sign in sign up
<<
Home , Aquatic insect, Hexagenia, Hexagenia bilineata, Mayfly

Downloaded by guest on September 30, 2021 a Kelly F. Jeffrey and waterways Stepanian M. American Phillip North burrowing major the across , mayfly, aquatic abundant an in Declines www.pnas.org/cgi/doi/10.1073/pnas.1913598117 (13) anglers recreational and industry fishing commercial transportation the inhib- ing river and large halting visibility These temporarily (12). reduced navigation, swarms water dense ited mayflies the grit and of and clear drifts could roadways, reg- snowplows Deep until cities (12). impassable streets waterfront headlines rendered blanketing newspaper and filled spectacle, aquatic ularly natural the a them of made reports emergences mayfly immense The of waterways. scale largest America’s North of many across of swarms mertime human and impacts cycling, with biogeochemical fluxes society. , ecosystem ( massive fundamental mayflies of on burrowing example of extreme con- an lifecycle ecosystem eco- aquatic, aquatic–terrestrial an the the across in tone, Spanning interfaces problematic. movements remains habitat seasonal text quanti- terrestrial of advances, and magnitude aerial, these the Despite and environmental fying (5–11). these foundational impor- processes in and the highlight movement ecological habitats, scale individu- spatial aerial of and of tance quantitative and number billions both first terrestrial, in by extremes the aquatic, across undertaken ani- within of nutrients in journeys als some advances of and enabled technological descriptions have Recent monitoring of (4–7). through mal time cycling connectivity to commu- and and and difficult space drive transport function, particularly ecosystem been the of has structure, movements organisms nity Seasonal biomass, soil of (3). and flow quantify plant the of have but and budgeting techniques ecology landscape-scale remote-sensing on enabled Modern effects yet cascading (3). 2), dynamic biogeochemistry (1, with environ- organisms change anthropogenic and by mental disrupted energy, increasingly are nutrients, flows of these flows spatial of W nutrient environmental bioflow and levels trophic declines production primary these cycling. higher ecosystems, a years, impact terrestrial As and 50%. recent will aquatic over in produce in by source declined but can prey the has into waterways event hours, both biomass emergence several across of tons single over 3,078.6 A airspace releasing West- mayflies, Basin. and billion River Erie 87.9 Mississippi Lake Upper of the ern observations along annual transport radar in changes biomass long-term analyzed quantify to We flights emergence mayfly macroscales impossible. at such remained characterization fresh- their of has from but swarms example habitats, mayfly benthic of dramatic water emergence annual A biomass the ecotones. and is exchange fun- nutrients, across energy, a transported 2019) is which are 6, habitats August by review disparate for mechanism (received among 2019 damental 12, movement December approved animal and Canada, Seasonal Edmonton, Alberta, of University Schindler, W. David by 46556 Edited IN Dame, Notre 46556; Dame, IN Notre Dame, of Notre University Dame, Sciences, Notre Biological of University Sciences, 24060; VA Earth Blacksburg, and Engineering Environmental and Civil eateto ilg,Uiest fOlhm,Nra,O 73019; OK Norman, Oklahoma, of University Biology, of Department hog h ideo h 0hcnuy nrossum- enormous century, 20th the of middle the Through csse ucinadtepeooyadmagnitude and phenology the between link and critical function the of ecosystem understanding limited have e | ecotone | emergence Hexagenia e oprtv nttt o eocl eerlgclSuis nvriyo kaoa omn K702 and 73072; OK Norman, Oklahoma, of University Studies, Meteorological Mesoscale for Institute Cooperative a,b Hexagenia a,b,c,1 | Ephemeroptera ouain eevtlfrsupport- for vital were populations al .Entrekin A. Sally , afle eeacmo sight common a were mayflies | aa radar d hrot .Wainwright E. Charlotte , p. is spp.) b oi lisIsiue nvriyo kaoa omn K73019; OK Norman, Oklahoma, of University Institute, Plains Corix doi:10.1073/pnas.1913598117/-/DCSupplemental at online information supporting contains article This 1 the under Published Submission.y Direct PNAS a is article This interest.y competing no declare S.A.E., authors P.M.S., The and paper.y data; the analyzed wrote J.F.K. P.M.S. research; and J.L.T., tools; performed C.E.W., P.M.S. reagents/analytic research; new designed contributed C.E.W. D.M. and P.M.S. contributions: Author of veys 16). (14, large-scale capabilities of monitoring development motivating and freshwater waterways of change, large “health” environmental these to vulnerable that making especially shows are More- impossible. precedent ecosystems remained historical has significance of macroscales over, ecological at much mayfly the events in of quantifying these commonplace cycle of 1), (Fig. become annual America the more North Although once 18). has (17, of emergence 1990s recovery early eventual the 18). the conservation 17, to in led (12–15, efforts Hexagenia protection targeted Rivers environmental absence, Mississippi segments of and large and decades and two Ohio, Basin After Illinois, Erie extir- the Lake complete Western of with the waterways, from pation midwestern of environ- prominent disappearance and the many in engineering, resulted toxicity hydrologic mental , agricultural disappeared. chronic from largely runoff, had increasing emergences of mass combination The these How- 1970, conspicuous (14–17). by ecosystem a aquatic ever, were resi- functional emergences productive, waterside a mayfly for of these sign annoyance all, perennial of a most dents; as serving also while owo orsodnemyb drse.Eal [email protected] Email: addressed. be may correspondence whom To iapaac rmsm fNrhAeiaslargest America’s North of widespread current some to if cascade waterways. and, from could quality continue, disappearance water losses trends in these aquatic population deterioration indicators, from signal ecological flux As may biomass impossible, habitats. insect previously terrestrial in to been aquatic declines have quantify persistent that to revealing scales sensing unknown. at remote abundance impacts radar anthropogenic apply We intensifying com- these to of be vulnerability munities to the long-term continues leaving infeasible, ecosystems uncover Monitoring logistically across trends. to abundance insect population efforts aquatic invertebrate motivate reports large-scale Alarming declines and webs. food phenomenon insect regional in natural of role spectacular key a and plays source that a fascination is swarms public mayfly of massive of appearance annual The Significance eue ete uvilnerdrt odc ihl sur- nightly conduct to radar surveillance weather used We Hexagenia Hexagenia c ouain n eooiaino ao aiasin habitats major of recolonization and populations jrj Mirkovic Djordje , NSlicense.y PNAS bnac vrteWsenLk reBasin Erie Lake Western the over abundance mrec nefcieidctro ecological of indicator effective an emergence d eateto noooy ignaTech, Virginia Entomology, of Department e . enfrL Tank L. Jennifer , y https://www.pnas.org/lookup/suppl/ NSLts Articles Latest PNAS f eatetof Department Hexagenia c eatetof Department f , | from f6 of 1

ENVIRONMENTAL ECOLOGY SCIENCES Hexagenia’s synchronous aerial emergences to quantify the flux of these benthic organisms across the water–air interface and produce a long-term time series of changes in system- wide abundance (Materials and Methods). This application of macroscale remote sensing provides a phenomenological per- spective of these synchronized emergences, demonstrating the regional extent of mayfly abundance, dispersal, and deposition (Fig. 2). Moreover, this expanded capacity to make quantitative long-term measurements of that engage in syn- chronized mass emergence flights offers a regional view of the effects of environmental change on emergence phenomena, a key aspect of ecology (Figs. 3 and 4).

Results Total annual bioflux of Hexagenia mayflies occurs in several Fig. 1. Local-scale phenomenology of a Hexagenia mayfly emergence. (A) Following up to 2 y of growth as an aquatic , mayflies ascend to the episodic emergence events, each occurring over an isolated geo- water surface en masse, molt into a volant subadult form, and fly to shel- graphical extent and demonstrating a unique phenology that is tered land to undergo a second molt. These dusk emergence flights result in likely associated with distinct benthic thermal regimes and abi- dense waves of subadults that blanket shorelines. (B) The mayflies spend the otic cues (20, 21). The largest emergence events in following day molting into their sexually mature adult form, taking flight at occur over the center of the western basin and can result in a sunset to engage in spectacular mating swarms that are followed quickly by flux of up to 87.9 billion mayflies (3,078.6 tons of biomass) across oviposition and death. (C) Within 2 d of the initial emergence, tons of dead the water–air interface in a single night. A 697-km stretch of the mayflies litter the shoreline, resulting in a substantial biomass flux to the Upper can produce up to 3.25 billion individ- surrounding terrestrial environment. Image courtesy of Jeff Ferguson/U.S. Army Corps of Engineers. uals (114 tons) in one evening. Accumulating this over the emergence season, annual aquatic–terrestrial bioflux represents the total biomass transported from benthic habitats and Upper Mississippi River and investigate patterns in emer- through the airspace into terrestrial ecosystems. Annual Hexage- gence magnitude across these two iconic waterbodies over time. nia bioflux over the western basin of Lake Erie can exceed 115 Just as radar remote sensing has been used to quantify long- billion individuals (4,031 tons; 2.19 g m−2 y−1, 0.94 g C m−2 y−1, term changes in the abundance of migratory organisms in flight 0.22 g N m−2 y−1, 0.01 g P m−2 y−1), while the Upper Mis- (i.e., birds (10, 11), insects (8, 9), and (19)), we exploit sissippi River produces up to 20.5 billion mayflies annually,

Fig. 2. Macroscale phenomenology of a mayfly emergence over Lake Erie on the night of June 27, 2018 as observed by weather surveillance radar. (A) Radar snapshot at 01:56 Coordinated Universal Time (UTC) depicting the initial ascent of mayflies from the lake surface surrounding the shorelines of Point Pelee, Pelee Island, and Kelleys Island. At this time, a total of 2.1 million mayflies are detected in the airspace. (B) Radar snapshot at 02:50 UTC showing the continuing ascent and downwind drift of mayflies across the lake to the southeast. Additional emerging mayfly plumes develop surrounding North, Middle, and South Bass Islands. Mayflies reaching the southern lakeshore rapidly descend out of the airspace. At this time, a total of 394 million mayflies are detected in the airspace. (C) Radar snapshot at 03:32 UTC. Emergence and ascent have largely terminated as mayflies continue to fly downwind toward the southern lakeshore. At this time, the aerial abundance reaches a maximum, with a total of 2.0 billion mayflies detected in the airspace. (D) Radar snapshot at 04:32 UTC. Most mayflies have already descended from the airspace as the trailing edge of the mayfly plume approaches the southern lakeshore. At this time, a total of 81 million mayflies are detected in the airspace. (Lower) The time series of aerial mayfly abundance during the emergence event. The mayfly numbers given in A–D are annotated as well as the time of local sunset. The full radar loop of this emergence event is provided as Movie S1.

2 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1913598117 Stepanian et al. Downloaded by guest on September 30, 2021 Downloaded by guest on September 30, 2021 bnac vrteUprMsispiRvr(lc)a ela otiuin rmtenrhr L rse I e)adsuhr Dvnot A blue) IA; (Davenport, southern and red) WI; Crosse, (La al. northern et the Stepanian from (circles). contributions surveillance radar as and well (62) (crosses) as sampling (black) benthic by River measured Mississippi as subdomains Upper the over abundance insects g terrestrial migratory 0.046 of (e.g., bioflows than aquatic–terrestrial greater magnitude of magnitude million the during 53 transport comparison, biomass over for Methods). basis and of resources— a (Materials fledging demands food As to of energetic hatching from calories the birds trillion nestling support 12 to to (23, enough up birds export insectivorous can in Basin particular, success in Annual fledgling insects, to 24). aquatic linked volant systems been of trophic has abundance terrestrial the surrounding mas- and deposition for a (2), as atmospheric pulse serve resource through also movements sive basin These through Methods). the and y (Materials to 1 phos- reactive loading in soluble annual Basin phorus the of Erie removed one-third offsets Lake phosphorus emergence phos- Western the of context, the tons 16 For from and ecotones. nitrogen of across tons and phorus 475 as (22), much annual as ecosystems translocate waterways, terrestrial two these surrounding within to transport ent N g 111.11 i.4. Fig. biomass kg of 1.03 tons shoreline: river 720 g 1.88 length of area: flux per a biomass aquatic–terrestrial for (emergent an period developmental in 2-y resulting required studies. referenced the the Considering in procedures (cyan). sampling subimagoes benthic on emerging details of have 49–61 surveys and radar 18, 17, by 15, directly as well Hexagenia as Methods) and (Materials total of mates 3. Fig. qai neteegnecnpa usata oei nutri- in role substantial a play can emergence insect Aquatic non elnsin declines Ongoing ogtr aiblt in variability Long-term yp orahmtrt,rdreegnesres(yn hudb otcmaal ihteaudneo er2nmh bu ice) Refs. circles). (blue nymphs 2 year of abundance the with comparable most be should (cyan) surveys emergence radar maturity, reach to nymph m −1 Hexagenia Hexagenia m −2 y −1 y . P g 3.6 , −1 bnac r eie rmbnhcsmln fnmhdniispirt bak,drn rd,adatr(le extirpation (blue) after and (red), during (black), to prior densities nymph of sampling benthic from derived are abundance 8 n prahn h asflxof flux mass the approaching and (8) ) Hexagenia mrec nteWsenLk Erie Lake Western the in emergence Hexagenia 0.0 0.2 0.4 0.6 0.8 1.0 1.2 1.4 1.6 10 20 30 40 50 60 70 80 90 0 Hexagenia m −1 m −1 y afl bnac (individuals abundance mayfly −1 mrecscnb resof orders be can emergences m Hexagenia y afl bnac (individuals abundance mayfly ). −2 −1 mretboasper biomass emergent ; 4.7gC g 7 446. , Upper MississippiRiver mrecscan emergences Lake Erie Hexagenia m −1 y ×10 −1 Hexagenia Present study Stapanian etal.2017(year-2) Stapanian etal.2017 Green etal.2013 Schloesser etal.2000 Farrara &Burt1993 Manny &Schloesser1999 Dermott 1994&OME1981 Britt etal.1980 Veal &Osmond 1968 LEES 1968 Carr &Hiltunen1965 Britt 1955 Wood 1953 Manny 1991 Shelford &Boesel1942 Wright & Tidd 1933 year , 9 year ×10 Present studysouthernsubdomain Present studynorthernsubdomain Present studytotaldomain Sauer 2004southernsubdomain Sauer 2004northernsubdomain Sauer 2004totaldomain n ims (tons biomass and ) Hexagenia mrec n eildit h liaeft fteematerials these surrounding of fate the ultimate to insect the quantify drift, energy can aerial of and surveillance emergence radar worth organisms, While of calories habitat. billions terrestrial of biomass, trillions of elemental tons and of tons of of thousands hundreds Annual nutrients, of (23). exchange the behavior represent animal gences to (22) nutrient with environmental cycling ecotones, from ranging across influences biomass rapidly ecological direct for of mechanism pulses effective enormous an transporting is emergence insect Aquatic 4). (Fig. 2019 Discussion to 2012 which from well, 52% as of River decrease Mississippi a of an Upper showed pattern the indicated This for (17). true surveys nymphs holds decline of radar sampling 2019, benthic (17). localized to 3) from in 2015 (Fig. decrease from abundance 84% period in the declines fluctuations of chronic In acute recolonization exhibiting by begun the have punctuated after populations decade Erie, change. Lake a rapid undergoing than is phenomenon Less this that clear already Hexagenia subsidies. resource to contribution significant kg 72.5 (e.g., birds migrating 12 n ims (tons biomass and ) lhuhw r utnwqatfigteetn owhich to extent the quantifying now just are we Although Abundance Abundance mrecscnrbt oeooia rcse,i is it processes, ecological to contribute emergences ×10 3 nteUprMsispiRvr uvy of Surveys River. Mississippi Upper the on ) Hexagenia ×10 3 nteWsenLk reBsn itrclesti- Historical Basin. Erie Lake Western the in ) m bnac,crooaigtrends corroborating abundance, −1 0 0.35 0.70 1.05 1.40 1.75 2.10 2.45 2.80 3.15 y −1 0 7 14 21 28 35 42 49 56 1) eosrtn their demonstrating (11), ) NSLts Articles Latest PNAS Hexagenia Hexagenia Hexagenia | emer- f6 of 3 in

ENVIRONMENTAL ECOLOGY SCIENCES is often subject to the effects of human influence (e.g., large- and can be subject to bias (35, 36). Long-term radar measure- scale removal efforts) (Fig. 1C). Especially for the midwestern ments are an emerging tool for substantiating magnitudes and water bodies considered, it is difficult to contextualize the effect rates of regional declines of insect biomass. Moreover, radar of Hexagenia emergence separate from related human activi- measurements can extend exploration of these themes to benthic ties. For example, although the export of phosphorus from water ecotones, providing the first spatially comprehensive, regional bodies by Hexagenia emergence may be of similar magnitude assessments of aquatic insect population declines. This tech- to some natural inputs, when considering current contribu- nique holds the potential of providing standardized sampling tions from anthropogenically enhanced inputs (e.g., industrial in other parts of the world (e.g., Africa) (37) and may be point sources and agricultural runoff), phosphorus exports rep- used to monitor population trends in other aquatic insects that resent less than 1% of total annual loading. It is possible that, emerge in large numbers, such as caddisflies and midges. As a prior to the onset of industrial agriculture, aquatic insect emer- vital prey source for insectivores, Hexagenia declines undoubt- gence may have been a significant mechanism for offsetting edly impact trophic structure of surrounding ecosystems. Our phosphorus inputs from natural sources; presently, however, results suggest a widespread and multiyear decline in the pop- anthropogenic loadings to these specific water bodies make ulations of mayflies in the American Midwest. These patterns these emergent nutrient exports virtually negligible to the overall contribute a spatiotemporal perspective to existing data and budget. further motivate examination of the changing Although humans contribute heavily to nitrogen and phospho- of the Great Lakes region, with particular interest in interac- rus cycling in midwestern waterways, these nutrient contributions tions among water temperature, nutrient runoff, and . are not available across all trophic levels, making insect emer- If these population trends continue, persistent environmen- gence a major nutritional source for terrestrial predators and tal changes could threaten to once more extirpate Hexagenia scavengers (2, 23, 24). Seasonal pulses of volant aquatic insects mayflies from ’s largest waterways, making this are especially important to avian aerial insectivores, which syn- ephemeral spectacle—and its vital ecological functions—a thing chronize their breeding phenology to correspond with emer- of the past. gence and rely on these high-quality food sources for fledgling success (23). In this regard, reports of significant declines in Materials and Methods aerial insectivore populations across North America have been The US National Weather Service operates a network of weather surveil- partially tied to the availability of insect prey (25) and in lance radars (NEXRAD, hereafter) that provides continuous, high-resolution particular, emerging aquatic insects (23, 24). measurements of the national airspace. Although this system was deployed We have found persistent declines in Hexagenia abundance with the mission of improving weather prediction and analysis, a beneficial within Lake Erie and the Mississippi River. Similar trends across by-product has been the capacity to systematically monitor aerial wildlife both lentic and lotic waterways suggest the pervasive effect (e.g., birds, bats, and insects) (38). Background information on radar theory of multiple anthropogenic stressors on freshwater ecosystems. and operation, specifically focusing on ecological applications of NEXRAD, Hexagenia has been compiled in several primers (38–40). Among the phenomena rou- These ongoing reductions in populations may offer a tinely detected by radar, regional emergences of aquatic insects have been window to the near-future environmental and ecological changes repeatedly documented over several waterways and validated by visual throughout these waterways. As the climate continues to warm, ground observations. By far, the most prolific of these emergences are the lake stratification between June and September will become annual flights of burrowing mayflies (Hexagenia spp.) on the Upper Mis- more common (26), leading to decreased benthic concen- sissippi River and Western Lake Erie Basin, both of which regularly garner trations, chronic hypoxia, and emergence failures (27). Warmer widespread media coverage. It is because of the high confidence in surface waters fed by phosphorous-rich spring runoff into Lake composition making up these emergence events that we chose to focus Erie will continue to trigger summer blooms, releasing tox- analysis on these two waterways. ins, such as microcystin, into the environment (28). Hexagenia are highly sensitive to these toxins (29), and as algae blooms System Specifications and Site Descriptions. Our analysis become more expansive and frequent in regions already suscep- domain on the Upper Mississippi River spans a 697-km stretch from Lock 3 to Lock 19 and includes a 10-km buffer extending outward from the tible to hypoxia, emergence failures are more likely to occur. At river. The combined surveillance area of two weather radars covers the the same time, nutrient-laden runoff will continue to increase entirety of this domain. The first radar is located at the National Weather lake turbidity and orthophosphates that promote hypoxic con- Service office in La Crosse, Wisconsin (International Civil Aviation Organi- ditions by driving oxygen concentrations lower and for longer zation site identifier: KARX) and transmits at a frequency of 2,770 MHz (30). Compounding the effects of hypoxia and toxicity, pes- (wavelength: 10.82 cm). The KARX radar location (43.8228◦N, 91.1911◦W, ticide concentrations are increasing in freshwater ecosystems. 413.6 m above mean sea level [AMSL]) provides coverage of the upper concentrations in Great Lake tributaries can be segment of the analysis domain, north of the 42.67◦N parallel. Dual- up to 40 times greater than the Chronic Concentration set by radar measurements at the KARX site began on 15 April US Environmental Protection Agency Aquatic Life Benchmark 2012. The second radar is located at the National Weather Service office Hexagenia in Davenport, Iowa (International Civil Aviation Organization site iden- (31), and are among the most sensitive aquatic insects tifier: KDVN) and transmits at a frequency of 2,860 MHz (wavelength: to a suite of these commonly applied pesticides. Even at sub- 10.48 cm). The KDVN radar location (41.6116◦N 90.5810◦W, 259.4 m lethal levels, the presence of will lead to greater AMSL) provides coverage of the lower segment of the analysis domain, susceptibility to hypoxia, reduced fitness, and increased preda- south of the 42.67◦N parallel. Dual-polarization radar measurements at tion (32). Exacerbating these effects, concentrations the KDVN site began on 23 March 2012. Our analysis domain on Lake in sediment can be even greater than in the overlying water Erie covers the western and central basins and is surveyed by the radar (33), and as , Hexagenia nymphs will experience two located at the National Weather Service office in Cleveland, Ohio (Inter- pathways of increasing pesticide exposure: dissolved in water national Civil Aviation Organization site identifier: KCLE). The KCLE radar and stored in sediment. Taken as a whole, multiple interact- transmits at a frequency of 2,875 MHz (wavelength: 10.43 cm) and is positioned on the southern lakeshore (41.4131◦N, 81.8597◦W, 262.1 m ing threats to aquatic insects may present the possibility of once AMSL). Dual-polarization radar measurements at the KCLE site began on again extirpating Hexagenia from these waterways. 7 December 2011. Persisting global declines in insect abundance have flooded public awareness and have led to speculation of so-called “Eco- Radar Data Access and Processing. The full dataset of historical NEXRAD logical Armageddon” scenarios in the near future (34, 35). There measurements is archived on the Amazon Web Services cloud and is con- is a critical need to objectively inform these dialogues, but quan- tinually appended with current measurements in real time. This dataset is titative monitoring of insect systems is logistically challenging open access and available for download online (41). We constrained our

4 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1913598117 Stepanian et al. Downloaded by guest on September 30, 2021 Downloaded by guest on September 30, 2021 tpna tal. et Stepanian rdcinae ftervra nrf 5(rm meter (grams 15 ref. in as river m [411,445,932 mayfly the northern the over of units flux area into convert production to River area Mississippi production the km over mayfly approach the (1,840 by Erie Erie) Lake Lake over of flux 2015 annual in g of meter 4,030,792,020 (grams units (e.g., 1 reach To ref. tons. in metric presented as 4,031 or g 4,030,792,020 become niiul oboas emlil ytems fa vrg individ- average an of of mass number the the by convert multiply To mea- individuals. we radar ual of biomass, with number to associated is individuals unit abundance measuring of Composition. the sures Elemental previously, and described Bioflux, Biomass, As to the Individuals find from to Converting season the over estimates all productivity. represent sum mayfly annual estimates we accumulated abundance night, abundance an each our obtaining for result, After present. estimate a individuals of As altitudes number beam. high minimum sufficiently the radar at the fly all enter do nor individuals to simultaneously all airspace not the because in abundance are 2, total Fig. of in underestimate dur- value an airspace maximum the inherently the in (e.g., observed emergence mayflies given the of a number ing for highest abundance single mayfly the the as define night we of scans, volume number subsequent the in of 2, als snapshot (Fig. instantaneous aloft an observed into mayflies converted been has scan Esti- Radar from Productivity mates. Annual and Abundance Mayfly Nightly Estimating mayflies. these individual of over number cross-section the radar quantifying mean cm The (0.00179 observations). aspects radar the of tative acltda ad(.6Gz o lvto nlssann through 0 spanning angles elevation for were GHz) polarization horizontal (2.86 the −2 band from at S obtained cross-sections GHz at Radar 2.47 47). calculated at dielectric ref. Borer in and Grain 5 10.2391, (Lesser table 15.21 of to ratio 42.8 length-to-height of permittivity 8.8246, of 45). ratio prolate (44, equimass to-width an frequencies a created of we radar model 44, at ref. ellipsoid in biota described methods of the for cross-sections Following technique modeling radar package electromagnetic software the effective WIPL-D an predicting be the to in shown implemented been as has moments of method 2, The (Fig. the scan Calculating volume in radar aloft the mayflies in individual captured of snapshot number Lower cm final the total The (0.00179 during subsection). estimated mayfly domain following the individual the in is an described result of is centimeters cross-section method (units: individual; radar summed per the was domain by radar centimeters divided entire (units: the sample from radar area the in present area si e.1,tevlm farpc ape a acltdfo beam from calculated was sampled centimeters airspace (units: reflectivity of kilometers volume (units: the geometry 19, sig- ref. 3 mayfly in a classified As using of field despeckled all resulting was altitudes, the nals Finally, sea- high computations. at emergence up present the speed 2 be avoid of the not to above ends should removed sweeps mayflies the were pix- because at all dB Fourth, birds Third, 5 son. removed. migrating than were less from lake) the reflectivity contamination the of differential of outside having (i.e., outside els section and spa- previous buffer the the of river in outside 10-km pixels described of all domains Second, threshold analysis dBZ. tial ratio 45 of depolarization in threshold their described factor reflectivity applying methods polarimetric by signals the 43 meteorological using all ref. removed First, the described and modifications. (using workflow identified following the were the twilight with following civil 19 processed after using ref. and Python in h into (42) 4 read package was the to Py-ART scan volume the before downloaded radar local h Each and of package). 1 time package) Boto3 Python from the PyEphem scans found Python we volume the period, radar this (using in twilight chi- day civil (e.g., each phenology 1 For emergence biomass midges). as avoid earlier ronomid to with season served taxa emergence also other window our from analysis contributions defined This August. we 15 July), through June early Based in present). of through occurring 2012 phenology (typically spring known (i.e., the sites were radar on measurements three dual-polarization the which at during available period the to analysis ◦ Hexagenia n costefl e f30aiuhage ie,apcsrepresen- aspects (i.e., angles azimuth 360 of set full the across and ). sarsl fterdrpoesn oko,ec aa volume radar each workflow, processing radar the of result a As Hexagenia afl 005g 4)sc ht15154620individuals 115,165,486,290 that such (46) g) (0.035 mayfly 2 ◦ Hexagenia a ae ob h otrpeettv au for value representative most the be to taken was ) lvto nl eermvdfo h nlssto analysis the from removed were angle elevation aa rs-eto rmEetoantcModeling. Electromagnetic from Cross-Section Radar 2 1)t il .9gm g 2.19 yield to (15) ) 2 n oten[5,2,1 m [353,425,712 southern and ] 3 n utpidb h orsodn radar corresponding the by multiplied and ) 2 Hexagenia Lower × afl sn aso .3 4) length- (46), g 0.035 of mass a using mayfly kilometers tutrn lmn olwn e.43. ref. following element structuring 3 −2 .T vi obecutn individu- counting double avoid To ). y −1 mrecso hs waterways these on emergences ,w iieteana asflux mass annual the divide we ), −3 ooti h backscattering the obtain to ) −2 y −1 2 .Tebackscattering The ). Lower etk h same the take We . 2 udmi areas) subdomain ] −2 .Ti ercis metric This ). 25d and dB −12.5 sn 0 of 50% using 2 and ) 2 rnir rn 803 n S–iiino rdaeEuainGrant Education Graduate on of of Emerging discussions NSF–Division draft of for and early NSF–Division 1545261. an by Knutson 1840230 supported on Grant M. was commenting Frontiers research for and Vaughn This Haro, C. manuscript. C. the R. and Sullivan, phenology mayfly J. Baumgardt, D. (41). ACKNOWLEDGMENTS. cloud Services Web open Amazon is the analysis on this in archived used and measurements access radar NEXRAD of dataset full The Availability. Data resource food this by supported be arrive birds). can we million that (65), (53.6 nestlings period of development number 15-d total the the over at nestling required a the raise by total to kcal) the billion kcal Dividing (12.016 224 emergence 24). the emergence (23, of insect season content aquatic caloric nesting annual on the rely during fledglings to feeding shown (12.016 for been bicolor has content (Tachycineta that caloric swallow insectivore tree annual aerial the get took We to calories). individuals) trillion billion (115 single emergence a in tained Hexagenia and deposition atmospheric of 33% inputs). total (i.e., of mass 0.74% input from to Basin respect values with Erie export input Lake Western these the compared total from genia We 2013 export the tons). phosphorus as (1,732 the well phospho- with sources as reactive 2013) all soluble in including tons annual data input (39 the the deposition took from atmospheric We from Huron 63. rus Lake ref. from in presented contributions Erie tables inflow Lake Western with the to summed inputs Basin phosphorus reactive soluble of (2013) using mates 15 Calculations. Budget ref. Phosphorus Erie in Lake as scaled subdomains, southern (62) and samples northern River the benthic Mississippi sites, of refs. for area the respectively. the in surface taken of benthic found was of the 13 of approach be details and 50% same can 8 Full This 3 pools 49–61. Fig. Basin. on habitable and in Erie 18 the appearing 17, Lake den- by strategies 15, nymph Western densities sampling scale multiplying and the to dates, by of 15 abundance area ref. radar. basin repre- in benthic by full more presented surveyed be to method subimagoes should the sities emerging nymphs follow 3, of 2 emergence, we (Fig. abundance year Finally, to nymphs the of egg class abundance of from age the sentative cycle 2 that development year other expect 2-y of all we a density with Following the circles). consistent as blue well triangles) as downward-pointing all surveys blue total of benthic the 3, density both total plotted (Fig. year. we the sity that and present class, for age studies to points all year,nymphs season 17, a the study ref. within of seasons during Hexagenia unique exception several samples multiple study across the took in taken single With studies result were a multiple cases samples represents if if these season— such, 3 and or study As Fig. year given year. same in a given taken within point the samples typically site Each for samples all sites. multiple of average of with season—the bottom, variety lake a of across nymphs studies of meter These units using 49–61). square density 18, benthic per estimates of 17, terms (15, historical in abundance Basin of nymph Erie present review Lake Western literature throughout a veys represent 3 Fig. Estimation. of in Abundance shown Historical ples and Sampling Benthic US Midwest upper from (48). are populations (0.35%) phosphorus and of (10%), Values nitrogen prey. (43%), to subsidy the demonstrate to phosphorus billion m (2.56 kg nia 72.5 spring of States, flux and United passage northern a birds) the in along resulting billion transect 4,503.22-km (3.97 a over fall passage birds) annual the considered we (3,200 biomass dividing m g by flux (8) final migrants the y insect tons reach high-altitude to of km) flux (697 annual domain m analysis kg river (1.0336 the units (2.05835178e10 of 2012 length meter the in (grams by production 2 mayfly ref. y annual in individuals total presented as the shoreline example, the For along as well as Hexagenia ims n iflxt lmna otiuin fcro,ntoe,and nitrogen, carbon, of contributions elemental to bioflux and biomass −2 −1 mrec n21 1.6tn)t n h ecnaeo phosphorus of percentage the find to tons) (12.86 2013 in emergence y −1 ypsaeae 7,0 km (70,000 area passage by ) .Smlry o irtn id iha vrg aso 0g(11), g 50 of mass average an with birds migrating for Similarly, ). nrei Calculations. Energetic ypswti h ape n td 1)frhridentified further (17) study One sample. the within nymphs −1 yp este bandb rdeadga apesur- sample grab and dredge by obtained densities nymph scnetdt ims 704313gy g (720,423,123 biomass to converted is ) −1 eaei limbata Hexagenia y −1 etakM tigabr .Posthumus, E. Steingraeber, M. thank We .W pl hssm prahfrcluaigthe calculating for approach same this apply We ). trigwt h 0.9clre con- calories 104.49 the with Starting 2 −1 ooti h rpruis(0.04571 units proper the obtain to ) 6) emlil yteLk Erie Lake the by multiply we (64), y eotie h otrcn esti- recent most the obtained We −1 ial,w converted we Finally, . NSLts Articles Latest PNAS Hexagenia h eti sam- benthic The Hexagenia −1 n divided and ) samodel a as ) yp den- nymph −1 Hexage- | carbon Hexa- f6 of 5 y −1 ).

ENVIRONMENTAL ECOLOGY SCIENCES 1. I. Gounand, C. J. Little, E. Harvey, F. Altermatt, Cross-ecosystem carbon flows con- 37. D. R. Reynolds, J. R. Riley, Radar observations of concentrations of insects above a necting ecosystems worldwide. Nat. Commun. 9, 4825 (2018). river in Mali, West Africa. Ecol. Entomol. 4, 161–174 (1979). 2. D. M. Walters, J. S. Wesner, R. E. Zuellig, D. A. Kowalski, M. C. Kondratieff, Holy flux: 38. P. M. Stepanian, K. G. Horton, V. M. Melnikov, D. S. Zrnic,´ S. A. Gauthreaux Jr., Spatial and temporal variation in massive pulses of emerging insect biomass from Dual-polarization radar products for biological applications. Ecosphere 7, e01539 western U.S. Rivers. Ecology 99, 238–240 (2018). (2017). 3. O. J. Schmitz et al., Animals and the zoogeochemistry of the carbon cycle. Science 39. R. H. Diehl, R. P. Larkin, “Introduction to the WSR-88D (NEXRAD) for ornithologi- 362, eaar3213 (2018). cal research” in Bird Conservation Implementation and Integration in the Americas: 4. R. Nathan et al., A movement ecology paradigm for unifying organismal movement Proceedings of the Third International Partners in Flight Conference, C. J. Ralph, research. Proc. Natl. Acad. Sci. U.S.A. 105, 19052–19059 (2008). T. D. Rich, Eds. (US Department of Agriculture, Forest Service, Pacific Southwest 5. S. Bauer, B. J. Hoye, Migratory animals couple biodiversity and ecosystem functioning Research Station, Albany, CA, 2005), pp. 876–888. worldwide. Science 344, 1242552 (2014). 40. R. P. Larkin, R. H. Diehl, “Radar techniques for wildlife research” in The Wildlife Tech- 6. N. E. Hussey et al., telemetry: A panoramic window into the niques Manual, N. J. Silvy, Ed. (The Johns Hopkins University Press, Baltimore, MD, underwater world. Science 348, 1255642 (2015). ed. 7, 2012), pp. 319–335. 7. R. Kays, M. C. Crofoot, W. Jetz, M. Wikelski, Terrestrial animal tracking as an on 41. Amazon Web Services, NEXRAD on AWS. https://s3.amazonaws.com/noaa-nexrad- life and planet. Science 348, aaa2478 (2015). level2/index.html. Accessed 1 July 2019. 8. G. Hu et al., Mass seasonal bioflows of high-flying insect migrants. Science 354, 1584– 42. J. J. Helmus, S. M. Collis, The Python ARM Radar Toolkit (Py-ART), a library for working 1587 (2016). with weather radar data in the Python programming language. J. Open Res. Softw. 9. J. W. Chapman et al., Flight orientation behaviors promote optimal migration 4, e25 (2016). trajectories in high-flying insects. Science 327, 682–685 (2010). 43. A. Kilambi, F. Fabry, V. Meunier, A simple and effective method for separating mete- 10. B. M. Van Doren, K. G. Horton, A continental system for forecasting bird migration. orological from nonmeteorological targets using dual-polarization data. J. Atmos. Science 361, 1115–1118 (2018). Ocean. Technol. 35, 1415–1424 (2018). 11. A. M. Dokter et al., Seasonal abundance and survival of north America’s migratory 44. D. Mirkovic, P. M. Stepanian, J. F. Kelly, P. B. Chilson, Electromagnetic model reliably avifauna determined by weather radar. Nat. Ecol. Evol. 2, 1603–1609 (2018). predicts radar scattering characteristics of airborne organisms. Sci. Rep. 6, 35637 12. C. R. Fremling, Documentation of a mass emergence of hexagenia mayflies from the (2016). Upper Mississippi River. Trans. Amer. . 4, 373–398 (1994). 45. D. Mirkovic, P. M. Stepanian, C. E. Wainwright, D. R. Reynolds, M. H. M. Menz, Char- 13. J. S. Schaeffer, J. S. Diana, R. C. Haas, Effects of long-term changes in the benthic acterizing animal anatomy and internal composition for electromagnetic modelling community on yellow perch in Saginaw Bay, Lake Huron. J. Gt. Lakes Res. 23, 340–351 in radar entomology. Remote Sens. Ecol. Conserv. 5, 169–179 (2019). (2000). 46. J. R. Coelho, Body temperature and flight muscle ratio in the burrowing mayfly, 14. T. B. Reynoldson, D. W. Schloesser, B. A. Manny, Development of a benthic inverte- . J. Freshw. Ecol. 14, 337–341 (1999). brate objective for mesotrophic great lakes waters. J. Great Lakes Res. 97, 278–281 47. S. O. Nelson, P. G. Bartley Jr., K. C. Lawrence, RF and microwave dielectric properties (1968). of stored-grain insects and their implications for potential insect control. Trans. ASAE 15. B. A. Manny, Burrowing mayfly nymphs in Western Lake Erie, 1942-1944. J. Great 41, 685–692 (1998). Lakes Res. 17, 517–521 (1991). 48. M. A. Evans-White, R. S. Stelzer, G. A. Lamberti, Taxonomic and regional patterns in 16. J. K. Jackson, L. Fureder,¨ Long-term studies of freshwater macroinvertebrates: A benthic macroinvertebrate elemental composition in streams. Freshwater Biol. 50, review of the frequency, duration and ecological significance. Freshwater Biol. 51, 1786–1799 (2005). 591–603 (2006). 49. S. Wright, W. M. Tidd, Summary of limnological investigations in western Lake Erie in 17. M. A. Stapanian, P. M. Kocovskˇ y,´ B. L. Bodamer Scarbro, Evaluating factors driving 1929 and 1930. Trans. Am. Fish. Soc. 63, 271–285 (1933). population densities of mayfly nymphs in western Lake Erie. J. Great Lakes Res. 43, 50. V. E. Shelford, M. W. Boesel, Bottom animal communities of the island area of western 1111–1118 (2017). Lake Erie in the summer of 1937. Ohio J. Sci. 42, 179–190 (1942). 18. D. W. Schloesser, K. A. Krieger, J. J. H. Ciborowski, L. D. Corkum, Recolonization and 51. K. Wood, “Distribution and ecology of certain bottom-dwelling invertebrates of the possible recovery of burrowing mayflies (Ephemeroptera: : Hexagenia western basin of Lake Erie,” PhD thesis, The Ohio State University, Columbus, OH spp.) in Lake Erie of the Laurentian Great Lakes. J. Aquat. Ecosyst. Stress Recovery 8, (1953). 125–141 (2000). 52. N. W. Britt, Hexagenia (Ephemeroptera) population recovery in western Lake Erie 19. P. M. Stepanian, C. E. Wainwright, Ongoing changes in migration phenology and following the 1953 catastrophe. Ecology 36, 520–522 (1955). winter residency at bracken cave. Glob. Change Biol. 44, 3266–3275 (2018). 53. J. F. Carr, J. K. Hiltunen, Changes in the bottom fauna of western Lake Erie from 1930 20. D. W. Schloesser, K. A. Krieger, J. J. H. Ciborowski, L. D. Corkum, Timing of hexagenia to 1961. Limnol. Oceanogr. 10, 551–569 (1965). (Ephemeridae:Ephemeroptera) mayfly swarms. Can. J. Zool. 84, 1616–1622 (2006). 54. US Department of Interior, “Lake Erie environmental summary 1963-1964” 21. L. L. Wright, J. S. Mattice, Emergence patterns of Hexagenia bilineata: Integration of (Tech. Rep., Federal Control Administration, Cleveland, OH, laboratory and field data. Freshw. Invertebr. Biol. 4, 109–124 (1985). 1968). 22. J. Dreyer et al., Quantifying aquatic insect deposition from lake to land. Ecology 96, 55. D. M. Veal, D. S. Osmond, “Bottom fauna of the western basin and near-shore Cana- 499–509 (2015). dian waters of Lake Erie” in Proceedings of the 11th Conference of Great Lakes 23. C. Wingfield Twining, J. Ryan Shipley, D. W. Winkler, Aquatic insects rich in omega- Research (International Association for Great Lakes Research, Ann Arbor, MI, 1968), 3 fatty acids drive breeding success in a widespread bird. Ecol. Lett. 21, 1812–1820 pp. 151–160. (2018). 56. N. W. Britt, A. J. Pliodzinskas, E. M. Hair, “Benthic macroinvertebrate distribution in 24. C. W. Twining et al., Aquatic and terrestrial resources are not nutritionally reciprocal the central and western basins of Lake Erie” in Lake Erie Nutrient Control Program, for consumers. Funct. Ecol. 33, 2042–2052 (2019). C. Herdendorf, Ed. (USEPA, Duluth, MN, 1980). 25. K. J. Spiller, R. Dettmers, Evidence for multiple drivers of aerial insectivore declines in 57. R. Dermott, “Benthic invertebrate fauna of Lake Erie 1979: Distribution, abundance north America. Condor 121, duz010 (2019). and biomass” (Tech. Rep., Great Lakes Laboratory for Fisheries and Aquatic Sciences, 26. L. D. Mortsch, F. H. Quinn, Climate change scenarios for Great Lakes basin ecosystem Canada Centre for Inland Waters, Burlington, ON, Canada, 1994). studies. Limnol. Oceanogr. 4, 373–398 (1994). 58. OME, “An assessment of the bottom fauna and sediments of the western basin 27. T. B. Bridgeman, D. W. Schloesser, A. E. Krause, Recruitment of Hexagenia mayfly of Lake Erie, 1979” (Tech. Rep., Ontario Ministry of the Environment, London, ON, nymphs in Western Lake Erie linked to environmental variability. Ecol. Appl. 16, Canada, 1981). 601–611 (2006). 59. B. A. Manny, D. W. Schloesser, Changes in the Bottom Fauna of Western Lake Erie 28. A. M. Michalak et al., Record-setting in Lake Erie caused by agricultural (Backhuys Publishers, Leiden, the Netherlands, 1999), pp.197–217. and meteorological trends consistent with expected future conditions. Proc. Natl. 60. D. G. Farrara, A. J. Burt, “Environmental assessment of western Lake Erie sediments Acad. Sci. U.S.A. 110, 6448–6452 (2011). and benthic communities—1991” (Tech. Rep., Beak Consultants Limited, Brampton, 29. J. L. Smith, G. L. Boyer, E. Mills, K. L. Schulz, Toxicity of microcystin-LR, a cyanobacte- ON, Canada, 1993). rial toxin, to multiple life stages of the burrowing mayfly, Hexagenia, and possible 61. E. L. Green, A. Grgicak-Mannion, J. J. H. Ciborowski, L. D. Corkum, Spatial and tem- implications for recruitment. Environ. Toxicol. 23, 499–506 (2008). poral variation in the distribution of burrowing mayfly nymphs (Ephemeroptera: 30. N. C. Everall, M. F. Johnson, P. Wood, L. Mattingley, Sensitivity of the early life stages and H. rigida) in western Lake Erie. J. Gt. Lakes Res. 39, 280–286 of a mayfly to fine sediment and orthophosphate levels. Environ. Pollut. 237, 792–802 (2013). (2018). 62. J. Sauer, “Multiyear synthesis of the macroinvertebrate component from 1992 to 31. M. L. Hladik et al., Year-round presence of neonicotinoid in tributaries to 2002 for the long term resource monitoring program” (Tech. Rep. 2004-T005, US the Great Lakes, USA. Environ. Pollut. 235, 1022–1029 (2018). Geological Survey, Upper Midwest Environmental Sciences Center, La Crosse, WI, 32. A. J. Bartlett et al., Lethal and sublethal toxicity of neonicotinoid and butenolide 2004). insecticides to the mayfly, Hexagenia spp. Environ. Pollut. 238, 63–75 (2018). 63. M. J. Maccoux, A. Dove, S. M. Backus, D. M. Dolan, Total and soluble reactive phos- 33. L. Hunt et al., concentrations in stream sediments of soy production phorus loadings to Lake Erie a detailed accounting by year, basin, country, and regions of South America. Sci. Total Environ. 547, 114–124 (2016). tributary. J. Gt. Lakes Res. 42, 1151–1165 (2016). 34. C. A. Hallmann et al., More than 75 percent decline over 27 years in total flying insect 64. E. M. Dean, “The effect of seasonal fish migration on energy budgets in two coastal biomass in protected areas. PLoS One 12, e0185809 (2017). Michigan streams,” Master’s thesis, Grand Valley State University, Allendale, MI 35. S. R. Leather, “Ecological armageddon”—more evidence for the drastic decline in (2016). insect numbers. Ann. Appl. Biol. 172, 1–3 (2018). 65. J. W. Nichols, C. P. Larsen, M. E. McDonald, G. J. Niemi, G. T. Ankley, Bioenergetics- 36. B. I. Simmons et al., Worldwide insect declines: An important message, but interpret based model for accumulation of polychlorinated biphenyls by nestling tree swallows, with caution. Ecol. Evol. 9, 3678–3680 (2019). tachycineta bicolor. Environ. Sci. Technol. 29, 604–612 (1995).

6 of 6 | www.pnas.org/cgi/doi/10.1073/pnas.1913598117 Stepanian et al. Downloaded by guest on September 30, 2021