment lars (Metcalf and Metcalf 1970), were often to natural food resources after prolonged cap- not identifiable in the fecal samples and may tivity (Dodd Jr. and Seigel 1991, Berry and have led to results that are biased towards Christopher 2001, Smith 2015). Head-start- insects with heavily sclerotized exoskeletons ed turtles, in this study, displayed insect and highly fibrous plants and seeds. consumption at percentages comparable to or We assumed T. ornata ornata prefer- even greater than those reported in previous ence for highly productive habitats would studies on wild populations of midwestern increase the likelihood of predator interac- Terrapene species (Cahn 1937, Klimstra tions; however, only one of 26 turtles was and Newsome 1960, Legler 1960). Successful predated during this two-year study. In het- feeding behavior could be a result of innate erogeneous habitats, predation rates on T. predatory behavior and general omnivorous ornata ornata nests increases near ecological tendencies of the species. edges (Temple 1987); this trend was docu- Enclosures can be beneficial for mon- mented at TSP where mesopredators were itoring released organisms by increasing extremely effective at raiding nests along site fidelity and providing protection from riparian areas. Head-starting is often most predators, but can lead to unsafe behaviors successful in populations where juvenile such as frequent walking along the enclosure and adult survival rates are stable and high barriers (presumably in an effort to move be- (Heppell et al. 1996); high juvenile and adult yond the confines of the enclosure), targeting survival rates are indicative of populations by predators, or limited nutrient availability. experiencing low to moderate predation and Benefits may be offset by the often high cost high resource availability. These factors are associated with constructing and maintain- generally in congruence with areas selected ing an enclosure. Analysis of the diversity of for head-start or reintroduction programs. insect species consumed was not significantly In instances where constant monitor- different between enclosure or open release ing of target individuals in reintroduction areas, suggesting that foraging behavior for programs is not feasible, analysis of feces insects is not compromised by enclosures. may anecdotally indicate where individuals The lack of differences in insect consumption forage, especially in heterogeneous habitats between soft and hard release approaches where food resources are patchy. The ability may be due partly to the enclosed area being to clearly predict microhabitat preference similar in size and habitat to other release is reduced by the mobility of the turtle and sites without an enclosure. While insects the high mobility of insects they consume. are mobile and capable of moving through Future research on predation of adult and these enclosures, the same is not true for neonate turtles, and turtle nests in highly sessile organisms that turtles frequently productive habitats is necessary to evaluate eat and that are less likely to be repopulated the cost-benefit of head-start release into from outside the enclosure. To address this areas with higher resource availability.
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Success in reintroduction programs may be ca. Houghton Mifflin Harcourt, Boston, MA. facilitated by avoiding or limiting release 616 pp. into habitats where individuals do not spend Convention on International Trade in En- a majority of their time foraging. dangered Species of Wild Fauna and Flo- Perhaps the most notable insect ra. 2017. Appendices I, II, and III. Available species encountered during this study was from https://cites.org/eng/app/appendices.php Cyclocephala longula LeConte-[IL: (accessed 10 August 2017). Carroll Co./Thomson Sand Prairie/REF Corbett, E., and R. Anderson. 2006. Landscape pitfall/15 July 2013/E. Sievers]. Two males analysis of Illinois and Wisconsin remnant were collected from a pitfall trap in Thom- prairies. The Journal of the Torrey Botanical son Sand Prairie, Carroll County, Illinois. Society 133: 267–279. Cyclocephala longula is known from Oregon south to Mexico and as far east as Kansas. Dodd, C. K., Jr. 2001. North American Box The species’ occurrence is surprising, but the Turtles: A Natural History. University of habitat coincides with that experienced in Oklahoma Press, Norman, OK. 231 pp. the species’ previously known range. These Dodd, C. K., Jr., and R. A. Seigel. 1991. Re- individuals represent a new state record location, repatriation, and translocation of for Illinois. The presence of C. longula in amphibians and reptiles: Are they conser- Illinois adds validity to Endrödi’s (1985) vation strategies that work? Herpetologica record of the species from Wisconsin, which 47: 336–350. was at the time deemed questionable due to Ebinger, J., L. Phillippe, and R. Nyboer. 2006. the distance from the species’ known range Vegetation and flora of the sand deposits of (Saylor 1945). the Mississippi River valley in northwestern Illinois. Illinois Natural History Survey Bul- Acknowledgments letin 37: 191–221. We would like to thank Joe Mac- Endrödi, S. 1985. The Dynastinae of the World. Gowan, Bob Anderson, Michael Caterino, Jo- Dr. W. Junk Publisher, Dordrecht, Nether- Vonn Hill, Blaine Mathison, and Ed Zuccaro lands. 800 pp., 46 plates. for verification of identified specimens. The Ernst, C. H., and J. E. Lovich. 2009. Turtles Upper Mississippi River National Fish and of the United States and Canada. Second Wildlife Refuge staff, especially Ed Britton edition. Johns Hopkins University Press, and Jeramie Strickland, provided invaluable Baltimore. 827 pp. support during field work. This research was Ford, D. K., and D. Moll. 2004. Sexual and sea- conducted with the prior approval obtained sonal variation in foraging patterns in the from the Missouri State University IACUC Stinkpot, Sternotherus odoratus, in south- Board (27 September 2011; protocol number western Missouri. Journal of Herpetology 120011) and the Illinois Endangered Species 38: 296–301. Protection Board, permit number 10-06A. The findings and conclusions in this article Heppell, S., L. Crowder, and D. Crouse. 1996. are those of the authors and do not neces- Models to evaluate headstarting as a man- agement tool for long-lived turtles. Ecological sarily represent the views of the U.S. Fish Applications 6: 556–565. and Wildlife Service. We would like to thank two anonymous reviewers for their valuable Klimstra, W. D., and F. Newsome. 1960. Some ideas and input on our manuscript. observations on the food coactions of the common box turtle, Terrapene c. carolina. Literature Cited Ecology 41: 639–647. Legler, J. M. 1960. Natural history of the ornate Berry, K. H., and M. M. Christopher. 2001. box turtle, Terrapene ornata ornata Agassiz. Guidelines for the field evaluation of desert University of Kansas Museum of Natural tortoise health and disease. Journal of Wild- History 11: 527–669. life Diseases 37: 427–450. Levell, J. P. 1997. A Field Guide to Reptiles Bowen, K., P. Colbert, and F. Janzen. 2004. and the Law. Second Edition. Serpent’s Tail Survival and recruitment in a human- Publisher, Lanesboro, MN. 270 pp. impacted population of ornate box turtles, McCallum, M. L., and E. O. Moll. 1994. Herpe- Terrapene ornata, with recommendations tological inventory of the upland/terrestrial for conservation and management. Journal habitats of the Savanna Army Depot. Illinois of Herpetology 38: 562–568. Natural History Survey. 27 pp. Cahn, A. R. 1937. The turtles of Illinois. Illinois Metcalf, A. L., and Metcalf, E. L. 1970. Observa- Biological Monographs 16: 1–218, 31 plates. tions on ornate box turtles (Terrapene ornata Conant, R., and J. Collins. 1998. Reptiles and ornata Agassiz). Transactions of the Kansas Amphibians: Eastern/Central North Ameri- Academy of Science 73: 96–117.
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Platt, S. G., C. Hall, H. Liu, and C. K. Borg. Sloan, K. N., K. A. Buhlmann, and J. E. 2009. Wet-season food habits and intersex- Lovich. 1996. Stomach contents of com- ual dietary overlap of Florida box turtles mercially harvested adult alligator snapping (Terrapene carolina bauri) on National Key turtles, Macroclemys temminckii. Chelonian Deer Wildlife Refuge, Florida. Southeastern Conservation and Biology 2: 96–99. Naturalist 8: 335–346. Smith, P. C. 2015. First do no harm: Recognizing Platt, S. G., C. M. Ritzi, K. Craig, D. J. Miller, and mitigating the risk of disease introduc- and T. R. Rainwater. 2012. Terrapene tion associated with Chelonian head-starting ornata luteola (Desert Box Turtle). Diet. initiatives. Herpetological Conservation and Herpetological Review 43: 641. Biology 10: 550–558. R Core Team. 2013. R: A language and environ- ment for statistical computing. R Foundation Strickland, J., C. Tucker, E. Britton, E. for Statistical Computing, Vienna, Austria. Tomasovic, R. Engelke, and A. Ander- ARL. Version 3.3.3. Available from http:// son. 2013. Conservation and management www.R-project.org/ (accessed 16 May 2017). of Ornate Box Turtles (Terrapene ornata) at the Upper Mississippi River National Redder, A. J., C. K. Dodd, Jr., D. Keinath, D. McDonald, and T. Ise. 2006. Ornate box Wildlife and Fish Refuge: 2012 Accomplish- turtle (Terrapene ornata ornata): a technical ment Report and 2013 Work Plan. Illinois conservation assessment. USDA Forest Ser- Department of Natural Resources Endan- vice, Rocky Mountain Region. Available from gered Species Protection Board. Available https://www.fs.usda.gov/Internet/FSE_DOC- from http://docs.wixstatic.com/ugd/10e5f9_ UMENTS/stelprdb5182076.pdf (accessed 7 d08f6635531f4 98c9a8294afe8e5b005.pdf February 2013). (accessed 13 September 2017). Refsnider, J. M., J. Strickland, and F. J. Surface, H. A. 1908. First report on the economic Janzen. 2012. Home range and site fidelity features of turtles in Pennsylvania. Zoological of imperiled ornate box turtles (Terrapene Bulletin of the Pennsylvania Department of ornata) in northwestern Illinois. Chelonian Agriculture 6: 107–195. Conservation and Biology 11: 78–83. Temple, S. A. 1987. Predation on turtle nests Rosenburg, K. V., and R. J. Cooper. 1990. increases near ecological edges. Copeia 1987: Approaches to avian diet analysis. Studies 250–252. in Avian Biology 13: 80–90. U.S. Fish and Wildlife Service. 1995. Changes Samson, F. B., and F. L. Knopf. 1994. Prairie conservation in North America. BioScience in the list of species in appendices to the 44: 418–421. convention on international trade in endan- gered species of wild fauna and flora. Federal Saylor, L. W. 1945. Synoptic revision of the Register 60: 665–670. United States scarab beetles of the sub-family Dynastinae, No. 1: tribe Cyclocephalini. Jour- White, J. 1978. Illinois natural areas inventory nal of the Washington Academy of Sciences technical report (Volume 1). Illinois Natural 35: 378–386. Areas Inventory, Urbana, IL.
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The Drosophilids of a Pristine Old-Growth Northern Hardwood Forest Thomas Werner Department of Biological Sciences, Michigan Technological University 1400 Townsend Drive, Houghton, Michigan 49931 USA
Abstract The current study summarizes the results of a species inventory survey for drosophilid flies (family Drosophilidae, order Diptera) in a primeval forest in northern Michigan. The two main goals of the investigation were to list the species inhabiting the Huron Mountain Club and to collect live specimens for the illustrations of the book “Drosophilids of the Mid- west and Northeast”. From 2014 to 2016, I found 22 drosophilid species, which belong to the two subfamilies Steganinae and Drosophilinae. Future long-term studies are planned to test how the drosophilid populations respond to climate change. Keywords: Huron Mountains, Huron Mountain Club, Drosophila, drosophilids, old- growth hardwood forest
The Huron Mountains, situated about highly suitable habitats for drosophilids, 40 km NW of Marquette in the Upper both for native and invasive species. In order Peninsula of Michigan, comprise one of to investigate the drosophilid fauna, I placed the largest old-growth hemlock-hardwood baits and traps at 23 research sites across forests in the upper Great Lakes area. The the Huron Mountain Club property. Over Huron Mountain Club has privately owned a three years, I found a total of 22 drosophilid considerable portion of the Huron Mountains species, which I will report here. Many of since its foundation in 1889 and protected the specimens that I collected in the Huron the forest from being logged. Today, the Mountains were used for the illustrations ~6,000 ha club property preserves one of in the now published book “Drosophilids the most extensive tracks of remnant old- of the Midwest and Northeast”, which is growth forest in the Great Lakes area. For freely available to the public (Werner and a comprehensive review on the history of Jaenike 2017). the region, see (Flaspohler and Meine 2006). The Huron Mountains offer a great variety Materials and Methods of habitat types: a total of fifty landscape ecosystem types have been described for Baits, Traps, and Natural Sub- the area (Simpson 1990). I had the great strates. Flies were collected with a net privilege to obtain permission to conduct from tomato baits, mushroom baits, banana an inventory survey of the drosophilid flies traps, beer traps, and wild mushrooms. Shelf (family Drosophilidae) on the Huron Moun- mushroom feeders were aspirated from the tain Club property during the summers of underside of shelf mushrooms (Ganoderma 2014 – 2016. Although most people associate applanatum (Persoon)). Tomato baits were the name Drosophila with only one species, prepared from large- to medium-sized over- “the fruit fly”, or more precisely, the genetic ripe tomatoes that were cut in half and model organism Drosophila melanogaster placed on the ground next to fallen logs. Meigen, the genus Drosophila alone contains Mushroom baits consisted of store-bought more than 4,100 species worldwide (Markow white button mushrooms (Agaricus bisporus and O’Grady 2006, Yassin 2013). The many (Lange)) pre-soaked for at least 30 minutes species of the family Drosophilidae are in water to keep them moist for several adapted to a broad variety of habitats and days. Like tomato baits, the mushroom baits diets. While forest-inhabiting species feed on were placed on the ground in groups of ~10 mushrooms (including the most toxic ones), mushrooms. Banana traps were made of tree sap, acorns, rotten fruit, leaves, or flow- mushed over-ripe bananas (without the peel) ers, many other species are habitat and food with a few sprinkles of Baker’s yeast added. generalists and can thus be found virtually The banana/yeast mixture was placed into anywhere. The Huron Mountains offer many plastic bottles with a few sticks as perching sites and hung in trees to protect them from small mammals. Beer traps consisted of Email: [email protected] wide-necked glass bottles (“Frappuccino”
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bottles) filled with ~80 mL of golden-ale- later breeding and imaging to create the style beer. Because Amiota flies (the target images for the book “Drosophilids of the Mid- group for beer traps) live in the forest canopy, west and Northeast” (Werner and Jaenike beer traps were hung in trees. At the time of 2017). Hence, the current investigation was collection, all flies were immediately trans- of semi-quantitative nature: while I recorded ferred into sugar agar vials. I usually collect- numbers of specimens for rare species, I only ed flies twice from the baits and traps: the recorded rough estimates for the more abun- first time two days after their installation, dant species. In 2014, I collected 18 drosoph- and the second time four to five days later. ilid species in the Huron Mountains: Amiota The flies were identified alive at the end of humeralis Loew, Amiota leucostoma Loew, each collection day. For more details about Chymomyza amoena (Loew), Hirtodrosoph- collecting drosophilid flies, see “Drosophilids ila duncani (Sturtevant), D. melanogaster, of the Midwest and Northwest” (Werner and Drosophila suzukii (Matsumura), Drosoph- Jaenike 2017). ila algonquin Sturtevant & Dobzhansky, Collection Periods and Sites. Drosophila affinis Sturtevant, Drosophila During the summers from 2014–2016, I athabasca Sturtevant & Dobzhansky, Dro- spent one week in each month of June, sophila busckii Coquillett, Scaptomyza sp., July, and August on the Huron Mountain Drosophila robusta Sturtevant, Drosophila Club property to collect drosophilid flies. paramelanica Griffen, Mycodrosophila (6/23/2014–6/29/2014, 7/22/2014–7/28/2014, claytonae Wheeler & Takada, Drosophila 8/25/2014–8/31/2014, 6/15/2015–6/21/2015, immigrans Sturtevant, Drosophila neotesta- 7/6/2015–7/12/2015, 8/10/2016–8/16/2015, cea Grimaldi, James, & Jaenike, Drosophila 6/27/2016–7/3/2016, 7/25/2016–7/31/2016, falleni Wheeler, and Drosophila recens and 8/18/2016–8/24/2016). The daytime Wheeler. In 2015, two more species were temperatures usually ranged from 18 to attracted to my baits and traps, both of which 25°C and rarely reached 30°C or above. are quite uncommon in northern Michigan: Sites 3–25 were established in 2014, while Drosophila putrida Sturtevant and Drosoph- sites 26 and 29 were added in 2015 and ila tripunctata Loew. Finally, I found two 2016, respectively (Fig. 1). Sites 3 and 5–26 additional species in 2016: A. minor and D. received banana, tomato, and mushroom macrospina. In total, I found 22 drosophilid traps/baits. Site 29 received only beer traps. species in the Huron Mountains, including Gaps in site numbers were sites established the invasive agricultural pest D. suzukii, to study butterflies and moths, which are which originated in Southeast Asia. Table 2 not reported in the current study, with the lists the substrates to which the individual exception of site 4, where I collected Amiota species were attracted. minor (Malloch) from my arm. Each trap The accompanying figures 2–9 summa- position was recorded with a hand-held GPS. rize the distribution of each species in time The GPS coordinates and site descriptions and space. Additional information about are provided in Table 1. the ecology, evolution, and geographical Drosophilid species identification. distribution of these species can be found To identify the species, I used the characters in (Markow and O’Grady 2006, Miller et al. published in our book “Drosophilids of the 2017, Werner and Jaenike 2017). Midwest and Northeast” (Werner and Jae- Amiota humeralis Loew, subfam- nike 2017) and examined external male and ily Steganinae. I encountered this species female terminalia whenever necessary. I also infrequently and each time in very low reared many species from females collected numbers (one or two individuals). Most spec- in the field and double-checked the key imens were collected at wooded sites close characters in the F1 generation. In the case to Pine Lake and Mountain Lake, usually of Drosophila macrospina Stalker & Spencer, in July and August (Fig. 1 and 2A). Banana mitochondrial DNA was sequenced to con- traps were the most efficient to attract this firm the species. No voucher specimens were species, although I also collected a few flies stored in ethanol, but many specimens from from tomato baits, mushroom baits, and wild the Huron Mountain study were digitalized mushrooms (Table 2). Very little is known and can be found in our book “Drosophilids of the Midwest and Northeast” (Werner and about the life history of Amiota flies. Jaenike 2017). Amiota leucostoma Loew, subfami- ly Steganinae. This species was very rare. Results I only found three individuals in total, one each year in July (Fig. 2B). The substrates Twenty-two Drosophilid Species that attracted these flies were diverse: mush- in the Huron Mountains. The two main rooms, beer, and banana (Table 2). Like A. objectives of this investigation were to 1) humeralis, A. leucostoma visited wooded make a species inventory list for the Huron sites adjacent to Pine Lake and Mountain Mountain Club and 2) collect live flies for Lake (Fig. 1 and 2B).
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Figure 1. Map of the Huron Mountains and the research sites
Amiota minor (Malloch), subfamily Chymomyza amoena (Loew), sub- Steganinae. During a butterfly collection family Drosophilinae. I found this some- walk on a hot day in June 2016, one specimen what uncommon species in wooded as well of A. minor landed on my arm at site 4, which as more open areas (Fig. 1). Chymomyza is adjacent to Ives Lake. This specimen was amoena visited mainly tomato baits, but spo- apparently attracted to sweat. I have never radically also wild mushrooms and banana seen this species come to baits (Fig. 1, 2C, traps (Table 2). I encountered this species and Table 2). throughout the summer months (Fig. 3A).
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Table 1. Characteristics of the research sites and GPS coordinates in the Huron Moun- tains.
Site Characteristics GPS Coordinates
3 Ives Lake Field Station, shaded area next to the stone N46° 50.644’ W87° 51.290’ house, former farmland
4 Sun-exposed dirt road along south side of Ives Lake, high N46° 50.326’ W87° 50.828’ diversity of deciduous trees/bushes and flowering plants 6 Hemlock-dominated forest along north side of Second Lake N46° 52.309’ W87° 51.431’ 8 Hemlock-dominated forest northwest of Pine Lake, N46° 53.096’ W87° 52.922’ adjacent to a dirt road 9 Hemlock-dominated forest west of Pine Lake, adjacent to dirt N46° 52.956’ W87° 53.199’ road, lots of fallen logs with shelf mushrooms on the ground 10 Hemlock/sugar maple forest west of Pine Lake, adjacent to a N46° 52.729’ W87° 53.049’ dirt road 11 Mixed hemlock forest, undergrowth dominated by sugar N46° 52.454’ W87° 53.104’ maple saplings, adjacent to a sandy dirt road 12 Hemlock-dominated forest, undergrowth dominated by sugar N46° 52.108’ W87° 53.799’ maple saplings, adjacent to a dirt road, large log with shelf mushrooms on the ground 13 Hemlock forest east of Mountain Lake N46° 51.687’ W87° 54.377’ 14 Hemlock/sugar maple forest, undergrowth dominated by N46° 51.946’ W87° 54.122’ sugar maple saplings, adjacent to a dirt road 15 Hemlock/sugar maple forest, undergrowth dominated by N46° 52.050’ W87° 54.160’ sugar maple saplings, east of Mountain Lake 16 Hemlock-dominated forest north of Mountain Stream N46° 52.222’ W87° 53.576’ 17 Hemlock forest with large logs containing shelf mushrooms N46° 52.321’ W87° 53.207’ on the ground 18 Hemlock/sugar maple forest, undergrowth dominated by sugar maple saplings, south of boat landing at Pine Lake N46° 52.560’ W87° 52.905’ 19 Hemlock forest bordering the jack pine barren at the N46° 53.233’ W87° 52.782’ northwest corner of Pine Lake, blueberry bushes in the undergrowth 20 Hemlock forest adjacent to dirt road N46° 52.526’ W87° 51.916’ 21 Hemlock forest adjacent to dirt road N46° 52.015’ W87° 50.888’ 22 Hemlock forest N46° 51.501’ W87° 50.148’ 23 Hemlock-dominated forest with sugar maple saplings in the N46° 52.404’ W87° 50.247’ undergrowth and a large log with shelf mushrooms on the ground 24 Hemlock-dominated forest adjacent to dirt road and a swamp N46° 52.218’ W87° 50.919’ 25 Hemlock-dominated forest adjacent to dirt road, N46° 51.731’ W87° 50.616’ sun-exposed during mid-day 26 Hemlock/sugar maple forest adjacent to dirt road, often N46° 50.255’ W87° 50.766’ flooded after heavy rain 29 Half-shaded area adjacent to Rush Creek and dirt road, N46° 53.020’ W87° 53.421’ swampy character
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Table 2. Species list for drosophilids found in the Huron Mountains from 2014 to 2016 and the substrates from which they were collected. The species are sorted by their phyloge- netic relationships. * = shelf mushroom Ganoderma applanatum.
Species Banana Tomato Mushroom Beer Sweat Amiota humeralis X X X Amiota leucostoma X X X Amiota minor X Chymomyza amoena X X X Hirtodrosophila duncani X X Drosophila melanogaster X X Drosophila suzukii X X X X Drosophila algonquin X X X Drosophila affinis X X Drosophila athabasca X X X Drosophila busckii X X X Scaptomyza sp. X Drosophila robusta X X X X Drosophila paramelanica X X Mycodrosophila claytonae X* Drosophila immigrans X X X Drosophila macrospina X Drosophila neotestacea X X X X Drosophila putrida X X Drosophila falleni X X X Drosophila recens X X X Drosophila tripunctata X
This species is known to breed in acorns and about half of the collection sites in moder- apples (Band 1988), which occur in the area. ate numbers over the three years combined Hirtodrosophila duncani (Stur- (Fig. 1 and 3C). Drosophila melanogaster tevant), subfamily Drosophilinae. was most common at the Ives Lake Field Hirtodrosophila duncani appeared in very Station, where I regularly found this species low numbers throughout the summer in somewhat larger numbers on tomato baits months in wooded areas (Fig. 1 and 3B). and in banana traps (Fig. 3C and Table 2). Although this species is mycophagous (Lacy This species breeds in various decaying fruits 1984), i.e., a mushroom-feeder, banana traps and is known to be common around humans worked best to attract it (Table 2), while I settlements and rare quite rare in the woods only found one specimen at a mushroom (Sturtevant 1921). bait. Hirtodrosophila duncani breeds more Drosophila suzukii (Matsumura), often in various species of shelf mushrooms, subgenus Sophophora. Also known as the which could be why regular store-bought “Spotted Wing Drosophila” or “SWD”, this mushrooms are not very attractive to them. species was one of the most abundant spe- Drosophila melanogaster Meigen, cies in the Huron Mountains. It was equally subgenus Sophophora. This cosmopoli- common in the woods as in open areas, and tan species was surprisingly uncommon in it visited all designated fly collection sites the deep woods of the Huron Mountains. I (Fig. 1 and 4A). Although I did not encounter sparsely encountered this species at only a single specimen in June, the numbers of
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flies increased as the summers progressed, them. An identification key can be found in with few flies in July and dozens of flies per “Drosophilids of the Midwest and Northeast” trap in August. Banana traps and tomato (Werner and Jaenike 2017). Future collec- baits worked equally well in attracting D. tion trips to the Huron Mountain Club are suzukii, while I also found a few flies on planned to reveal the species identity of the mushroom baits and wild mushrooms. This flies of this genus. species is known to breed in a variety of Drosophila robusta Sturtevant, berries and other small fruits (Lee et al. subgenus Drosophila. This species was a 2011), of which there are many available in common sight throughout the summers in the Huron Mountains, such as raspberries banana traps and on tomato baits, while I and blueberries. Notably, the beer trap at collected it much less frequently from mush- site 29 contained a few hundred drowned D. room baits. Drosophila robusta was also suzukii flies of both sexes in August of 2016, attracted to beer at site 29 (Fig. 1 and 6A, suggesting that beer traps might provide a Table 2). This species breeds in slime fluxes useful tool to reduce D. suzukii populations or various trees (Carson and Stalker 1951). on fruit plantations. Drosophila paramelanica Griffen, Drosophila algonquin Sturtevant subgenus Drosophila. I collected this spe- & Dobzhansky, subgenus Sophophora. cies sporadically at open and wooded sites. This species was very abundant and mainly Drosophila paramelanica showed a prefer- attracted to banana traps and tomato baits, ence for banana traps, but it also came a few although some specimens also visited mush- times to tomato baits (Table 2). I collected it room baits and wild mushrooms (Table 2). usually in July and August (Fig. 1 and 6B). I found it at nearly all research sites from This species is likely to breed in slime fluxes June throughout August (Fig. 1 and 4B). of trees (Stalker 1960). The primary breeding sites of this and the following two species are not known. Mycodrosophila claytonae Wheeler & Takada, subgenus Drosophila. Unlike Drosophila affinis Sturtevant, most other species, M. claytonae never visit- subgenus Sophophora. This species was ed traps or baits. I only found it only at three quite rare. I found it both in open and wooded collection sites, where G. applanatum shelf areas (Fig. 1 and 4C). Most specimens came mushrooms were abundant on dead logs (Fig. to banana traps, while a few flies visited 1 and 6C). The flies of this mycophagous tomato baits (Table 2). I did not encounter species (Lacy 1984) sat or walked across this species in 2016. the mushrooms’ white underside, usually on Drosophila athabasca Sturtevant warm, sunny days just after heavy rainfalls & Dobzhansky, subgenus Sophophora. (Table 2). The undersides of the mushrooms This species was about as common as D. often steamed off water vapor when flies algonquin. I found it in open and wooded were present. Flies were present in high areas throughout the summer months (Fig. numbers (ten individuals) at times on this 1 and 5A). Most specimens came to banana species. I never encountered this species traps and tomato baits, while few individuals under dry conditions. visited mushroom baits and wild mushrooms Drosophila immigrans Sturtevant, (Table 2). subgenus Drosophila. This cosmopolitan Drosophila busckii Coquillett, species (Sturtevant 1921) was absent in June subgenus Dorsilopha. I found a total of and became increasingly abundant as sum- three individuals of this species: one on a mer progressed. I found it in banana traps, mushroom bait, one on a tomato bait (both as well as on tomato and mushroom baits at the Ives Lake Field Station), and one across the study area (Fig. 1 and 7A, Table in a banana trap in a wooded area near 2). Drosophila immigrans usually breeds in Mountain Lake (Fig. 1 and 5B, Table 2). decaying fruits and vegetables (Atkinson and The sampling results reflect the fact that Shorrocks 1977). D. busckii breeds in a very large variety of Drosophila macrospina Stalker & substrates, including garbage and decaying Spencer, subgenus Drosophila. This very vegetables (Atkinson and Shorrocks 1977). rare species was attracted to banana baits It is possible that this species breeds in the in the woods. I only encountered two speci- garbage of the field station. mens on the same day in August 2016 (Fig. Scaptomyza sp., subgenus Dro- 1 and 7B, Table 2). This species has been sophila. A total of three specimens visited described as living in the woods near streams tomato baits: two at the Ives lake Field Sta- and swamps, although its natural breeding tion and one near Pine Lake (Fig. 1 and 5C, substrates are unknown (Mainland 1942). Table 1). I was unable to identify Scaptomyza Drosophila neotestacea Grimaldi, flies to the species until just recently, and James, & Jaenike, subgenus Drosophi- the flies perished before I was able to image la. Drosophila neotestacea is a mycophagous
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FIGURE 2 FIGURE 3
FIGURE 4 FIGURE 5
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FIGURE 6 FIGURE 7
FIGURE 9
Figures 2–9. Plots of spatio-temperal distri- butions of the 22 drosophilid species. The y-axis shows the months and years during which I collected flies. The actual dates can be found in the Materials and Methods section. The research FIGURE 8 sites are listed on the x-axis.
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species (Grimaldi 1985) and was the most The diverse trap and bait types used abundant drosophilid species in the Hu- here attracted different sets of species, al- ron Mountains. It was very common at all though there was also substantial overlap sites and times (Fig. 1 and 7C). Although (Table 2). Banana traps attracted larger it strongly preferred mushroom baits and numbers of drosophilid flies that feed on fruit wild mushrooms, I also found it on tomato and also tree sap and mushroom feeders in baits and far less often in banana and beer lower numbers. Tomatoes attracted a wide traps (Table 2). range of species, but none in large numbers. Drosophila putrida Sturtevant, Mushroom baits attracted large numbers of subgenus Drosophila. I encountered only mostly mushroom-feeding species, except two specimens of this mycophagous species the shelf mushroom feeder M. claytonae, (Grimaldi 1985): one fly came to a mushroom which I was only able to collect from G. bait and one to a banana trap. Both research applanatum shelf mushrooms. It is worth sites 16 and 22 were positioned in the woods, noting that omitting mushroom baits in this a bit further away from the lakes (Table 2, study would have resulted in an identical Fig. 1 and 8A). species list because all species that were attracted to mushroom baits also visited Drosophila falleni Wheeler, subge- other substrates. nus Drosophila. This mycophagous species (Jaenike 1978, Lacy 1984) was a regular Although I was unable to find any visitor of mushroom baits, wild mushrooms, remarkable correlations between particular tomato baits, and banana traps (Table 2). I habitats and overall species occurrence, I found it at virtually all collection sites with note that the sites in the valley between nearly equal abundance throughout the Mountain Lake and Pine Lake (sites 11 – summer months (Fig. 1 and 8B). 18) were my favorite ones because of the highest abundance of Amiota flies. This ge- Drosophila recens Wheeler, subge- nus is poorly studied because of the elusive nus Drosophila. Like D. falleni, D. recens lifestyle of the flies and may contain cryptic is mycophagous (Grimaldi 1985) and was species to be discovered in the future. Also, a common visitor of mushroom baits, wild I encountered nearly all drosophliid species mushrooms, tomato baits, and sometimes there, except Scaptomyza sp. and A. minor. banana traps (Table 2). I found it at all fly collection sites (except the beer trap) with Amiota and Scaptomyza species are nearly equal abundance throughout the not easily attracted to commonly used fruit summer months (Fig. 1 and 8C). fly baits and traps. In addition to that,Ami - ota flies live high up in the canopy of forests Drosophila tripunctata Loew, (Beppu 1984). It is therefore likely that my subgenus Drosophila. This is perhaps sparse encounters with flies of these genera the rarest drosophilid species in the Huron are an underestimate of the true abundance Mountains. I found a single specimen of D. Amiota and Scaptomyza species in the area. tripunctata at site 18 near Pine Lake on a I consider the Huron Mountains a superb tomato bait (Fig. 1 and 8C, Table 2). The study ground for Amiota flies because diet of this species includes mushrooms and three species are present and likely well fruits (Carson and Stalker 1951, Collins established. Future studies in the Huron 1956, Lacy 1984). Mountains will include improved beer and wine traps, to which some Amiota species Discussion are attracted (Bächli et al. 2004). The trap This three-year study from 2014 to designs will have to be modified from the 2016 has shown that the Huron Mountain current standard though, so that the flies Club property is home to at least 22 droso- can be collected alive for imaging purposes. philid species, which represent ~40% of the The species of most economic interest species that inhabit the Midwest and North- is D. suzukii, the spotted wing Drosophila east of the USA (Miller et al. 2017, Werner (SWD), which was introduced to the North and Jaenike 2017). The current study is the American mainland in California in 2008 most comprehensive investigation of wild and quickly spread to the east coast (Lee et drosophilid populations performed in the al. 2011). I found D. suzukii in high abun- Upper Peninsula of Michigan thus far, and dance in the Huron Mountains, especially it is the first study describing these insects during late summer, when it became one in the Huron Mountains. According to the of the most frequently encountered species. distribution maps in (Miller et al. 2017), no Notably, the beer trap at site 29 contained one has collected drosophilids in the Upper hundreds of drowned D. suzukii flies of both Peninsula before. Therefore, most, if not sexes. It would be worthwhile testing if beer all, species encounters are new records for traps can be used as a feasible way to reduce this area. crop losses on SWD-infested fruit farms.
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The three most rarely encountered sophila in the eastern United States. Ecology bait-visiting species were D. macrospina, D. 32: 317–330. putrida, and D. tripunctata. All three species Collins, W. E. 1956. On the biology and control of reach their northwestern distribution range Drosophila on tomatoes for processing. Jour- in northern Michigan (Miller et al. 2017). nal of Economic Entomology 49: 607–610. Although D. macrospina has been found earlier in Michigan (Stalker and Spencer Flaspohler, D. J., and C. Meine. 2006. Plan- 1939), the Huron Mountain location is the ning for wildness: Aldo Leopold’s report on northern-most site for this species on record Huron Mountain Club. Journal of Forestry in the Northeast (Miller et al. 2017). The 104: 32–42. geographical distribution range of D. putri- Grimaldi, D. A. 1985. Niche separation and da is concentrated around the eastern part competitive coexistence in mycophagous Dro- of the USA, where this species is the most sophila (Diptera: Drosophilidae). Proceedings commonly encountered mushroom-feeding of Entomological Society of Washington 87: species (Miller et al. 2017, Werner and Jae- 498–511. nike 2017). Similarly, D. tripunctata is rarely seen in the North, but it has spread north- Jaenike, J. 1978. Resource predictability and ward over the past few decades (Patterson niche breadth in the Drosophila quinaria and Wagner 1943, Spiess 1949, Lacy 1984). species group. Evolution 32: 676–678. The Huron Mountain Club is home of Lacy, R. C. 1984. Predictability, toxicity, and one of the largest old-growth forests of the trophic niche breadth in fungus-feeding Dro- Great Lakes region and provides an invalu- sophilidae (Diptera). Ecological Entomology able ground for future long-term studies, 9: 43–54. particularly to test how climate change af- Lee, J. C., D. J. Bruck, H. Curry, D. Edwards, fects the species community in the area. Will D. R. Haviland, R. A. Van Steenwyk, and we see rare southern species become more B. M. Yorgey. 2011. The susceptibility of common in the Huron Mountains, and will small fruits and cherries to the spotted-wing they perhaps replace northern species in the drosophila, Drosophila suzukii. Pest Manage- coming decades? Future long-term studies ment Science 67: 1358–67. will be able to shed light on this question. Mainland, G. B. 1942. VI. Genetic relationships in the Drosophila funebris group. Studies in Acknowledgments the genetics of Drosophila 2: 74. I would like to thank the Huron Moun- Markow, T. A., and P. M. O’Grady. 2006. Dro- tain Wildlife Foundation for supporting sophila. A guide to species identification and this research (Michigan Tech agreement use, Elsevier Inc., Amsterdam. #1401076), the Michigan Tech Research Ex- Miller, M. E., S. A. Marshall, and D. A. Grimal- cellence Fund (Mentoring Grant 1205026) for di. 2017. A review of the species of Drosophila funding my meetings with Dr. John Jaenike (Diptera: Drosophilidae) and genera of Dro- (University of Rochester, NY), who taught sophilidae of northeastern North America. me how to identify drosophilids and who gave Canadian Journal of Arthropod Identification valuable comments on this manuscript, and 31: 1–282. the Walmart store in Houghton, MI, for the generous supply of overripe produce. Patterson, J. T., and R. P. Wagner. 1943. Geographical distribution of species of the Literature Cited genus Drosophila in the United States and Mexico. University of Texas Publications Atkinson, W. and B. Shorrocks. 1977. Breed- 4313: 217–281. ing site specificity in the domestic species of Simpson, T. B. 1990. Landscape ecosystem and Drosophila. Oecologia 29: 223–232. cover types of the reserve area and adjacent Bächli, G., C. R. Vilela, S. A. Escher, and A. lands of the Huron Mountain Club, Mar- Saura. 2004. The Drosophilidae (Diptera) of quette County, Upper Michigan (Doctoral Fennoscandia and Denmark, Brill Academic dissertation). Retrieved from University of Publishers, Boston. Michigan. (Accession No. (UMI)AAI9034516). Band, H. 1988. Host shifts of Chymomyza amoena Spiess, E. B. 1949. Drosophila in New England. (Diptera: Drosophilidae). American Midland Journal of the New York Entomological So- Naturalist 120: 163–182. ciety 57: 117–131. Beppu, K. 1984. Vertical microdistribution of Stalker, H. D. 1960. Chromosomal polymorphism Drosophilidae (Diptera) in a beech forest. in Drosophila paramelanica Patterson. Ge- Kontyu, Tokyo 52: 58–64. netics 45: 95–114. Carson, H. L., and H. D. Stalker. 1951. Natural Stalker, H. D., and W. P. Spencer. 1939. Four breeding sites for some wild species of Dro- new species of Drosophila, with notes on the
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funebris group. Annals of the Entomological Libraries, University of Rochester, Rochester, Society of America 32: 105–112. NY, USA. Sturtevant, A. H. 1921. The North American Yassin, A. 2013. Phylogenetic classification of species of Drosophila, Carnegie Institution the Drosophilidae Rondani (Diptera): the of Washington. role of morphology in the postgenomic era. Werner, T., and J. Jaenike. 2017. Drosophilids Systematic Entomology 38: 349–364. of the Midwest and Northeast, River Campus
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The Ability of Specific-wavelength LED Lights in Attracting Night-flying Insects Ryan S. Zemel1 and David C. Houghton1* 1Department of Biology, Hillsdale College, 33 East College Street, Hillsdale, MI 49242
Abstract This paper describes a portable collecting light, designed by the authors, that weighs 0.3 kg, is powered by 8 AA batteries, and uses 9 light-emitting diodes (LEDs) to attract night-flying insects. Five different wavelengths of these LED lights, all within the long-wave ultraviolet spectrum, were compared to each other and to a commercially-available 15w fluorescent ultraviolet tube light for their abilities to collect insects over a series of 5 nights in July 2016. There was no difference in order richness, total specimen abundance, or the specimen abundance of most common orders between any of the wavelengths tested. Most LED wavelengths, however, caught fewer Diptera specimens than the fluorescent tube light, largely due to a lower abundance of chironomid midges. Differences in specimen abundance were greater based on sampling date or specific sampling location than based on type of collecting light. Due to their greater portability and possibly lower bycatch of Diptera, these new LED lights are presented as a potential alternative to ultraviolet tube lights. Keywords: Light, emitting, diode, LED, night, insect, attraction
Night-flying insects are frequently Materials and Methods collected using fluorescent ultraviolet tube lights. While these devices are generally Light housings were made from com- effective, they are cumbersome to carry due mercially-available clear high density poly- to the bulky and heavy power supply. A ethylene (HDPE) tubes of 3.8 cm diameter standard 15w light typically requires a bulky (www.uline.com) (Fig. 1A). Tubes were cut lead acid battery weighing 7–8 kg. Thus, into 31 cm sections and fitted with water- such lights are not realistic for remote field tight caps at both ends. One cap was drilled for insertion of the power switch and then conditions where hiking long distances with sealed with watertight adhesive. Six 3-watt multiple lights are required. LEDs (~3.2–3.8V, 700 mA) were glued in an Light-emitting diodes (LEDs) have alternating manner at either ~45º or ~180º potential as insect collecting devices due to angles along a 1 cm diameter polyvinyl chlo- their small size and weight, long life span, ride (PVC) tube inserted into the housing. and low power needs (Price and Baker 2016). Three additional LEDs were glued onto the Moreover, LEDs are available in many dif- face of the battery pack. The battery pack ferent wavelengths, allowing for potential was wired to three 10w constant current specificity in the insects attracted (Chu et (900 mA) drivers to maintain a steady light al. 2003, Nakamoto and Kuba 2004, Chen output. Each driver was wired to three of the et al. 2004, Longcore et al. 2015). Several LEDs (Fig. 1B). Each light thus consisted of 9 recent studies (Green et al. 2012, Pawsen LEDs of a particular ultraviolet wavelength. and Bader 2014, Price and Baker 2016) have A completed light (Fig. 1C), including the 8 indicated the efficacy of various configura- 1.5V AA alkaline batteries needed to run tions of LEDs relative to fluorescent tube it, weighed 0.3 kg. A completed light took lights. The objective of this research was to 2–3 hours to construct, did not require any design our own LED ultraviolet light and to complex circuitry, and cost between $13.00 and $25.00 for parts, depending on the cost test the ability to catch night-flying insects of the specific LED bulbs. of this light against fluorescent tube lights. We also tested several different wavelengths Ultraviolet wavelengths of our pur- of LEDs within the long-wave ultraviolet chased LED bulbs were confirmed by using spectrum to ascertain if small differences a Red Tide Spectrometer (www.oceanoptics. in wavelength would affect capture ability. com) and LoggerPro 3 software (www.ver- nier.com). Each individual bulb was placed inside its HDPE tube 30 cm above the spec- *Corresponding author: (email: david.houghton@ trometer, aimed downwards, and its intensi- hillsdale.edu). ty at wavelengths 350–450 nm recorded. We
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Figure 1. Components of the collecting lights (A), wiring schematic (B), and completed light (C).
did likewise with a commercially available Field testing of the lights was conduct- 12V, 15w, fluorescent ultraviolet tube light ed during the nights of 19, 21, 22, 25, and (www.bioquip.com, model #2805). Although 26 July 2016 adjacent to a ~400m section of we purchased bulbs of 7 different advertised Fairbanks Creek, located in northwestern LED wavelengths, only 5 were actually Lower Michigan (N 44.04º, W 85.67º). Due to historical (>15 ybp) agriculture at the site, found: 380, 385, 390, 395, and 403 nm (Fig. riparian vegetation was primarily grasses 2). The fluorescent ultraviolet tube light had and sedges (Carex spp.), with some young several peaks of intensity. Our experimental pines (Pinus strobus L, P. resinoa Aiton) and lights consisted of the 5 determined LED oaks (Quercas spp.). More thorough recent wavelengths and the fluorescent tube. descriptions and previous research at this
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Figure 2. Peaks of light intensity within the 350–450nm range for the 10 LED (primary axis) and 2 fluorescent UV (secondary axis) bulbs tested. Intensity is in arbitrary units (a.u.), because bulbs were tested to confirm their primary wavelengths only. Thus, the spectrophotometer was not calibrated for absolute intensity, precluding any meaningful comparison of intensity between bulbs.
site can be found in Houghton and Wasson Lepidoptera, and Trichoptera was also com- (2013), Brakel et al. (2015), and Houghton pared via 1-way ANOVA. Mean specimen (2015). abundance, as well as specimen abundance Lights were tested at 12 sampling for each of the above 7 orders, were also locations along the stream, each separated analyzed per sampling location and per date by ~15m. Two light traps of each of the 5 with individual 1-way ANOVAs. Mean order LED wavelengths and 2 of the fluorescent richness per wavelength was analyzed with a tube lights were placed randomly within the Mann-Whitney U test since the distribution 12 sampling locations over the 5 evenings. violated parametric assumptions. Individual Thus, different treatments were in different correlations with total specimen abundance locations on different evenings. Each light were determined for LED wavelength, and was set on top of a 24×30 cm white plastic maximum temperature and dew point for pan filled with 80% EtOH and placed ~1 m the collecting day. from the water’s edge. Lights were simulta- neously turned on at 10:20 pm and turned off Results at 12:20 am. Sampling occurred on evenings There was no difference in either mean with daytime temperatures >25°C and with specimen abundance or mean order richness no precipitation within 2h of dusk or during between the 5 LED wavelengths or the flu- the sampling period. Batteries were replaced orescent ultraviolet light. There was no dif- in each light after every 2h trial. ference in mean specimen abundance of the Collected specimens were identified 7 most abundant orders between the lights to the order level and counted. Mean total except for the Diptera, which exhibited some specimen abundance per wavelength was statistical overlap (Table 1). Wavelength compared with a 1-way Analysis of Variance exhibited a weak negative correlation (r = (ANOVA) with a post-hoc Tukey test. Speci- 0.45) with total number of specimens caught. men abundance per wavelength within the 7 The 21 July sampling night had both the most abundant orders: Coleoptera, Diptera, highest mean specimen abundance for all Ephemeroptera, Homoptera, Hymenoptera, orders combined and the highest specimen
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Table 1. Mean number of specimens from the 7 most abundant insect orders, and mean total num- ber of orders, based on wavelength during the 5 nights of our study. Asterisks represent statisti- cally distinct groups of means based on a 1-way Analysis of Variance with a post-hoc Tukey test. For number of orders, a Mann-Whitney U test was used due to the non-normal distribution. ‘UV’ = ultraviolet fluorescent bulb.
Wavelength 380 385 390 395 403 UV p Coleoptera 33.0 27.2 20.0 39.0 34.3 29.2 0.93 Diptera 342.3a 232.9ab 88.7b 187.3ab 161.5ab 433.4a 0.03 Ephemeroptera 21.2 10.6 8.2 13.4 14.5 9.0 0.59 Homoptera 120.4 99.1 78.8 107.7 72.7 107.1 0.59 Hymenoptera 15.2 13.9 8.8 14.5 11.2 13.7 0.98 Lepidoptera 421.7 300.6 162.4 245.4 257.8 374.6 0.66 Trichoptera 169.2 136.3 151.9 140.3 75.2 139.1 0.51 Combined 1142.3 840.0 533.2 768.8 650.1 1123.8 0.42 Number of orders 9.6 9.3 9.5 9.7 9.5 9.5 0.70
abundance for each individual order except and fluorescent lights. Similarly, Price and Ephemeroptera (Table 2). Total number of Baker (2016) found that their designed LED specimens caught per sampling night did collecting light compared “favorably” to fluo- not correlate with maximum temperature rescent ultraviolet lights. Although no statis- (r < 0.01), and only weakly (r = 0.51) with tical comparisons were performed, the LED dew point. Mean specimen abundance for all lights collected a greater overall number of orders combined was not different between insect orders than fluorescent lights. Both of sampling locations. The Ephemeroptera these studies tested LED bulbs of ~395 nm. and Trichoptera, however, both had higher mean specimen abundance at the 2 most Our results also suggested that subtle downstream sampling sites (Table 3). wavelength differences within the long- wave ultraviolet spectrum were generally Discussion not important in attracting night-flying insects with LED lights. Ours appears to be Our results clearly indicated the vi- the first study to specifically address these ability of LEDs in catching night-flying in- differences within the ultraviolet spectrum. sects, as both specimen abundance and order Previous studies either tested a single ultra- richness were comparable to that of fluores- violet wavelength (typically ~395 nm) or else cent ultraviolet lights. This result is similar compared ultraviolet LEDs to white LEDs to that of Green et al. (2012), who found no (Green et al. 2012, Pawsen and Bader 2014, significant difference in the total number of Price and Baker 2016). Although there were specimens caught between ultraviolet LED some differences in specimen abundance
Table 2. Mean number of specimens from the 7 most abundant insect orders based on collecting date for all lights tested. Asterisks represent statistically distinct groups of means based on a 1-way Analysis of Variance with a post-hoc Tukey test. Weather data from www.wunderground.com. 19 July 21 July 22 July 25 July 26 July p Maximum temperature 26.1 28.3 32.2 27.8 29.4 N/A Dew point 11.7 19.4 17.2 17.3 14.4 N/A Coleoptera 6.0b 101.6a 26.8b 7.6b 10.3b <0.01 Diptera 123.7b 610.0a 173.8b 167.8b 129.8b <0.01 Ephemeroptera 10.3ab 5.2b 17.5ab 24.5a 6.7ab 0.03 Homoptera 53.3b 169.6a 145.4a 54.5b 65.4b <0.01 Hymenoptera 2.8b 47.5a 5.8b 3.6b 4.8b <0.01 Lepidoptera 103.2b 927.2a 159.5b 138.7b 140.3b <0.01 Trichoptera 95.4b 247.4a 126.2b 90.8b 116.8b <0.01 Combined 394.7b 2108.5a 655b 487.5b 474.1b <0.01
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p 0.86 0.63 0.59 0.99 0.99 0.83 0.01 0.04
b b
7.6 9.2 12 36.8 211.6 133.4 402.6 159.4 960.6
b b
5.6 11 26.6 99.4 13.4 266.0 358.6 100.2 869.8
b b
6.4 7.8 10 11.0 78.8 124.8 151.4 136.6 516.8
b b
9 6.6 14.0 78.8 14.0 163.8 167.8 108.4 553.4
b b
8 8.2 16.0 65.2 12.8 98.8 175.4 307.4 683.8
b b
7 24.4 70.2 14.4 10.4 96.2 197.8 217.6 630.9
b b
6 7.0 33.2 91.6 15.2 242.2 254.0 125.8 769.0
b b
5 8.8 25.8 90.8 20.0 310.0 370.4 102.2 928.0
b b
4 26.6 76.4 10.6 10.8 95.4 147.0 258.6 625.4
b b
3 45.8 15.6 12.0 269.6 116.4 341.8 100.8 902.0
ab b
2 39.2 11.4 28.0 252.8 112.8 329.4 151.4 925.0
a a
1 66.0 14.2 42.4 531.2 157.8 348.8 365.4 1525.8
Table 3. Mean number of specimens from the 7 most abundant insect orders based on sampling location for all lights tested during 5 nights our study. Asterisks represent statistically distinct groups of means based on a 1-way Analysis Variance with post-hoc Tukey test. Lower-numbered sites were downstream of higher-numbered sites. Sampling location Coleoptera Diptera Ephemeroptera Homoptera Hymenoptera Lepidoptera Trichoptera Combined
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between our ultraviolet wavelengths, these between LED and fluorescent bulbs, howev- differences were not significant and were er, as well as the nearly identical intensity much smaller than differences between values of the 2 fluorescent bulbs do suggest collecting dates. Specific trap placement light intensity differences between the 2 was also more important than wavelength bulb types and, possibly, between some of for the aquatic orders Ephemeroptera the LED bulbs. Such differences may have and Trichoptera. This observation is not affected insect catch. Lastly, information on surprising considering the importance of potential UV light attenuation by the HDPE stream microhabitat in affecting aquatic tubes that we used for light housings was not insect distributions (Houghton and Wasson available. Better quality control and infor- 2013). These results collectively suggest that mation would allow us to view our results natural variation in field conditions are more with greater confidence. important in affecting trap catches than the Further research will be needed to ad- specific ultraviolet wavelength that we used. dress the potential lower bycatch of Diptera Longcore et al. (2015) similarly found that with particular wavelengths, as well as any collecting site, temperature, and humidity other potential specific responses in other were as important in attracting insect spec- insect orders. Further, while we noticed imens as was spectral composition of the no loss of light intensity during our 2-hour white LEDs. field trials, preliminary research suggested It is not clear why our LED lights a loss of such intensity during longer trials. generally caught fewer specimens of Diptera Thus, battery life may need to be addressed than did the fluorescent ultraviolet light. for longer field situations. Lastly, a center Trends in most of our data exhibited a bimod- tube composed of aluminum instead of PVC al distribution: high specimen abundance at may be necessary for longer trials to combat 380 nm, low at 390, and high again at 403 potential heat build-up. and with the fluorescent ultraviolet light. Despite these potential issues, our For most data, however, results were not LED collecting light was as effective as a statistically significant. Chironomid midg- commercially available fluorescent ultravi- es were present in large numbers during olet light in collecting night-flying insects. several sampling nights. It may be that the Our lights are ~1/5th of the cost of such lights, statistical significance of the Diptera data is <1/20th of the weight when factoring in both simply due to the larger numbers increasing light and power supply, run on self-contained the statistical power of the test (Zar 2010). AA batteries, and are fairly easy to build. Numbers of Lepidoptera specimens, howev- Several can easily be carried in a backpack er, were even higher than those of Diptera, to remote collecting sites. Thus, these lights and yet did not exhibit a significant differ- appear to be viable alternatives to ultraviolet ence between wavelengths. fluorescent lights. It is possible that the 15m space be- tween our traps led to some overlapping Acknowledgments attraction. Van Grusven et al. (2014) found that a 5w fluorescent light attracted Lepi- We thank Emma Elsenheimer, Paul doptera specimens released up to 50m away Hosmer, Joel Parker, and Claire Schumock from it. They also found that that attraction for their assistance in the field and labora- decreased markedly as distance increased tory. Research costs were supported by the from 10m to 25m, suggesting that any over- Hillsdale College biology department. This lapping attraction between our traps was paper is #19 of the G.H. Gordon BioStation fairly minor. Research Series. Some potential sources of error existed within our study, primarily due to the com- Literature Cited mercial, rather than scientific, origin of our Brakel, K., L.R. Wassink, and D.C. Houghton. light components. First, it was not possible to 2015. Nocturnal flight periodicity of cad- obtain detailed specification data or quality disflies (Trichoptera) in forest and meadow control information about our LED bulbs, as habitats of a first order northern Michigan they were unbranded and shipped directly stream. The Great Lakes Entomologist 48: from the People’s Republic of China via www. 34–44. ebay.com. As mentioned earlier, only about half of the bulbs that we received emitted Chen, T., C. Chu, G. and T.J. Henneberry. their advertised ultraviolet wavelength. The 2004. Monitoring and trapping insects on effect of bulb light intensity was not clear, poinsettia with yellow sticky card traps as we were not able to calibrate our spectro- equipped with light-emitting diodes. Hort- photometer within acceptable tolerances to Technology 14: 337–341. obtain absolute intensity data between bulbs Chu, C., C.G. Jackson, P.J. Alexander, K. (Fig. 2). The order of magnitude difference Karut, and T.J. Henneberry. 2003. Plastic
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cup traps equipped with light-emitting diodes Philosophical Transactions of the Royal for monitoring adult Bemisia tabaci (Ho- Society B 370: 20140125. moptera: Aleyrodidae). Journal of Economic The effec- Entomology 96: 543–546. Nakamoto, Y., and H. Kuba. 2004. tiveness of a green light emitting diodes Green, D., D. Mackay, and M. Whalen. 2012. (LED) trap at capturing the West Indian Next generation insect light traps: the use of sweet potato weevil, Euscepes postfasciatus LED light technology in sampling emerging (Falmaire) (Coleoptera: Curculionidae) in a aquatic macroinvertebrates. The Australian sweet potato field. Applied Entomology and Entomologist 39: 189–194. Zoology 39: 491–495. Houghton, D.C. 2015. A 5-year study of 27 species of caddisflies (Trichoptera) in forest Pawson, S.M., and M.F. Bader. 2014. LED and meadow habitats of a first-order Mich- lighting increases the ecological impact of igan stream. Environmental Entomology night pollution irrespective of color tempera- 44:1472–1487. ture. Ecological Applications 24: 1561–1568. Houghton, D.C, and J.L. Wasson. 2013. Price, B., and E. Baker. 2016. NightLife: a Abrupt biological discontinuity in a first- cheap, robust, LED based light trap for order Michigan stream due to riparian can- collecting aquatic insects in remote areas. opy loss. Journal of Freshwater Ecology 28: Biodiversity Data Journal 4: e7648. 293–306. Van Grunsven, R.H.A., L. Dechen, Van Gef- Longcore, T., H.L. Aldern, J.F. Eggers, S. fen, K.G., and E.M. Veenendaal. 2014. Flores, L. Franco, E. Hirshfield-Yaman- Range of attraction of a 6-W moth light trap. ishi, L.N. Petrinec, W.A. Yan. and A.M. Experimentalis et Applicata 152: 87–90. Barroso. 2015. Tuning the white light spectrum of light emitting diode lamps to Zar, J.H. 2010. Biostatistical Analysis, 5th edition. reduce attraction of nocturnal arthropods. Englewood Cliffs (NJ): Prentice-Hall.
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Insect Visitors of Cirsium pitcheri, a Threatened and Endemic Dune Species, in Relation to Annual Weather Variation Jordan M. Marshall Department of Biology, Indiana University-Purdue University Fort Wayne, Fort Wayne, IN 46805.
Abstract Cirsium pitcheri (Torr. ex Eaton) Torr. & A. Gray (Pitcher’s thistle) is a threatened herbaceous plant endemic to sand dune ecosystems along Lakes Huron, Michigan, and Su- perior in North America. Habitat for this plant is limited to active dunes with moving sand. I observed floral visitors ofC. pitcheri in Indiana Dunes National Lakeshore and Indiana Dunes State Park, and calculated frequency and density of visitor families. Additionally, I tested for relationships between visitor counts and previous growing season mean temperature and precipitation. Formicidae, Anthomyiidae, and Cecidomyiidae were the most frequent families. However, Apidae was the only family correlated with the number of subsequent C. pitcheri seedlings. Counts of mean visitors per plant were different between years, with 2013 being the lowest. These values were related to previous growing season precipitation, which was lowest in 2012 due to a widespread severe drought. There was clear depression of floral visitor frequency and density following the 2012 drought, but that was short-lived and subsequent years displayed recovery of visitor numbers. Many of the floral visitors of C. pitcheri are likely feeding on nectar, pollen, and vegetative structures, and providing minimal, if any, pollination benefit. However, families such as Apidae and Halictidae carry visible pollen loads between multiple individual plants. Pollinator augmentation with these families may benefit C. pitcheri reproduction, especially following years of drought. Keywords: Apidae, Pollinators, Pitcher’s thistle, sand dunes
Open sand dune ecosystems along the the Great Lakes. The range for C. pitcheri Great Lakes shoreline in North America are includes dunes along Lakes Huron, Mich- exceedingly sensitive to various anthropo- igan, and Superior, in Indiana, Michigan, genic disturbances including residential and Wisconsin, USA, and Ontario, Canada (Voss recreational development and activities (van 1996, Higman and Penskar 1999, Indiana Dijk and Vink 2005). This sensitivity is due Department of Natural Resources 2007, to the existing repeated natural disturbances Wisconsin Department of Natural Resourc- to which specialized plant communities have es 2015, Global Biodiversity Information developed composed of species adapted to Facility 2016). Historically, C. pitcheri did exploit limited resources (Moreno-Casaso- occur along the Lake Michigan shoreline in la 1986, Maun 1998, Maun and Perumal Illinois, USA, but those populations were 1999, Lichter 2000, Bach 2001). When that extirpated as a result of land development continual sand movement related to dune and have subsequently been reintroduced development and maintenance is altered or (United States Fish and Wildlife Service halted, new species can colonize the area 2001, Illinois Endangered Species Protection displacing those native, specialized plants Board 2015). As a result of the rarity of C. (Marshall et al. 2008). Successful ecological pitcheri and its necessary habitat, as well as restoration efforts have focused on mimick- the sensitivity of both the species and habi- ing natural succession within dunes (Emery tat, the United States Fish and Wildlife Ser- and Rudgers 2009). With alteration of Great vice listed C. pitcheri as a threatened species Lakes sand dune ecosystems comes the al- (i.e. likely to become endangered within the teration of limited habitat for rare species foreseeable future) in 1988 (United States that only occur in those dunes. Fish and Wildlife Service 2001). One of those rare plant species is Cirsium pitcheri has an extended mat- Cirsium pitcheri (Torr. ex Eaton) Torr. & A. uration period (5–8 years) between seedling Gray (Asteraceae, Pitcher’s thistle), which is establishment and a single flowering event, endemic to the sand dune ecosystems along after which the plant senesces (United States Fish and Wildlife Service 2002). Typically, C. pitcheri occurs in areas with increased Email: [email protected] bare sand (less neighboring vegetation)
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Figure 1. Indiana Dunes National Lakeshore and Indiana Dunes State Park with blowout locations used for Cirsium pitcheri surveys in Porter County, Indiana, USA.
compared to more stabilized areas and in ecological importance of these families in C. dune blowouts, as a result of active sand pitcheri populations. The objectives of this movement (Bowles et al. 1990, McEachern study were to 1) survey the insect visitors et al. 1994, Marshall 2014, Jolls et al. 2015). of C. pitcheri within established populations Consequently, burial and cold stratification in Indiana Dunes National Lakeshore and are required for successful C. pitcheri seed Indiana Dunes State Park, 2) quantify the germination (i.e. Chen and Maun 1998, subsequent seedling presence as a surrogate 1999; Hamzé and Jolls 2000). As such, not for seed viability, 3) identify relationships only is C. pitcheri limited in distribution to between insect visitation, seedling counts, Great Lakes dunes, but it is also limited in and local growing season weather, and 4) distribution within those rare and sensitive test the hypotheses that weather patterns ecosystems (Higman and Penskar 1999, influence floral visitation and that certain Marshall 2014). Floral and seed herbivory insect taxa are more important to the success add to limitations in distribution (Havens of C. pitcheri reproduction. et al. 2012, Marshall 2013). Patterns of C. pitcheri occurrence within dunes are likely Methods also limited by seed dispersing within 1.5–4 m from the parental plant and seed bank Indiana Dunes National Lakeshore persisting two years maximum (i.e. Keddy and Indiana Dunes State Park (henceforth and Keddy 1984, Bowles et al. 1993, Rowland IDNL and IDSP, respectively) are adjacent and Maun 2001, Jolls et al. 2015). protected areas along Lake Michigan in By quantifying insect visitors to flow- Indiana, USA (Fig. 1). IDNL is managed ers and their effectiveness in pollination of by the National Park Service and covers C. pitcheri, we can better understand the approximately 24 km of shoreline and 6,070
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Table 1. Insect families observed visiting Cirsium pitcheri individual plants during 2012-2015 and calculated frequencies (total number of plants visited by a family), densities (number of individuals per plant [N = 61]), and correlation between number of individuals observed and subsequent year C. pitcheri seedling count within 4 m of focal survey plants. Asterisk (*) indicates significant p-value. Order Family Frequency Density r p Coleoptera Chrysomelidae 11 0.26 –0.03 0.795 Curculionidae 10 0.25 –0.17 0.199 Melyridae 8 0.43 –0.19 0.139 Scarabaeidae 1 0.02 –0.12 0.360 Diptera Anthomyiidae 24 0.90 0.10 0.449 Calliphoridae 2 0.03 0.05 0.702 Cecidomyiidae 22 0.67 –0.06 0.657 Syrphidae 15 0.89 –0.17 0.186 Hemiptera Cicadellidae 1 0.02 0.05 0.704 Pentatomidae 2 0.03 0.04 0.768 Hymenoptera Apidae 16 0.79 0.34 0.007* Formicidae 25 1.69 –0.11 0.409 Halictidae 14 0.41 –0.10 0.463 Orthoptera Acrididae 1 0.02 0.17 0.181
ha in area. IDSP is managed by the Indiana between density of flowering individuals Department of Natural Resources and covers within 4 m radius of focal plant and number approximately 5 km of shoreline and 883 ha of floral visitors. Analysis of variance (ANO- in area. Both properties include active sand VA) with Tukey’s HSD as a post-hoc test was dunes and hardwood forests. used to compare mean count of visitors per Populations of C. pitcheri were se- plant between survey years. Simple linear lected, one in each IDNL and IDSP, within regression was used to test for relationships two well established blowout features (Fig. between mean count of visitors per plant 1). Each year (2012–2015), ten flowering C. and previous year growing season weather pitcheri individuals were selected randomly (total precipitation and mean temperature). from the population. If ten individuals could Pearson correlation was used to test for rela- not be located, then all flowering individ- tionships between insect family counts at the uals were selected. During July of each focal plant and subsequent year C. pitcheri year, selected C. pitcheri individuals were seedling counts. observed for 10 minutes on two consecutive days during a 4-hour time bracket centered Results on solar noon. All insect floral visitors were identified to family. Prior to observation, At IDNL, 10 flowering individuals all flowering C. pitcheri individuals were were observed in 2012, 2013, and 2014. counted within a 4 m radius plot centered on However, no plants were included at IDNL the selected individual. In subsequent years in 2015 due to permit application delays. (including 2016 for the 2015 focal flowers), At IDSP, 10 flowering individuals were ob- first-year seedlings were counted within a 4 served in 2012, six in 2013, nine in 2014, and m radius plot centered on each focal flower six in 2015. Density of flowering individuals location, which is the maximum distance within a 4 m radius plot was significantly seedlings are typically found from the parent greater in IDNL compared to IDSP (2.6 [SE plant (Keddy and Keddy 1984). Frequency 0.8] vs. 0.8 [SE 0.2]; t = 2.27; df = 59; P = (number of observed plants visited) and 0.014). However, there was no difference in density (number of individuals visiting each count of first year seedlings within 4 m of the observed plant) were calculated for each observation plant location between parks (t family observed. Previous year’s weather = 1.21; df = 59; P = 0.232). was summarized for the growing season A total of 14 insect families were (March–September) as total precipitation observed visiting C. pitcheri plants during and mean temperature (National Oceanic survey years (Table 1, Fig. 2). While IDNL and Atmospheric Administration 2016). and IDSP had different densities of flowering T-test was used to compare mean total C. pitcheri individuals, the number of floral number of C. pitcheri flowering and first visitors was not related to flowering density year seedlings between IDNL and IDSP (F = 1.44; df = 1, 59; P = 0.235, R2 = 0.02). within the 4 m radius plots. Simple linear Mean count of insect visitors per plant was regression was used to test for relationships significantly different between years, with
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Figure 2. Example of floral visitors onCirsium pitcheri. A: Apidae. B: Halictidae.
2013 having the fewest visitors (Fig. 3A). In (Fig. 3B). Of the observed families, only 2013, Anthomyiidae, Apidae, and Calliph- Apidae counts were significantly correlated oridae had only one occurrence. The other with subsequent year seedling counts (Table families occurring in 2013 included Ceci- 1). All observed Apidae individuals were domyiidae, Chrysomelidae, Curculionidae, Bombus spp. Formicidae, and Halictidae (6, 4, 4, 25, 5 occurrences each, respectively). Mean visits Discussion per plant was not significantly related to previous growing season mean temperature Habitat for C. pitcheri is limited to (F = 3.02; df = 1,2; P = 0.225). However, mean sensitive sand dune ecosystems along Lakes visits per plant was significantly related to Huron, Michigan, and Superior, in North previous growing season total precipitation America (Voss 1996). Within IDNL and
Figure 3. A: Mean count of insect visits per Cirsium pitcheri plants between survey years. Error bars represent standard error. Unique letters represent significant differences between years with Tukey’s HSD. B: Simple linear regression of mean count of visits per C. pitcheri plants by total precipitation from previous growing season. Dashed lines represent 95% confidence intervals.
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IDSP, as with other dune systems in the this drought on the floral visitors was clear Great Lakes region, C. pitcheri is limited in 2013. Subsequent years (2014 and 2015) to blowout features with areas of active dis- illustrated recovery as the drought lessened turbance (Bowles et al. 1990, McEachern et in the region after 2012. The pattern of mean al. 1994, Marshall 2014, Jolls et al. 2015). visitors per plant was not significantly re- While not quantified for this study, IDNL lated to the previous growing season mean areas surveyed had lower overall plant temperature, but was linearly related to the cover compared to IDSP areas surveyed, mean precipitation of the previous growing which likely explains the greater density of season. Scarcity of Apidae (specifically flowering neighbors around observational Bombus spp.) in Europe has been observed plants in IDNL. and linked to drought conditions (Rasmont Seed predation, by both vertebrate and and Iserbyt 2012). Pollination success in C. invertebrate animals, and floral feeding by pitcheri may be severely impacted following agricultural pests likely have significant major drought events when floral visitor impact on C. pitcheri reproduction success populations are suppressed. (Loveless 1984, Phillips and Maun 1996, In this study, I used seedling counts Havens et al. 2012, Marshall 2013). Also, from the following year as a surrogate for mortality rates are relatively high in juvenile pollination success. There is little persistent stages (D’Ulisse and Maun 1996). Adding to seed bank for C. pitcheri (Bowles et al. these obstacles, many of the insect families 1993). While the majority of new individ- observed in this study have rather limited uals establish as the result of germination effectiveness in pollination. Neither the from the previous year’s seed crop, there is two families with the greatest frequencies potential for a short-lived seed bank (Jolls and densities (Formicidae and Anthomyii- et al. 2015). However, one limitation for dae), nor the third most frequent family this study was the higher density of other (Cecidomyiidae), are known to be effective flowering C. pitcheri individuals at some pollinators. Formicidae can negatively affect locations at INDL compared to INSP, which pollination efficacy and has been omitted would have added to the seed bank for the in counts from previous studies regarding following spring germination. Because of the C. pitcheri pollination (Beattie et al. 1984, presence of other floweringC. pitcheri during Baskett et al. 2011). Anthomyiidae and Ceci- the course of this study, the correlations domyiidae are common fly families and have between Apidae individuals and neighboring been found as stem and flower head feeders seedling establishment should be interpreted in other thistles (Gassman and Kok 2002). conservatively. Quantifying pollen loads Within the same family as C. pitcheri (As- carried by individual visitors would likely teraceae), Anthomyiidae individuals cause add a layer of confidence to measuring visi- feeding damage in flowers (Anderson 1996). tor roles in pollination. Additionally, pollen Additionally, Cecidomyiidae are known contamination rates from other species on to frequent small tubular flowers found visitors may also aid in measuring such in Asteraceae (Larson et al. 2001). While roles. Collecting seed from senescing flowers these three families had high frequency and following successful pollination would have density values, they were not significantly also added to this measure. However, inter- correlated with subsequent year seedlings, fering with successful pollination (measuring likely because of their lack of pollination pollen loads and contamination) or dispersal activity. (collecting seeds) could pose an undue bur- Apidae was the only family that was den on an already rare population. Overall, significantly correlated with subsequent these limitations add external factors that year seedling counts. This family carries complicate the interpretation of pollinator obvious pollen loads and visibly move from visitation and seedling success in C. pitcheri C. pitcheri individual to individual (personal (i.e. seed predation, mate densities, residual observations). While Halictidae visitation seed bank). However, pollinator visitation was not correlated with seedling counts, it rates have some influence on seedling suc- is another family that carries visible pollen cess and provides initial insight regarding loads and moves directly between C. pitch- the success of C. pitcheri. eri individuals. Additionally, both of these Because of the limited distribution of families are known important pollinators suitable habitat and individuals within that in Asteraceae, including C. pitcheri (Olsen suitable habitat, C. pitcheri may benefit from 1997, Theis et al. 2007, Baskett et al. 2011,). augmenting local pollinator communities. During 2012, much of the United Lab rearing and releasing native pollinator States, including the Great Lakes region, species, specifically Bombus spp. in the experienced a significant drought that family Apidae, may improve pollination had widespread impact on agricultural success and subsequent seed production. systems (Mallya et al. 2013). The effect of Augmentation may be especially beneficial
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after drought years where naturally occur- the Great Lakes region. Restoration Ecology ring floral visitors are suppressed. 18:184–194. Gassman, A., and L.T. Kok. 2002. 18 Musk This- Acknowledgments tle (Nodding Thistle), pp. 229–246.InR. Van Driesch, B. Blossey, M. Hoddle, S. Lyon, and I would like to thank Noel Pavlovic (US R. Reardon (tech. coords.), Biological Control Geological Survey) for assistance in locating of Invasive Plants in the Eastern United plant populations. Surveys were conducted States. FHTET-2002-04. USDA Forest Ser- under permits INDU-2012-SCI-0007, IN- vice, Forest Health Technology Enterprise DU-2013-SCI-0008, INDU-2014-SCI-0004 Team, Morgantown, WV. at Indiana Dunes National Lakeshore; and NP12-28, NP13-15 at Indiana Dunes Global Biodiversity Information Facility. State Park. I also would like to thank the 2016. Cirsium pitcheri (Torr. ex Eaton) anonymous reviewers for their comments Torr. & A. Gray. GBIF Backbone Taxon- improving this manuscript. omy. Available from http://www.gbif.org/ species/3113668 (accessed 6 Oct 2017). Literature Cited Hamzé, S. I., and C. L. Jolls. 2000. Germination ecology of a federally threatened endem- Anderson, S. 1996. Floral display and pollination ic thistle, Cirsium pitcheri, of the Great success in Senecio jacobaea (Asteraceae): Lakes. The American Midland Naturalist Interactive effects of head and corymb size. 143:141–153. American Journal of Botany 83:71–75. Havens, K., C. L. Jolls, J. E. Marik, P. Vitt, Bach, C. E. 2001. Long-term effects of insect her- A. K. McEachern, and D. Kind. 2012. bivory and sand accretion on plant succession Effects of a non-native biocontrol weevil, on sand dunes. Ecology 82:1401–1416. Larinus planus, and other emerging threats on populations of the federally threatened Baskett, C. A., S. M. Emery, and J. A. Rudgers. Pitcher’s thistle, Cirsium pitcheri. Biological 2011. Pollinator visits to threatened species Conservation 155:202–211. are restored following invasive plant remov- al. International Journal of Plant Science Higman, P. J., and M. R. Penskar. 1999. Special 172:411–422. Plant Abstract for Cirsium pitcheri. Michigan Natural Features Inventory. Available from Beattie, A. J., C. Turnbull, R. B. Knox, and E. https://mnfi.anr.msu.edu/abstracts/botany/ G. Williams. 1984. Ant inhibition of pollen Cirsium_pitcheri.pdf (accessed 6 Oct 2017). function: A possible reason why ant polli- nation is rare. American Journal of Botany Illinois Endangered Species Protection 71:421–426. Board. 2015. Checklist of Illinois Endan- gered and Threatened Animals and Plants. Bowles, M. L., M. M. DeMauro, N. Pavlovic, Available from http://www.dnr.illinois. and R. D. Hiebert. 1990. Effects of anthro- gov/ESPB/Documents/2015_ChecklistFI- pogenic disturbances on endangered and NAL_for_webpage_051915.pdf (accessed 6 threatened plants at the Indiana Dunes Oct 2017). National Lakeshore. Natural Areas Journal 10:187–200. Indiana Department of Natural Resources. 2007. Endangered, Threatened, Rare and Bowles, M., R. Flakne, K. McEachern, and Extirpated Plants of Indiana. Available from N. Pavlovic. 1993. Recovery planning and http://www.in.gov/dnr/naturepreserve/files/ reintroduction of the federally threatened etrplants.pdf (accessed 6 Oct 2017). Pitcher’s thistle (Cirsium pitcheri) in Illinois. Natural Areas Journal 13:164–176. Jolls, C. L., J. E. Marik, S. I. Hamzé, and K. Havens. 2015. Population viability analysis Chen, H., and M. A. Maun. 1998. Population and the effects of light availability and litter ecology of Cirsium pitcheri on Lake Huron on populations of Cirsium pitcheri, a rare, sand dunes. III. Mechanisms of seed dorman- monocarpic perennial of Great Lakes shore- cy Canadian Journal of Botany 76:575–586. lines. Biological Conservation 187: 82–90. Chen, H., and M. A. Maun. 1999. Effects of Keddy, C. J., and P. A. Keddy. 1984. Reproduc- sand burial depth on seed germination and tive biology and habitat of Cirsium pitcheri. seedling emergence of Cirsium pitcheri. Plant The Michigan Botanist 23:57–67. Ecology 140:53–60. Larson, B. M. H., P. G. Kevan, and D. W. D’Ulisse, A., and M. A. Maun. 1996. Population Inouye. 2001. Flies and flowers: taxonomic ecology of Cirsium pitcheri on Lake Huron diversity of anthophiles and pollinators. The sand dunes: II. Survivorship of plants. Ca- Canadian Entomologist 133:439–465. nadian Journal of Botany 74: 1701–1707. Lichter, J. 2000. Colonization constraints during Emery, S. M., and J. A. Rudgers. 2009. Eco- primary succession on coastal Lake Michigan logical assessment of dune restorations in sand dunes. Journal of Ecology 88:825–839.
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Loveless, M. D. 1984. Population Biology and Olsen, K. M. 1997. Pollination effectiveness and Genetic Organization in Cirsium pitcheri, pollinator importance in a population of Het- an endemic thistle. Ph.D. dissertation, Uni- erotheca subaxillaris (Asteraceae). Oecologia versity of Kansas, Lawrence, Kansas, USA. 109:114–121. Mallya, G., L. Zhao, X. C. Song, D. Niyogi, and Phillips, T., and M. A. Maun. 1996. Population R. S. Govindaraju. 2013. 2012 midwest ecology of Cirsium pitcheri on Lake Huron drought in the United States. Journal of sand dunes I. Impact of white-tailed deer. Hydrologic Engineering 18:737–745. Canadian Journal of Botany 74: 1439–1444. Marshall, J. M. 2013. Occurrence of Diabrotica Rasmont, P., and S. Iserbyt. 2012. The bum- undecimpunctata howardi Barber (Coleop- blebees scarcity syndrome: are heat waves tera: Chrysomelidae) feeding on Cirsium leading to local extinctions of bumblebees pitcheri flowers. The Great Lakes Entomol- (Hymenoptera: Apidae: Bombus)? Annales ogist 46:138–141. de la Société entomologique de France Marshall, J. M. 2014. Influence of topography, 48:275–280. bare sand, and soil pH on the occurrence and Rowland, J., and M. A. Maun. 2001. Restoration distribution of plant species in a lacustrine ecology of an endangered plant species: es- dune ecosystem. Journal of the Torrey Bo- tablishment of new populations of Cirsium tanical Society 141:29–38. pitcheri. Restoration Ecology 9:60–70. Marshall, J. M., A. J. Storer, and B. Leutscher. Theis, N., M.Lerdau, and R. A. Raguso. 2007. 2008. Comparative analysis of plant and The challenge of attracting pollinators ground dwelling arthropod communities in while evading floral herbivores: patterns of lacustrine dune areas with and without Cen- fragrance emission in Cirsium arvense and taurea biebersteinii (Asteraceae). American Cirsium repandum (Asteraceae). Internation- Midland Naturalist 159:261–274. al Journal of Plant Sciences 168:587–601. Maun, M. A. 1998. Adaptations of plants to burial United States Fish and Wildlife Service. 2001. in coastal sand dunes. Canadian Journal of Pitcher’s Thistle Fact Sheet. Available from Botany 76:713–738. http://www.fws.gov/midwest/endangered/ Maun, M. A., and J. Perumal. 1999. Zonation of plants/pdf/Pitchersthistle.pdf (accessed 6 vegetation on lacustrine coastal dunes: effects Oct 2017). of burial by sand. Ecology Letters 2:14–18. United States Fish and Wildlife Service. 2002. McEachern, A. K., M. L. Bowles, and N. B.Pav- Pitcher’s Thistle (Cirsium pitcheri) Recovery lovic. 1994. A metapopulation approach to Plan. Fort Snelling, Minnesota. Pitcher’s thistle (Cirsium pitcheri) recovery in southern Lake Michigan dunes, pp. 194–218. van Dijk, D., and D. R. Vink. 2005. Visiting a In M. L. Bowles and C. J. Whelan (eds.), Res- Great Lakes sand dune: the example of Mt. toration of Endangered Species. Cambridge Pisgah in Holland, Michigan. The Great University Press, Cambridge. Lakes Geographer 12:45–63. Moreno-Casasola, P. 1986. Sand movement as Voss, E. G. 1996. Michigan Flora. Part III. Dicots a factor in the distribution of plant communi- (Pyrolaceae-Compositae). The Cranbrook In- ties in a coastal dune system. Plant Ecology stitute of Science Bulletin 61 and University 65:67–76. of Michigan Herbarium, Ann Arbor, MI. National Oceanic and Atmospheric Adminis- Wisconsin Department of Natural Resources. tration. 2016. Monthly Summaries Station 2015. Wisconsin Endangered and Threatened Details. Available from http://www.ncdc. Species Laws & List. Madison, WI. PUBL- noaa.gov/cdo-web/datasets/GHCNDMS/sta- ER-001. Available from http://dnr.wi.gov/ tions/GHCND:USC00124244/detail (accessed files/PDF/pubs/er/ER001.pdf (accessed 6 6 Oct 2017). Oct 2017).
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Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) Observed Feeding on Chamaesaracha sp. in Eastern Colorado. Michael S. Crossley*, Benjamin Pélissié, Zachary Cohen, and Sean D. Schoville Department of Entomology, University of Wisconsin-Madison, Madison, WI, 53706
Abstract Egg, larval, and adult life stages of Colorado potato beetle, Leptinotarsa decemlin- eata (Say), were observed feeding on or attached to a previously undocumented host plant belonging to the genus Chamaesaracha in eastern Colorado on July 2017. At one site, L. decemlineata were more abundant on Chamaesaracha sp. than the accepted ancestral host plant, Solanum rostratum (Dunal). While future studies should confirm the ancestral sta- tus of the observed L. decemlineata and suitability of Chamaesaracha sp. for completion of development, our observations suggest a need for further characterization of the ancestral host range of L. decemlineata. Keywords: Colorado potato beetle, host plant, ancestral range
The Colorado potato beetle, Leptino- Mexican L. decemlineata belong to a highly tarsa decemlineata (Say) (Coleoptera: divergent genetic lineage (Izzo et al. 2017). Chrysomelidae), is a globally distributed Since it became a pest of potato crops, agricultural pest and specialist of plants in L. decemlineata has been observed utilizing the family Solanaceae (Tower 1906, Hsiao several other cultivated and uncultivated So- et al. 1978, Jacques 1988). Prior to 1859, L. lanaceaous plants (Hare 1900, Latheef and decemlineata (then called Doryphora 10-lin- Harcourt 1974, Hsiao et al. 1978, Whitaker eata) was only known from the observations 1994, Mena-Covarrubias et al. 1996, Horton of Thomas Nuttall and Thomas Say of the et al. 1988), making it a potential model for leaf beetle apparently feeding on buffalo research on rapid host plant adaptation. bur, Solanum rostratum (Dunal), along the However, it is uncertain whether the pro- Missouri River somewhere between the pensity for adaptation to new host plants Platte and Yellowstone Rivers (Casagrande is novel and unique to pest lineages or if 1985). Since then, L. decemlineata has in- ancestral populations have already been corporated potato (Solanum tuberosum (L.)) utilizing multiple plant species. The role of into its host range and rapidly spread across S. rostratum as the ancestral host plant of potato-growing regions of the USA (including L. decemlineata has not been questioned in the Great Lakes region), Europe, and parts the literature. Here we report observations of of east Asia (Walsh 1866, Riley 1869, Grap- L. decemlineata in eastern Colorado feeding puto et al. 2005, Liu et al. 2012). There has and ovipositing on a previously undocument- been considerable discussion concerning the ed host plant in the genus Chamaesaracha, origin of pest lineages of L. decemlineata. and discuss potential implications for our Several authors have suggested a Mexican understanding of L. decemlineata host plant origin (Hsiao 1981; Jacobson and Hsiao adaptation. 1983; Casagrande 1985, 1987; Lu and Lazell 1996), due to high levels of observed genetic diversity among Mexican L. decemlineata Materials and Methods and the Central American distribution of Observations were made of host plant several other Leptinotarsa species (Jacques associations of L. decemlineata in eastern 1988). Others suggest an origin in the east- Colorado in July 2017. Visited areas included ern foothills of the Rocky Mountains, noting Pawnee and Comanche National Grasslands, the early observations of Nuttall and Say and areas where L. decemlineata had previously the first outbreak on potato in the plains of been observed on S. rostratum (W. Cranshaw Nebraska (Walsh 1865). Recent population and A. Norton, pers. comm.). Photos were genetic data provide compelling evidence for taken of host plants, and identification of the Great Plains origin, and suggest that Chamaesaracha plants was confirmed by the Wisconsin State Herbarium. Voucher *Corresponding author: (email: mcrossley@wisc. specimens of adult L. decemlineata are being edu) maintained (kept in 100% ethanol at –20°C)
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absent utilized present/ present/ significantly Chamaesaracha
not absent absent present/ Host plant associations S. elaeagnifolium
barely utilized utilized present/ present/ present/ rostratum S.
Date 7/19/17 7/19/17 7/20/17
1531 1330 1332 Elevation (m)
Lat -103.5076 -103.5891 –103.9571
Leptinotarsa decemlineata host plant associations in eastern Colorado, 2017. Lon 40.7871 37.7979 37.6331
Table 1. Observation sites of Location Pawnee Natl. Grassland Comanche Natl. Grassland (Rd.) Comanche Natl. Grassland (Picket Wire Canyon)
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Figure 1. Floral display (A) and Leptinotarsa decemlineata life stages (B, C D) on Chamaesaracha sp. Taken in Picket Wire Canyon, Comanche National Grassland, Colorado, USA on 20 July 2017.
in the Schoville laboratory at University of (Fig. 1). Notably in Picket Wire Canyon, L. Wisconsin-Madison. decemlineata were more frequently found on Chamaesaracha than on S. rostratum, Results despite the presence of large, healthy S. rostratum plants in the immediate vicinity. Leptinotarsa decemlineata were ob- The Chamaesaracha plants likely be- served at low densities on S. rostratum at long to C. conoides (Moricand ex Dunal), but three sites (Table 1). At each site, all life C. coronopus (Dunal) could not be excluded stages (except pupae) were observed feeding due to lack of measurements of distinguish- on or attached to S. rostratum. Solanum ing morphological features (M. Wetter, pers. elaeagnifolium (Cavanilles), another doc- comm.). Further investigations based on umented host plant of L. decemlineata in fresh material sampling will likely resolve southwestern USA, was equivalently abun- this uncertainty. dant as S. rostratum in Picket Wire Canyon, Comanche National Grassland. However, Previously documented host plant no L. decemlineata (nor any evidence of its associations of L. decemlineata were ob- activity) were observed on this plant during tained from Jacques (1988), Jolivet and Hawkeswood (1995), Jolivet and Verma the course of our observations. (2002), and Clark et al. (2004). Although At both Pawnee and Comanche Na- Jolivet and Hawkeswood (1995) and Clark tional Grasslands, a plant identified to genus et al. (2004) have records of Chamaesaracha Chamaesaracha was found in close proximity spp. (C. coniodes, C. coronopus, and C. sor- to S. rostratum, and all L. decemlineata life dida (Dunal)), none of them document asso- stages observed feeding on or attached to it ciations between Chamaesaracha spp. and
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L. decemlineata. The only leaf beetles Cha- Acknowledgments maesaracha spp. have been associated with are Lema daturaphila (Kogan & Goeden), L. We thank Mark Wetter and the Wis- trabeata (Lacordaire), L. trivittata (Say), and consin State Herbarium for plant identifi- Parorectis sublaevis (Barber). cation; Yolanda Chen, David Hawthorne, Whitney Chanshaw, and Andrew Norton for sampling advice. Discussion The occurrence of L. decemlineata on Literature Cited another host plant in the ancestral range raises an important question: Have ances- Casagrande, R. A. 1985. The “Iowa” potato tral lineages of L. decemlineata historically beetle, its discovery and spread to potatoes. utilized Chamaesaracha in addition to S. Bulletin of the Entomological Society of rostratum? One critical piece of evidence yet America 31: 27–29. to be ascertained is the origin of the L. dece- Casagrande, R. A. 1987. The Colorado potato mlineata associated with Chamaesaracha. beetle: 125 years of mismanagement. Bulletin If these L. decemlineata belong to the pest of the Entomological Society of America 33: lineage, their association would represent a 142–150. secondary colonization of eastern Colorado, Clark, S. M., D. G. LeDouz, T. N. Seeno, E. G. and yet one more plant added to the pest Riley, A. J. Gilbert, and J. M. Sullivan. lineage’s host range. The pest status of L. 2004. Host plants of leaf beetle species oc- decemlineata could be tested by genetic anal- curring in the United States and Canada: ysis and population assignment methods. (Coleoptera: Megalopodidae, Orsodacnidae, Our observations in Picket Wire Chrysomelidae, excluding Bruchinae), Spe- Canyon suggest Chamaesaracha might cial Publication No. 2, The Coleopterists be a preferred host plant in the putative Society, Sacramento, CA. ancestral range, as healthy and untouched Grapputo, A., S. Boman, L. Lindström, A. S. rostratum were often found next to it. Lyytinen, and J. Mappes. 2005. The voy- However, these observations could be an ar- age of an invasive species across continents: tifact of the time of year. Archives of weather genetic diversity of North American and data from the closest city (La Junta; www. European Colorado potato beetle populations. wunderground.com) document a maximum Molecular Ecology 14: 4207–4219. temperature of 37°C (98°F), which would Hare, J. D. 1900. Ecology and management of likely have been realized or exceeded at the the Colorado potato beetle. Annual Reviews time and location of observations, and it of Entomology 35: 81–100. could be that Chamaesaracha contains more Horton, D. R., J. L. Capinera, P. L. Chapman, water or is less enriched in feeding deter- D. R. Horton, J. L. Capinera, and P. L. rents relative to S. rostratum under these Chapman. 1988. Local differences in host conditions. In this case, the association with use by two populations of the Colorado potato L. decemlineata might only be transitional. beetle. Ecology 69: 823–831. Repeated reports are needed to confirm host plant utilization throughout the season and Hsiao, T. H. 1981. Ecophysiological adaptations across years. Additional experiments could among geographic populations of the Colo- also be done to verify the sufficiency ofCha - rado beetle in North America, pp. 69–85. In maesaracha for L. decemlineata development Advances in Potato Pest Management. Eds. and reproduction. J. H. Lashomb, R. Casagrande. Hutchinson Ross, New York, New York. Confirmation of the ancestral status of the observed L. decemlineata and suitability Hsiao, T. H., J. L. Capinera, and P. L. Chap- of Chamaesaracha for completion of develop- man. 1978. Host plant adaptations among ment would strongly support the hypothesis geographic populations of the Colorado po- tato beetle. Entomologia Experimentalis et that ancestral L. decemlineata lineages applicata 24: 437–447. have historically utilized Chamaesaracha in addition to S. rostratum. Historic utili- Izzo, V., Y. H. Chen, S. D. Schoville, C. Wang, zation of multiple host plants by ancestral and D. J. Hawthorne. 2017. Origin of pest populations would suggest the possibility lineages of the Colorado potato beetle, Lep- that L. decemlineata may have had genetic tinotarsa decemlineata. bioRxiv doi: https:// variation for broad host use, which could doi.org/10.1101/156612 have led to its success invading agricultural Jacobson, J. W., and T. H. Hsiao. 1983. Isozyme habitats. These observations suggest a need variation between geographic populations for further characterization of the ancestral of the Colorado potato beetle, Leptinotarsa host range of L. decemlineata. decemlineata (Coleoptera: Chrysomelidae).
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Annals of the Entomological Society of Amer- Mena-Covarrubias, J., F. A. Drummond, and ica 76: 162–166. D. L. Haynes. 1996. Population dynamics Jacques, R. L. 1988. The Potato Beetles: The of the Colorado potato beetle (Coleoptera: Genus Leptinotarsa in North America (Co- Chrysomelidae) on horsenettle in Michigan. leoptera: Chrysomelidae). E. J. Brill, New Environmental Entomology 25: 68–77. York, 144 pp. Riley, C. V. 1869. First annual report on the Jolivet, P., and T. J. Hawkeswood. 1995. noxious, beneficial and other insects, of the Host-plants of Chrysomelidae of the world: state of Missouri, Jefferson City, MO Ellwood An essay about the relationships between Kirby. leaf-beetles and their food plants. Backhuys Tower, W. L. 1906. An investigation of evolution Publishers, Leiden, The Netherlands. in Chrysomelid beetles of the genus Leptino- Jolivet, P., and K. K. Verma. 2002. Biology tarsa. Carnegie Institute of Washington, of leaf beetles. Intercept Limited, Andover, Washington, D.C. Hampshire, UK. Walsh, B. D. 1865. The new potato bug and its Latheef, M. A., and D. G. Harcourt. 1974. natural history. Practical Entomologist 1: The dynamics of Leptinotarsa decemlineata 1–4. populations on tomato. Entomologia Experi- mentalis et Applicata 17: 67–76. Walsh, B. D. 1866. The new potato bug. Practical Liu, N., Y. Li, and R. Zhang. 2012. Invasion of Entomologist 2: 13–16. Colorado potato beetle, Leptinotarsa decem- Whitaker, P. M. 1994. Agricultural and non- lineata, in China: dispersal, occurrence, and agricultural populations of the Colorado economic impact. Entomologia Experimenta- potato beetle (Leptinotarsa decemlineata lis et Applicata 143: 207–217. (Say)) in Wisconsin: studies on host plant Lu, W., and J. Lazell. 1996. The voyage of the adaptations, natural enemies, and population beetle. Natural History, American Museum dynamics. PhD thesis, University of Wiscon- of Natural History, pp. 36–39. sin-Madison.
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Arthropod Fauna Associated with Wild and Cultivated Cranberries in Wisconsin Shawn A. Steffan1,2*, Merritt E. Singleton2, Michael L. Draney3, Elissa M. Chasen1, Kyle E. Johnson2, and Juan E. Zalapa1 1USDA-ARS, Madison, WI, 53706 2Department of Entomology, University of Wisconsin-Madison, Madison, WI, 53706 3Department of Natural & Applied Sciences, University of Wisconsin-Green Bay, Green Bay, WI 54311
Abstract The cranberry (Vaccinium macrocarpon Aiton) is an evergreen, trailing shrub native to North American peatlands. It is cultivated commercially in the US and Canada, with major production centers in Wisconsin, Massachusetts, New Jersey, Washington, Québec, and British Columbia. Despite the agricultural importance of cranberry in Wisconsin, relatively little is known of its arthropod associates, particularly the arachnid fauna. Here we report preliminary data on the insect and spider communities associated with wild and cultivated cranberries in Wisconsin. We then compare the insect and spider communities of wild cranberry systems to those of cultivated cranberries, indexed by region. Approximately 7,400 arthropods were curated and identified, spanning more than 100 families, across 11 orders. The majority of specimens and diversity derived from wild ecosystems. In both the wild and cultivated systems, the greatest numbers of families were found among the Diptera (midges, flies) and Hymenoptera (bees, ants, wasps), but numerically, the Hymenoptera and Araneae (spiders) were dominant. Within the spider fauna, 18 new county records, as well as a new Wisconsin state record (Linyphiidae: Ceratinopsis laticeps Emerton), were documented. While more extensive sampling will be needed to better resolve arthropod biodiversity in North American cranberry systems, our findings represent baseline data on the breadth of arthropod diversity in the Upper Midwest, USA. Key Words: Cranberry, insect biodiversity, peatland, spider, survey, Vaccinium
Cranberry, Vaccinium macrocarpon Cranberries have been grown commer- Aiton (Ericaceae), is an evergreen trailing cially in Wisconsin for over 100 years (Eck shrub endemic to North American peat- 1990). Production is concentrated in the lands (Eck 1990). Peatlands are wetlands central portion of the state where growers that accumulate poorly decomposed organic produce approximately two-thirds of the matter (peat) and range from alkaline and nation’s cranberries (USDA NASS 2014). In minerotrophic (rich fens) to highly acidic and commercial cultivation, cranberries grow as ombrotrophic (bogs sensu stricto); they also dense monocultures, primarily in alternating range from treeless to forested (Rydin and layers of sand and detritus. Notably, culti- Jeglum 2013). These plant communities vary vated cranberry marshes exclude Sphagnum moss from the ecosystem, which almost but are usually floristically depauperate and completely carpet the ground in wild peat- dominated by Sphagnum and other mosses, lands (Rydin and Jeglum 2013). Fertilizers sedges, and ericaceous shrubs (Marshall et (N-P-K) and pesticides are added each year al. 1999). Cranberries can be found growing to maximize growth and berry production. in the wild in most Wisconsin counties, es- Cranberry beds are flooded in the spring for pecially in the central and northern portions frost protection/insect control, and again of the state (Johnson 2011, Chaddle 2013). in the fall to facilitate harvest (Eck 1990). While cranberry may dominate within rela- Thus, there are marked differences in soil tively small areas, it is often tightly associ- type, soil structure, floristic diversity, and ated with Sphagnum moss. hydrology between wild and managed cran- berry populations in Wisconsin. It stands to reason, then, that their respective fauna *Corresponding author: Dept. of Entomology, 1630 Linden Drive, University of Wisconsin, Madison, might also differ. WI, 53706, USA. (e-mail: steffan@entomology. The objective of this study was to begin wisc.edu) cataloging the arthropod diversity associat-
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Table 1. Sampling sites across central Wisconsin peatlands. Site # County Lat/Lon Habitat 1 Wood 44.38502°N/90.01452°W agricultural cranberry bed (cultivated) 2 Monroe 44.07005°N/90.40795°W agricultural cranberry bed (cultivated) 3 Monroe 44.11126°N/90.34675°W open to sparsely treed, poor fen (wild) 4 Jackson 44.31573°N/90.74091°W sparsely treed, poor fen (wild) 5 Jackson 44.27450°N/90.73953°W open, poor fen (wild)
ed with both wild and cultivated cranberry (Aronia melanocarpa (Michx.) Elliot) were systems. In doing so, we provide baseline sparse. Sporadic to sparse stunted tama- information on the fauna associated with rack (Larix laricina (Du Roi) K. Koch) was this economically important native plant. present at all sites, and one site (#4, Table 1) also had sparse stunted white birch (Betula Materials and Methods papyrifera Marshall) and white pine (Pinus strobus L.). This study was conducted in Jackson, Specimen collection and curation. Monroe and Wood counties, of central Wis- When an area harboring multiple visible consin (USA), the main production area of patches of cranberry had been located, a cranberry in the country. We sampled the single dense patch was randomly selected arthropod communities at two commercial for the initial suction-sampling of the plant cranberry marshes and three naturally oc- canopy. The suction-sample was taken using curring peatlands (total five sites). The sites a “D-vac” unit (Rincon Vitova, Ventura, CA), lie within a 60 km radius and all fall within which captures most above-ground arthro- the Glacial Lake Wisconsin Sand Plain pods within the 0.09 m2 sampling area of ecoregion (Johnson 2011). Sampling at all the unit. sites was done midday, under mostly clear Following the suction-sample, the skies (no rain or high winds) in late July and 2 early August of 2011. Each site was sampled 0.09 m area was excised to a depth of 0.3 once within a five-week period using multiple m using a common garden spade, and the sampling techniques. whole volume of plant, detritus, and soil was carefully removed from the ground. This Cultivated Sampling Sites. Two mass of soil and plant material (referred to commercial cranberry beds in central Wis- as a ‘core’) was placed within a plastic bag, consin (Table 1) were selected based on then into a cooler for transport back to the growers’ willingness to participate in the laboratory. The core-sample provided access study. Both commercial marshes were man- to below-ground arthropod diversity, and aged conventionally, and planted with the was supplemented with 80 further D-vac cultivar, ‘Stevens.’ A single cultivar was used samples, taken randomly from the general to control for insect and spider community area surrounding the core excavation (i.e., differences attributable to variable plant the available cranberry patches within 20 traits. All samples were taken at least three m of the core sample). The suction-samples meters from the edge of the bed. provided an assessment of arthropods within Wild Sampling Sites. The three the aerial portions of the plant canopy and peatland sites (Table 1) were selected based supplemented the initial suction-sample at on accessibility and the presence of large the site of the core-sample. patches of cranberry (V. macrocarpon) Once in the lab, the core sample was while lacking small cranberry (Vaccinium placed within an emergence cage (45 cm × 45 oxycoccos L.). Once many patches of cran- cm × 45 cm), within an incubator (22° C, 16:8 berries were located, a minimum patch-size photoperiod). The emergence cage restricted of approximately 0.3 m2 was sought. All almost all light sources except for a single three sites were predominately open oligo- circular portal that opened into a glass vial. trophic peatlands (poor fen). The immediate Small emerging arthropods, such as para- sampling area consisted of a mostly level sitoids, ants, and midges, were collected in Sphagnum angustifolium (C.E.O. Jensen this manner for 10–14 days. Following this ex Russow) C.E.O. Jensen carpet dominated emergence period, the core was dissected by sedges (esp. Carex oligosperma Michx.), and sorted under microscopes. All remaining grasses (mainly Calamagrostis canadensis arthropods were removed from the core, and (Michx.) P. Beauv.), and patches of cranber- curated in vials of 90% ethanol. Arthropods ry. Other mosses, leatherleaf (Chamaedaph- were separated to morphospecies, and ne calyculata (L.) Moench), dwarf raspberries identified to the lowest possible taxonomic (Rubus pubescens Raf.), steeplebush (Spi- level. Voucher specimens are housed at the raea tomentosa L.), and black chokeberry University of Wisconsin-Madison, Depart-
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Table 2. Insect specimens collected from wild and cultivated cranberry sites in Wisconsin. Order Family Genus species Wild Cultivated Odonata Coenagrionidae sp. 1 Orthoptera Gryllidae Allonemobius fasciatus (DeGeer) 8 Nemobius sp. 2 Hemiptera Aphididae sp. 6 1 Cicadellidae Macrosteles fascifrons (Stål) 4 sp. 288 17 Membracidae sp. 15 Cixiidae sp. 166 Delphacidae sp. 279 Mesoveliidae Mesovelia sp. 2 Hebridae Hebrus sp. 11 sp. 9 Veliidae Rhagovelia sp. 1 sp. 3 Oxycarenidae sp. 1 Miridae Coquillettia sp. 3 sp. 7 Tingidae sp. 1 Nabidae Nabis sp. 11 sp. 1 2 Anthocoridae Orius insidious (Say) 2 Pentatomidae sp. 2 1 Lygaeidae sp. 2 Geocoridae sp. 3 Thysanoptera Phlaeothripidae sp. 3 Coleoptera Carabidae sp. 1 Staphylinidae Paederus sp. 12 Stenus sp. 4 Subfamily: Scydmaeninae 2 Subfamily: Pselaphinae 37 1 sp. 22 2 Hydrophilidae Enochrus sp. 4 sp. 3 Scirtidae Cyphon sp. 3 sp. 3 Lycidae sp. 1 Melyridae sp. 1 Coccinellidae sp. 1 Silvanidae sp. 2 Latridiidae sp. 11 1 Anthicidae sp. 1 Chrysomelidae Systena frontalis (Fabricius) 3 Curculionidae sp. 3 sp.* 1 Neuroptera Chrysopidae sp. 2 Hymenoptera Ichneumonidae Gelis sp. 5 sp. 3 1 Braconidae sp. 33 1 Diapriidae sp. 16 Eucoilidae sp. 1 Platygastridae Baeus sp. 43 Macroteleia sp. 131 Opisthacantha sp. 254 Trimorus sp. 339 spp. 152 15 Ceraphronidae sp. 76 47 Chalcididae sp. 1 Pteromalidae sp. 31 4 Hymenoptera Perilampidae sp. 1 Eupelmidae Eupelmis sp. 1 Encyrtidae sp. 212 1 Aphelinidae sp. 7 Eulophidae Cirrospilus sp. 22 (Continued on next page) https://scholar.valpo.edu/tgle/vol50/iss2/6 56 et al.: TGLE Vol 50 nos. 3 & 4 full issue
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Table 2. Continued. Order Family Genus species Wild Cultivated Hymenoptera Eulophidae Closterocerus sp. 26 sp. 84 Elasmidae Elasmus sp. 2 Trichogrammatidae Trichogrammatoidea bactrae Nagaraja 3 sp. 24 Mymaridae sp. 48 Dryinidae Subfamily: Gonatopodinae 2 Halictidae sp. 2 Formicidae Tapinoma sessile (Say) 374 Crematogaster sp. 1 Dolichoderus sp. 27 Myrmica sp. 1 Stenamma sp. 1 sp. 1884 1 Lepidoptera Coleophoridae Coleophora sp. 4 Gelechiidae sp. 1 Tortricidae Sparganothis sp. 1 sp. 4 Noctuidae Hypenodes sp. 2 sp. 1 Diptera Tipulidae sp. 4 Dixidae sp. 23 Culicidae sp. 8 1 Chironomidae Chironomini sp. 4 sp. 4 4 Simuliidae sp. 15 Mycetophilidae sp. 8 1 Sciaridae sp. 3 28 Cecidomyiidae sp. 8 2 Tabanidae Chrysops sp. 1 Empididae Stilton sp. 3 sp. 1 Dolichopodidae sp. 1 Lonchopteridae sp. 2 Phoridae Megaselia sp. 2 17 sp. 27 7 Syrphidae sp. 1 Conopidae Conioscinella sp. 2 Ulidiidae sp. 4 Tephritidae sp. 1 Dryomyzidae sp. 2 Diptera Sepsidae Sepsis sp. 2 sp. 4 Sciomyzidae sp. 3 Chamaemyiidae sp. 4 Sphaeroceridae Leptocera sp. 9 sp. 26 2 Ephydridae sp. 2 Drosophilidae Drosophila sp. 1 sp. 33 4 Chloropidae Conioscinella sp. 3 Elachiptera sp. 1 Epichlorops sp. 1 Lasion sp. 1 Lasiosina sp. 5 Oscinella sp. 37 sp. 40 1 Aulacigastridae sp. 1 Asteiidae sp. 1 Anthomyiidae sp. 5 Scathophagidae sp. 1 Calliphoridae sp. 1 *Unknown immature Coleoptera.
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ment of Entomology (1630 Linden Drive, but little is known of the background taxa Department of Entomology, 545 Russell that likely represent the majority of the Laboratories). arthropod community in managed systems. Moreover, relatively little is known of the Results arthropod complex in wild cranberry habi- tats (Marshall et al.1999, Spitzer and Danks At the two cultivated cranberry sites, 2006). Most peatland survey work has fo- we collected a total of 384 specimens repre- cused either on a specific taxon or a relatively senting 5 orders and 39 families (Tables 2–4). specific geographic location (e.g. Rosenberg Diptera (flies) and Hymenoptera (wasps, and Danks 1987, Blades and Marshall 1994). bees and ants) had the highest numbers of The survey work reported here was conduct- families represented (12 and 10, respective- ed to establish broad, baseline estimates of ly) (Table 1), and Hymenoptera and Araneae arthropod diversity among wild and culti- (spiders) had the highest numbers of individ- vated V. macrocarpon stands in Wisconsin. ual specimens (155 and 109, respectively). The abundance and diversity of arthropods All insect and spider taxa were indexed by in this study are noteworthy considering county (Table 5–7), providing greater res- olution to the biogeography of Wisconsin’s the relatively small number of sample sites, peatland arthropods. total area surveyed, and narrow temporal coverage. Given the limited flora of Wiscon- At the three wild sites, we collected a sin peatlands (Chaddle 2013), the arthropod total of 7,058 specimens, spanning 11 orders fauna in wild and cultivated cranberry sites and 101 families (Tables 2–4). Again, Diptera appears to be relatively diverse. and Hymenoptera had the highest numbers of families represented (26 and 19, respec- The abundance of Hymenoptera was tively), and Hymenoptera and Araneae had particularly noteworthy, comprising 40% of the highest numbers of individual specimens all specimens collected at cultivated sites (3,723 and 1,336, respectively). We were (averaging 27 specimens per site) and 53% able to identify 625 specimens (9%) to spe- of all specimens at wild sites (averaging cies-level resolution. Most spiders, however, 478 per site). The hymenopterans found in were not identified to species because they the cultivated sites were almost exclusively were immatures (Table 3). Immature spiders parasitoid wasps (with the exception of one generally cannot be dependably identified ant), suggesting the presence of an ample to species because many of the characteris- prey base for the parasitoid community. Wild tic traits are not developed until maturity sites also harbored many parasitoid wasps (Ubick et al. 2005). Of the spiders identified (numerically, 20 times that of the cultivated to species, 18 were confirmed as new coun- sites), but at these wild sites, only 38% of hy- ty records and one was a new state record menopteran specimens were parasitoids, the (Table 6). Ten of the 18 county records were remaining 62% being ants. The abundance from the family Linyphiidae. The remaining and ecological importance of ants in peatland new records were from the following families: systems remains an interesting question for Araneidae (2), Clubionidae (1), Hahniidae future work. (2), Salticidae (1), Tetragnathidae (1) and Theridiidae (1). Most (44%) of the non-ant hymenopter- ans collected at the wild sites were exceed- The state record was for the species ingly minute parasitoids in the family, Ceratinopsis laticeps Emerton and was found Platygastridae (Table 2). Platygastrids are at one of the wild sites in Monroe County. egg parasitoids of insects and spiders, and It is a relatively small spider in the family are generally solitary parasitoids (O’Connor Linyphiidae, subfamily Erigoninae, which and Notton 2013). The more abundant platy- is the dominant spider group in temperate regions (Hormiga 2000). From the Great gastrids found in this study were Trimorus, Lakes region, this species has already been which are known to be parasitoids of beetle found in Ohio, Michigan, and Illinois, with eggs (Coleoptera: Carabidae and Staphylini- a predicted presence in Indiana (Sierwald et dae) (O’Connor and Notton 2013). The genus al. 2005). Therefore, it is not surprising to Macroteleia was also well-represented, and have found it in Wisconsin, and one would these platygastrids are egg parasitoids of assume it is present elsewhere in the state. tettigoniids (katydids) (Meusebeck 1977). It does not appear to be a peatland specialist Interestingly, many specimens of Baeus were (Kaston 1948). found, and these tiny wasps are relatively uncommon parasitoids of spider egg masses Discussion (Margaría et al. 2006). Spiders were hy- per-abundant in our study sites, suggesting Much research has been done on pests there was a significant prey base for Baeus of economic importance (and their natural populations. Virtually no platygastrids were enemies) in cultivated cranberry (Eck 1990), collected in the cultivated cranberry sites.
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Table 3. Arachnid specimens collected from wild and cultivated cranberry sites in Wisconsin. Order Family Genus species Wild Cultivated Opiliones Unknown sp. 2 Araneae Araneidae Araniella sp. 1 Argiope sp. 1 Cercidia prominens (Westring) 1 Gea sp. 9 Gea heptagon (Hentz) 1 Hypsosinga sp. 18 spp. 13 1 Tetragnathidae Leucauge sp. 1 Leucauge venusta (Walckenaer) 5 Pachygnatha sp. 1 Tetragnatha laboriosa Hentz 1 Tetragnatha sp. 4 sp. 1 Mysmenidae Microdipoena sp. 62 Linyphiidae Agyneta fabra (Keyserling) 4 2 Agyneta spp. 3 Bathyphantes pallidus (Banks) 6 Bathyphantes sp. 7 Ceraticelus bulbosus (Emerton) 3 Ceraticelus fissiceps(O. Pickard-Cambridge) 23 Linyphiidae Ceraticelus laetus (O. Pickard-Cambridge) 35 Ceraticelus sp. 14 1 Ceratinops sp. 2 Ceratinopsis laticeps Emerton 1 Collinsia plumosa (Emerton) 3 Eridantes erigonoides (Emerton) 1 Erigone atra Blackwall 1 Erigone autumnalis Emerton 3 Erigoninae sp. 100 56 Frontinella communis (Hentz) 16 Frontinella sp. 3 Grammonota gentilis Banks 2 Grammonota maculata Banks 7 Lepthyphantes sp. 1 Linyphiinae sp. 1 Microlinyphia mandibulata (Emerton) 1 Neriene clathrata (Sundevall) 15 Oedothorax trilobatus (Banks) 14 Scylaceus sp. 1 Walckenaeria sp. 2 spp. 153 6
Theridiidae Hentziectypus globosus (Hentz) 1 Theonoe stridula Crosby 4 Dipoena sp. 1 spp. 8 Dictynidae Dictyna/Emblyna 4 Anyphaenidae Anyphaena sp. 1 Wulfilasp. 7 Clubionidae Clubiona abboti L. Koch 1 Clubiona sp. 16 1 spp. 13 Corinnidae Phrurotimpus sp. 1 subfamily: Phrurolithinae 4 Scotinella divesta (Gertsch) 1 Philodromidae Ebo sp. 9 (Continued on next page)
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Table 3. Continued. Order Family Genus species Wild Cultivated Araneae Philodromidae Philodromus sp. 4 Thanatus sp. 32 Tibellus sp. 84 spp. 20 Salticidae Sitticus striatus Emerton 1 spp. 106 Thomisidae Coriarachne sp. 4 Mecaphesa sp. 21 Araneae Thomisidae Misumena sp. 1 Xysticus sp. 2 spp. 2 Gnaphosidae Drassyllus sp. 7 Gnaphosa sp. 3 spp. 5 Pisauridae Dolomedes sp. 11 1 sp. 1 Lycosidae Pardosa sp. 10 1 Pirata sp. 18 12 spp. 418 2 Hahniidae* Antistea brunnea (Emerton) 2 Hahnia sp. 1 Hahnia cinerea Emerton 3 Neoantistea sp. 3 Neoantistea agilis (Keyserling) 2 spp. 8 *The family Hahniidae has not been phylogenetically placed.
Table 4. Collembolan (springtail) specimens collected from wild and cultivated sites. Order Family Genus species Wild Cultivated Poduromorpha Poduridae Podura aquatica L. 3 Entomobryomorpha Isotomidae 1 13 Entomobryidae 605 Lepidocyrtus paradoxus Uzel 120
Table 5. Insect specimens collected in Wisconsin cranberries, indexed by county. County Order Family Genus species Jackson Monroe Wood Odonata Coenagrionidae X Orthoptera Gryllidae Allonemobius fasciatus (DeGeer) X Nemobius sp. X Hemiptera Aphididae X Cicadellidae X X X Macrosteles fascifrons (Stål) X Membracidae X Cixiidae X X Delphacidae X X Mesoveliidae Mesovelia sp. X Hebridae Hebrus sp. X X Veliidae X X Rhagovelia sp. X Oxycarenidae X Miridae X X Coquillettia sp. X (Continued on next page)
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Table 5. Continued. County Order Family Genus species Jackson Monroe Wood Hemiptera Tingidae X Nabidae X X Nabis sp. X X Anthocoridae Orius insidious (Say) X Pentatomidae X X Lygaeidae X X Geocoridae X X Thysanoptera Phlaeothripidae X X Coleoptera Carabidae X Staphylinidae Subfamily: Scydmaeninae X Subfamily: Pselaphinae X X Paederus sp. X X Stenus sp. X X Hydrophilidae Enochrus sp. X Scirtidae X Cyphon sp. X Lycidae X Melyridae X Coccinellidae X Silvanidae X Latridiidae X X Anthicidae X Chrysomelidae Systena frontalis (Fabricius) X Curculionidae X Neuroptera Chrysopidae X X Hymenoptera Ichneumonidae X X X Gelis sp. X X Braconidae X X X Diapriidae X X Eucoilidae X Platygastridae X X X Baeus sp. X X Macroteleia sp. X X Opisthacantha sp. X X Trimorus sp. X X Ceraphronidae X X X Chalcididae X Pteromalidae X X X Eupelmidae Eupelmis sp. X Encyrtidae X X X Aphelinidae X Eulophidae X X Cirrospilus sp. X Closterocerus sp. X Elasmidae Elasmus sp. X X Trichogrammatidae Trichogrammatoidea bactrae Nagaraja X Mymaridae X X Dryinidae Subfamily: Gonatopodinae X Halictidae X Formicidae Crematogaster sp. X Dolichoderus sp. X X Myrmica sp. X X Stenamma sp. X Tapinoma sessile (Say) X X (Continued on next page)
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Table 5. Continued. County Order Family Genus species Jackson Monroe Wood Lepidoptera Coleophoridae Coleophora sp. X X Gelechiidae X Tortricidae X X Sparganothis sp. X Noctuidae Hypenodes sp. X Diptera Tipulidae X Dixidae X X Culicidae X X Chironomidae X Chironomini sp. X Simuliidae X Mycetophilidae X X Sciaridae X Cecidomyiidae X X X Tabanidae Chrysops sp. X Empididae X Stilton sp. X Dolichopodidae X Lonchopteridae X Phoridae Megaselia sp. X X X Syrphidae X Conopidae Conioscinella sp. X Ulidiidae X Tephritidae X Dryomyzidae Sepsidae X X X X Sepsis sp. X Sciomyzidae X Chamaemyiidae X Sphaeroceridae Leptocera sp. X X Ephydridae X Drosophilidae X X X Drosophila sp. X Chloropidae X X X Conioscinella sp. X X Elachiptera sp. X Lasion sp. X Lasiosina sp. X Oscinella sp. X X Aulacigastridae X Asteiidae X Anthomyiidae X X Scathophagidae X Calliphoridae X
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Table 6. Arachnid specimens collected in Wisconsin cranberries, indexed by county († new county record; ‡ new state record). County Order Family Genus species Jackson Monroe Wood Opiliones X Araneae Araneidae X X X Araniella sp. X Argiope sp. X Cercidia prominens (Westring) X† Gea heptagon (Hentz) X† Hypsosinga sp. X X Tetragnathidae Leucauge venusta (Walckenaer) X X Pachygnatha sp. X Tetragnatha sp. X Tetragnatha laboriosa Hentz X† Mysmenidae Microdipoena sp. X Linyphiidae Agyneta fabra (Keyserling) X† X† Bathyphantes pallidus (Banks) X† Ceraticelus bulbosus (Emerton) X† Ceraticelus fissiceps (O. Pickard-Cambridge) X† X† Ceraticelus laetus (O. Pickard-Cambridge) X† X† Ceratinopsis laticeps Emerton X‡ Collinsia plumosa (Emerton) X Eridantes erigonoides (Emerton) X† Linyphiidae Erigoninae sp. X X X Erigone atra Blackwall X Erigone autumnalis Emerton X† X† Frontinella communis (Hentz) X X Ceraticelus laetus (O. Pickard-Cambridge) X Grammonota gentilis Banks X† Grammonota maculata Banks X Lepthyphantes X X Linyphiinae sp. X Microlinyphia mandibulata (Emerton) X† Neriene sp. X X Oedothorax trilobatus (Banks) X† Scylaceus sp. X Walckenaeria sp. X Theridiidae Dipoena sp. X Hentziectypus globosus (Hentz) X Theonoe stridula Crosby X† Anyphaenidae Anyphaena sp. X Wulfilasp. X Clubionidae Clubiona sp. X X Clubiona abboti L. Koch X† Corinnidae Phrurotimpus sp. X Scotinella sp. X Philodromidae Ebo sp. X Philodromus sp. X Thanatus sp. X Tibellus sp. X X Salticidae X X Sitticus striatus Emerton X† Thomisidae Coriarachne sp. X X Misumena sp. X Misumenops sp. X (Continued on next page)
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Table 6. Continued. County Order Family Genus species Jackson Monroe Wood Araneae Thomisidae Xysticus sp. X Gnaphosidae Drassyllus sp. X Gnaphosa sp. X Pisauridae Dolomedes sp. X X X Lycosidae Pardosa sp. X Pirata sp. X X Hahniidae* Antistea brunnea (Emerton) X X Hahnia cinerea Emerton X† Hahnia sp. X X Neoantistea sp. X Neoantistea agilis (Keyserling) X† *The family Hahniidae has not been phylogenetically placed.
Table 7. Collembola (springtails) found in Wisconsin cranberries, indexed by county. County Order Family Genus species Jackson Monroe Wood Poduromorpha Poduridae Podura aquatica L. X Entomobryomorpha Isotomidae X X X Entomobryidae Lepidocyrtus paradoxus Uzel X X
Of the hymenopteran specimens found of the spiders were lycosids, while only 14% in the cultivated sites, 21% were eulophid of the spiders at the cultivated sites were parasitoids, and 12% were ceraphronids, lycosids. compared with less than 1% from the wild Collembola (springtails) comprised sites for each of these families. The Eulo- 10% of the individuals collected from the phidae are a taxonomically and ecologically wild sites and 4% from the cultivated sites diverse family, often of significant economic (Table 4). Podura aquatica L. (Collembola: importance, with many species targeting an Poduromorpha), the only species of the array of dipterous hosts, as well as various family Poduridae, was collected only from agricultural pests (Goulet and Huber 1993). the cultivated sites. This may be due to the Araneae comprised 28% of the col- flooding events on cultivated beds, which lected specimens at the cultivated sites. involve the filling of cranberry beds with Of these, 79% were linyphiids (sheet-web large volumes of water from local reservoirs, spiders), and within this single family, 65% rivers, or lakes. The springtail species, P. were from its largest subfamily, Erigoninae aquatica, has been shown to be highly abun- (dwarf spiders). This subfamily is common dant during and immediately after ecological and pervasive in northern peatlands (Ubick flooding events, and then absent a short et al. 2005), thus it is not surprising to find time after such events (Lessel et al. 2011). such abundance in Wisconsin cranberry Many aquatic or semi-aquatic organisms, systems. From the wild sites, Araneae therefore, may be imported into cranberry comprised 19% of the collected specimens, beds from such water bodies, and these taxa 30% of which were linyphiids, and 26% of may persist for periods of time thereafter. those were from the subfamily Erigoninae. Other well-represented taxa from the Erigonines are very small spiders that tend cultivated sites were the dipteran families to live in leaf litter and readily balloon to Phoridae (6%) and Sciaridae (7%). Converse- disperse (Emerton 1902). They often have ly, in the wild sites, Phoridae represented a significant presence in agricultural fields less than 1% of the total number of spec- when other spider families are absent, and imens, and there were only three sciarid are particularly common in perennial sys- individuals collected among the three wild tems (Schmidt and Tscharntke 2005). Aside sites. Both fly families are widely distrib- from linyphiids, the Lycosidae (wolf spiders) uted, living in damp habitats and feeding were well represented. At the wild sites, 33% largely on detritus (McAlpine et al. 1981).
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Lepidoptera were poorly represented, Blades, D., and S. Marshall. 1994. Terrestrial with only 13 individuals representing at arthropods of Canadian peatlands: synopsis least six taxa (0.18% of the individuals at of pan trap collections at four Southern On- wild sites; none were found in cultivated tario peatlands. Memoirs of the Entomologi- sites). This is likely an artifact of the sam- cal Society of Canada 126: 221–284. pling techniques used, which are not ideal for Chaddle, S.W. 2013. Wisconsin Flora: An Illus- trapping adult Lepidoptera. Extensive sam- pling in peatland habitats across Wisconsin, trated Guide to the Vascular Plants of Wis- Michigan, and Minnesota have revealed the consin. CreateSpace Independent Publishing presence of over 1,000 lepidopteran species Platform. (M.S. thesis, KEJ). Even though these Chen, Y. H., G. A. Langellotto, A. T. Barrion, efforts were focused on Canadian life zone and N. L. Cuong. 2013. Cultivation of peatlands, there is currently no reason to domesticated rice alters arthropod biodiver- believe that Glacial Lake Wisconsin Sand sity and community composition. Annals of Plain peatlands do not support a diverse fau- the Entomological Society of America 106: na (although the number of boreal peatland 100–110. specialists should be less given the warmer climate and lower diversity of peatland Chen, Y.H., and C.C. Bernal. 2011. Arthropod habitats). One species, Lycaena epixanthe diversity and community composition on wild (Boisduval and Le Conte) was documented and cultivated rice. Agricultural and Forest at Site 4 (Table 1) and other similar, poor Entomology 13: 181–189. fen sites outside of this study; this species Eck, P. 1990. The American Cranberry. Rutgers is a well-known cranberry specialist and University Press. New Brunswick, NJ. field work in the Great Lakes region shows it uses both V. macrocarpon and V. oxycoccos Emerton, J.H. 1902. The common spiders of the (KEJ, pers. obs.). Unites States. Ginn & Company. Boston, MA. It is often found that agroecosystems Goulet, H. and J. Huber (eds). 1993. Hyme- contain substantially lower biodiversity than noptera of the world: an identification guide unmanaged, natural ecosystems (Andow to families. Center for Land and Biological 1991, Pimentel et al. 1992, Chen and Bernal Resources Research. Ottawa, Ontario. 2011, Chen et al. 2013). From our prelimi- Hormiga, G. 2000. Higher level phylogenetics nary investigation, this does appear to be of Erigonine spiders (Araneae, Linyphiidae, the case for cultivated and wild cranberry Erigoninae). Smithsonian Contributions to ecosystems, but further survey work will be Zoology, #609. Smithsonian Institute Press. required to better characterize the arthropod communities in these ecosystems. A better Johnson, K.E. 2011. Distributions, habitats, and understanding of the community compo- natural histories of Boloria (Lepidoptera: sition and trophic function of cranberry Nymphalidae) inhabitating central North arthropods will inform cranberry production American peatlands, emphasizing the Great practices and provide a baseline to gauge Lakes Region. Thesis (M.S.), University of future changes to the cranberry arthropod Wisconsin-Madison. community. Kaston, B.J. 1948. Spiders of Connecticut. Hart- ford, CT. Connecticut State Geological and Acknowledgments Natural History Surveys. Bulletin 70. Wisconsin cranberry growers are Lessel, T., M.T. Marx and G. Eisenbeis. 2011. gratefully acknowledged for their support Effects of ecological flooding on the temporal of the arthropod surveys conducted on and spatial dynamics of Carabid beetles their marshes. The Authors thank Dan (Coleoptera, Carabidae) and springtails Young (Dept. of Entomology, University (Collembola) in a polder habitat. ZooKeys of Wisconsin-Madison) for assistance with 100: 421–446. identifications of Coleoptera. Laboratory Margaría, C.B., M.S. Loiácono, and M.O. Gon- assistants (Scott Lee, Christopher Watson, zaga. 2006. A new species of Baeus (Hyme- Eric Wiesman) helped with the extrication noptera: Scelionidae) from Brazil, parasitoid of wild cranberry sods, as well as with sod of Cyclosa morretes (Araneae: Araneidae). dissections. The project was supported by Entomological News 117:181–187. USDA-ARS appropriated funds (awarded to SAS). Marshall, S.A., A.T. Finnamore, and D.A. Blades. 1999. Canadian peatlands: the ter- Literature Cited restrial arthropod fauna. In Invertebrates in Freshwater Wetlands of North America: Andow, D. A. 1991. Vegetational diversity and Ecology and Management, eds. D.P. Batzer, arthropod population response. Annual Re- R.B. Rader, S.A. Wissinger, pp. 383–400. view of Entomology 36: 561–586. New York: Wiley.
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McAlpine, J. F., B. Peterson, G. Shewell, H. Rydin, H. and J. Jeglum. 2013. The biology of Teskey, J. Vockeroth, and D. Wood. 1981. peatlands: second edition. Oxford University Manual of nearctic Diptera. Biosystematics Press. Oxford, United Kingdom. Research Institute. Ottawa, Ontario. Schmidt, M.H. and T. Tscharntke. 2005. The Meusebeck, C.F.W. 1977. The parasitic wasps role of perennial habitats for Central Euro- of the genus Macroteleia Westwood of the pean farmland spiders. Agriculture, Ecosys- New World (Hymenoptera, Proctotrupoidea, tems, and the Environment 105: 235–242. Scelionidae). United States Department of Sierwald, P., Draney, M., Prentice, T., Pascoe Agriculture, Agricultural Research Service, F., Sandlin, N., Lehman, E.M., Medland, Technical Bulletin No. 1565. V., and Louderman, J., 2005. The spider O’Connor, J.P., and D.G. Notton. 2013. A re- species of the Great Lakes states. Proceed- view of the Irish scelionids (Hymenoptera: ings of the Indiana Academy of Science 114: Platygastroidea, Platygastridae) including 111–206. four species new to Ireland. Bulletin of the Spitzer, K., and H.V. Danks, 2006. Insect Bio- Irish Biogeographical Society 37:20–44. diversity of Boreal Peat Bogs. Annual Review Pimentel, D., U. Stachow, D.A. Takacs, H.W. of Entomology 51:137–61. Brubaker, A.R. Dumas, J.J. Meaney, United Stated Department of Agriculture— J.A.S. O’Neil, D.E. Onsi and D.B. Corzi- National Agricultural Statistics Service lius. 1992. Conserving biological diversity (USDA NASS) 2014. Noncitrus fruits and agricultural forestry systems: most biological nuts: 2013 summary. http://usda.mannlib. diversity exists in human-managed ecosys- cornell.edu/usda/current/NoncFruiNu/Non- tems. Bioscience 42: 354–362. cFruiNu-07-17-2014_revision.pdf. Rosenberg, D., and H. Danks. 1987. Aquatic Ubick, D., P. Paquin, P.E. Cushing and V. insects of peatlands and marshes in Canada: Roth (eds). 2005. Spiders of North America: introduction. Memoirs of the Entomological An identification manual. American Arach- Society of Canada 140: 1–4. nological Society 377 pp.
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The Great Lakes Entomologist Published by the Michigan Entomological Society
Volume 50 Nos. 3 & 4 ISSN 0090-0222
Table of Contents
New Species Records for Wisconsin False Click Beetles (Coleoptera: Eucnemidae), with a Checklist of the Wisconsin Eucnemid Fauna Robert L. Otto and Daniel K. Young...... 47 The Effects of Soil Moisture, Soil Texture, and Host Orientation on the Ability of Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae) to Infect Galleria mellonella Suzanne M. Hartley and John R. Wallace...... 52 Insect (Arthropoda: Insecta) Composition in the Diet of Ornate Box Turtles (Terrapene ornata ornata) in Two Western Illinois Sand Prairies, with a New State Record for Cyclocephala (Coleoptera: Scarabaeidae) Reese J. Worthington, E. R. Sievers, D. B. Ligon, and P. K. Lago...... 61 The Drosophilids of a Pristine Old-Growth Northern Hardwood Forest Thomas Werner...... 68 The Ability of Specific-wavelength LED Lights in Attracting Night-flying Insects Ryan S. Zemel and David C. Houghton...... 79 Insect Visitors of Cirsium pitcheri, a Threatened and Endemic Dune Species, in Relation to Annual Weather Variation Jordan M. Marshall...... 86 Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) Observed Feeding on Chamaesaracha sp. in Eastern Colorado. Michael S. Crossley, Benjamin Pélissié, Zachary Cohen, and Sean D. Schoville...... 93 Arthropod Fauna Associated with Wild and Cultivated Cranberries in Wisconsin Shawn A. Steffan, Merritt E. Singleton, Michael L. Draney, Elissa M. Chasen, Kyle E. Johnson, and Juan E. Zalapa...... 98
Cover photo Top left: Leucophenga varia, male; Top right: Drosophila guttifera, female; Bottom left: Drosophila suzukii, male; Bottom right: Zaprionus indianus, female (Diptera: Drosophilidae) Photos by Dr. Thomas Werner
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