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106 American Entomologist • Summer 2009
Periodical cicadas (genus Magicicada) are found only in eastern North America and are notable for their long, prime-numbered life cycles, precisely timed mass emergences, and
dense, multispecies choruses. Their uniqueness has given them a special appeal and cultural status. Members of the Onondaga Na-tion maintain the oral tradition of being rescued from famine by periodical cicadas (Cooley et al. 2004). Early European colonists viewed periodical cicadas with a mixture of religious apprehen-sion and loathing (Kritsky 2004); and modern Americans maintain numerous Web sites to assist in planning weddings, graduations, and other outdoor activities around Magicicada emergences (e.g., cicadamania.com). Periodical cicadas have attracted the attention of such scientific luminaries as Linnaeus (who named one of the species), and Darwin, who commented on their unusual life cycles (quoted in Simon et al. 2000). In the future, periodical cicadas may become important bioindicators of ecological health and climate change, both natural and human-mediated (Reding and Guttman 1991, Clark 1992, Cooley et al. 2003, Yang 2004, Heckel and Keener 2007). These diverse ways of understanding periodical cicadas are united by one common theme: all rely on accurate information about emergence timing and location. To facilitate and promote future study, we present a detailed map of Brood X based on field mapping and public information that we solicited via the Internet.
BackgroundPeriodical cicada emergences in different regions are not syn-
chronized; different populations comprise the 15 largely parapatric
periodical cicada “broods,” or year-classes. Complicating matters, there are two life cycles (13 and 17 years), three species groups (-decim, -cassini, and -decula), and seven recognized species of periodical cicada, with slight ecological differences (Alexander and Moore 1962; Dybas and Lloyd 1962, 1974; Lloyd and Dybas 1966a; White 1980) (Marshall and Cooley 2000). Individual broods usually contain multiple synchronized species of the same life cycle type.
Broods are one of the more puzzling aspects of periodical ci-cada biology. On one hand, broods have a kind of cohesiveness in which local populations are bound together by a reliance on high population densities (several million per acre) to effect predator satiation (Dybas and Lloyd 1962, Lloyd and Dybas 1966a, Karban 1982, Williams and Simon 1995). On the other hand, broods can fragment and give rise to other broods, so that small isolated popu-lations separated from the main body of a brood may be relicts of a previously larger brood distribution, or they may have arisen independently from a different brood (Young 1958, Alexander and Moore 1962, White and Lloyd 1979, Simon and Lloyd 1982, Kritsky and Simon 1996). Detailed information about brood ranges, isolated populations, and brood overlap can help clarify their origins and biological interactions.
Our understanding of broods developed from emergent patterns in records accumulated by early naturalists. By the 19th century, enough information existed that several authors developed maps and nomenclatural schemes for keeping track of broods. For example, C. V. Riley (Riley 1885) compiled periodical cicada distribution records and presented a series of maps and schedules that could account
John R. Cooley, Gene Kritsky, Marten J. Edwards, John D. Zyla, David C. Marshall Kathy B. R. Hill, Rachel Krauss, and Chris Simon
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for past emergences and accurately predict future emergences. Riley named each brood by assigning it a Roman numeral, but his nomenclatural scheme did not clearly separate 13- and 17-year pe-riodical cicadas. This situation quickly led to confusion because the progression of emergence sequences of 17- versus 13-year broods disordered the numbering scheme.
To address this problem, C. L. Marlatt (1923) presented a series of distribution maps and proposed a nomenclature for the broods that assigned separate numbering systems to the 13- and 17-year populations. Marlatt designated 17-year broods with Roman numer-als I–XVII, and 13-year broods XVIII–XXX. Marlatt’s nomenclature is the basis for all subsequent published periodical cicada brood maps (e.g., Simon 1988).
Published periodical cicada distribution maps have uses beyond simply cataloguing and predicting emergences. For example, peri-odical cicada distributions allow some inferences about Pleistocene glacial cycles because these insects are so closely associated with eastern deciduous forests (Alexander and Moore 1962, Lloyd and Dybas 1966b, Cox and Carlton 1988, Cox 1992, Marshall et al. 2003). Contemporary climate and habitat change may also be reflected in distribution maps; some brood ranges have contracted noticeably within historical times (Young 1958, Simon 1988, Cooley et al. 2004, Nelson 2004). At least two small broods have become extinct: Brood XXI in the 19th century (Marlatt 1923), and Brood XI between 1954 and 1971 (Manter 1974).
Maps may help reveal the evolutionary implications of disjunct brood patches, such as V, IX, and X on Long Island; XIV in New Eng-land; VI in Wisconsin; or XXIII in DeWitt County, IL—all of which may be independently derived “parallel broods” not related by a common temporal origin to the main body of the brood (Simon and Lloyd 1982). Maps have revealed aspects of periodical cicada biology that bear on processes of speciation in the group, such as the pattern of reproductive character displacement between M. neotredecim and M. tredecim (Marshall and Cooley 2000). Finally, distributional infor-mation provides important tests of hypotheses about the formation of broods and species. Some of these hypotheses invoke patterns of spatial and temporal separation of broods of the same life cycle (Lloyd and Dybas 1966b), overlap of broods of different life cycles (Bryce and Aspinwall 1975), or possible replacement of 17-year cicadas by 13-year cicadas (Lloyd and White 1976, Cox and Carlton 1991).
For all their uses, Marlatt’s maps and their derivatives have limitations. Most records used in these maps were summarized and mapped by county, which limits the resolution of brood edges. Other records used in these maps appear to be incorrect, resulting from confusion with morphologically similar cicadas of the genus Okanagana (e.g., records in Maine or Canada). Marlatt’s maps are also cross-generational: the records for all of the years pertaining to a given brood (e.g., 2008, 1991, 1974) are combined in a single map, making it difficult to identify records that are best explained by off-cycle (“straggler”) emergences from an adjacent or overlapping brood (Marshall 2001). For all of these reasons, Marlatt’s maps tend to overestimate periodical cicada brood ranges (Maier 1985, Marshall 2001). Recent revisions have helped correct some of these problems (Simon 1988), but even so, uncertainties associated with these maps hamper resolution of important questions about periodical cicada brood and life cycle evolution. Any study making use of older maps, or comparing older maps with newer maps, cannot dismiss the possibility that apparent changes in distribution may reflect chang-ing criteria for collecting and evaluating records (Marshall 2001).
There have been efforts to make entirely new periodical cicada maps, including Stannard’s maps of the Illinois broods (Stannard 1975), Kritsky’s 1987 map of Brood X in Ohio (Kritsky 1988), and Zyla’s map of Brood XIX in Maryland (Zyla 2004), but no projects have been attempted on the scale of whole-brood distributions, and few such efforts have relied on recent advances in inexpensive GPS devices and georeferencing software. So far, only published maps of Brood VII (Cooley et al. 2004) and partial maps of Brood III (Irwin and Coelho 2000) and Brood X (Edwards et al. 2005) consist entirely of newly acquired, georeferenced records.
In this article, we present maps of the 2004 emergence of periodi-cal cicada Brood X, among the largest, by geographical extent, of all 17-year periodical cicada broods. Earlier maps show that this brood is divided into three main regions and bordered by several other broods (Fig. 1). Our maps are based exclusively on more than 8,000 positive (present) and negative (absent) georeferenced records that are available to the public (searchable database: http://hydrodictyon.eeb.uconn.edu/projects/cicada/). These records are of two types: “field-verified records” and “unverified records.” Field-verified records (~45% of records) were collected by the authors and their research groups. We made no attempt to search the entire possible distribution of Brood X uniformly. Rather, each research group con-centrated on mapping either general distributions or brood edges in specific areas. The Edwards group collected distribution records in
Pennsylvania (Edwards et al. 2005); the Kritsky group surveyed dis-tributions in southern Ohio; the UConn group mapped brood edges in southern Illinois and Indiana; and the Zyla group mapped the limits of Brood X in Delaware, Maryland, Virginia, and West Virginia. To col-lect records, we searched within the known distribution of the brood and in adjacent areas for physical evidence of cicadas (emerging nymphs, cast skins, adults, etc.). We also listened for singing cicadas by driving slowly (<40 mph) along roads with car windows open. We obtained negative records by listening or searching at locations (with no vehicle engine running) for a minimum of 2 minutes. We collected locality information by using handheld GPS units, writing detailed location descriptions, or marking highly detailed road maps and digitizing the latter two types of record using GIS or geocoding
Fig. 1. Composite map of all extant periodical cicada broods, adapted from maps published in Marlatt (1923) and Simon (1988). Base map is the original Marlatt base map. Individual brood records in Marlatt and Simon maps were traced on this map and then modified by removing or adding records on the basis of unpublished data. For clarity, dot size has been reduced.
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software packages (Arcview 3.0, Street Atlas, Google Earth). At some locations, we also recorded choruses using a Marantz digital recorder or a Sony DAT recorder sampling at 48 kHz.
Unverified records consist of observations submitted by the public through specific Web sites, e-mails, or other communications in response to media solicitations in the Washington, DC, Cincinnati, OH, and Allentown, PA, regions. Records submitted by the public con-sisted of locality information (a street address, intersection, public park, etc.) and comments. The comments sections of the records were examined, and records that described the emergences incorrectly (e.g., wrong body colors, nocturnal choruses, wrong time of year) were discarded (~3% of all records).
Locality information was used to geocode the remaining records in the following manner: the records were first submitted in batches to the Google Maps API geocoder (~7% of records were geocoded this way). Records that could not be geocoded in this way were geocoded by hand, using Google Earth (~37% of records). Records that did not describe unique locations or that could not be geocoded (~8% of all records) were discarded. All geocoded records were placed as a data layer in an Arc GIS 9.2 map, and records that fell far outside the known boundaries of the brood were discarded, as were records whose geocoded location fell outside the state or county described in the record submission (<5% of all records). All remaining records were entered into a database (http://hydrodictyon.eeb.uconn.edu/projects/cicada/) and used as layers in an Arc GIS 9.2 map.
ResultsOur map (Fig. 2) includes field-verified positive records (dark
green), in which we have a high degree of confidence; unverified
positive records (light green); verified negative records (dark gray); and unverified negative records (open circles). Like Marlatt, we do not attempt to delineate brood boundaries by drawing closed areas around data points. Because we concentrated our efforts on only some locations, our verified records do not include many loca-tions where unverified records suggest cicadas were present. It is also not possible to judge how completely the unverified records sample the range of Brood X. For these reasons, this map should not be considered exhaustive, although it may be used to estimate the brood’s boundaries.
Several assumptions are necessary to interpret the unverified records in our map. First, even though individual unverified records are open to doubt, clusters of records validate each other and suggest a higher degree of confidence. Likewise, given the degree of media saturation and the number of responses, it is unlikely that there were large, unnoticed populations near the metropolitan areas where media coverage was greatest. Thus, the total absence of records from a given area within one of these well-sampled regions suggests that no cicadas were present. Unverified records should not be used to make inferences about brood boundaries or range changes, but we have included them because they provide sampling in areas that the mapping teams could not investigate, and they will serve as a guide to future mapping efforts.
Given these assumptions, this new map, like earlier maps, sug-gests three main divisions in Brood X: a Midwestern division in western Ohio, southern Michigan, Indiana, and eastern Illinois; a southern division in eastern Tennessee, western North Carolina, and northern Georgia; and an eastern division concentrated in Washington, DC, Pennsylvania, northern Maryland, northern Dela-
Fig. 2. Map of records collected during
the 2004 emer-gence. Positive
records collected or verified by the
authors are shown in dark green; unverified positive records collected from the general public are
shown in light green. Verified negative records are shown in dark gray and unverified negative records are shown as open circles. Base map is USGS National Land Cover Database (NLCD) 2001 30m resolution forest canopy (Homer et al. 2004, Homer et al. 2007)
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ware, northern Virginia, and eastern West Virginia (Fig. 2). Brood X includes several metropolitan areas, such as Princeton, NJ; Wash-ington, DC; Philadelphia; Indianapolis; Cincinnati; and a scattering of records on Long Island, NY. We received no reports from west of the Mississippi River.
In the eastern United States, the 2004 Brood X map (Fig. 2) gener-ally resembles maps such as those published by Marlatt and Simon (Fig. 1), although the new map suggests a smaller range for Brood X in the East. Brood X does not appear to reach as far north in most of Pennsylvania as suggested by Marlatt’s county-level dots, nor is the coverage of New Jersey as extensive as suggested by the earlier records. In at least one area, the new map suggests a larger range than was reported historically. The southwestern edge of Brood X in Pennsylvania was comparatively well sampled with positive and negative records, and it appears to extend farther west than the old records, into central Somerset County. The records from Garrett County, MD, also appear to extend the range, or at least resolve it with better precision. The unverified public report from southern Armstrong County, PA, should be checked in future emergences. Whether the differences between old and new maps are due to range changes or are artifacts of map-making techniques (e.g., we used smaller dots on our map and did not lump records by county) is open to question.
Some of the field-verified records are of populations at surpris-ingly low density for Magicicada, sometimes so low that they consist of scattered individuals rather than full choruses (Fig. 3). Some of these records, such as those in northern Kentucky, are found in locations where Brood X and XIV border each other, and some are fully within the known range of Brood XIV (Lloyd and White 1976; Cooley et al. unpublished data). Such low-density populations could belong to either Brood X or XIV because periodical cicadas occasion-ally emerge off-schedule. When periodical cicadas accelerate,they tend to do so in increments of 1 or 4 years, with 4-year advance emergences especially common among 17-year species (Lloyd and Dybas 1966b, Simon et al. 1981, Simon and Lloyd 1982, Kritsky 1987). In some circumstances, repeated instances of straggling may allow low-density populations to exist at the periphery of a brood. For example, where two adjacent broods are separated by 4 years, early stragglers from the later brood will be synchronized with the earlier brood, and straggler populations may be able to persist
because their synchronization with an existing brood affords them some limited predator immunity.
This phenomenon of low-density, peripheral populations may be an important avenue of gene flow between two broods (Heliövaara et al. 1994). It may also be a source of confusion about brood boundaries because stragglers from one brood may be mistaken for low-density populations of another brood (Edwards et al. 2005). There is no way yet known to determine the age of an adult periodical cicada, nor are there known genetic differences among broods of the same life cycle, so that where two broods are adjacent, unambiguously as-signing brood membership to some border populations may not be possible. We include records of low-density populations in our map of the 2004 Brood X emergence with the caveat that brood member-ship of low-density, peripheral populations is an open question, and with the hope that these records will be carefully examined during upcoming emergences of Broods XIV, II, V, and VI or other brood pairs with shared boundaries (e.g., I/V, II/VI, V/IX).
Older brood maps (Fig. 1) suggest that many broods inhabit well-defined regions. Older maps also tend to portray broods as over-lapping, discounting the possibility that broods are fragmented, inter-digitating, or that some enclose isolated populations of other broods. Thus, the spatial relationships of many neighboring broods—such as II, VI, V, VI, IX, X and XIV—are not well understood (Fig. 1). More detailed records are needed to determine whether these broods are fragmented, whether or not they overlap locally in some regions, or whether the apparent confusion is mainly a consequence of accu-mulated records of stragglers (Lloyd and White 1976, Maier 1982, Marshall 2001). Detailed, Internet-based surveys of the public, com-bined with efforts to verify key records, have the potential to detect rare, isolated populations and resolve complex brood boundaries. In the Baltimore–Washington, DC, region, the public records from 2004 show that the closely spaced county-level dots from earlier maps correspond to an almost continuous band of populations, saturated even at the scale of Fig. 4. Similarly, the complete absence of negative public records from large areas of south-central Pennsylvania and central Maryland, combined with evenly spaced positive records, suggests that Brood X is also widespread in that region and not inter-rupted by populations of other broods. At the same time, clusters of negative records suggest that populations of other broods may be isolated within the range of Brood X (e.g., York and Adams Counties,
Fig. 3. Verified positive re-cords of low-density popu-lations (blue symbols) and verified positive records (green symbols) found in Kentucky during the 2004 emergence. At each record location, on days and at times appropriate for chorusing activity, only single individuals or a handful of individuals were heard, and no choruses were heard. We made no attempt to survey the entire periphery, so other low-density populations may exist elsewhere.
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PA). Revised maps of Broods XIV and II may show that these other broods completely surround isolated populations of Brood X. Once clarified, these patterns may be used to understand the climatic events or other processes that lead to temporal isolation and brood formation in periodical cicadas.
Our data add some information to ongoing discussions of contact zones between broods with different life cycles. There are two known major mitochondrial lineages in the “decim” species of periodical cicada, and contact between these lineages is of particular interest to theories of life cycle switching and species formation (Cox and Carlton 1988, 2003; Lloyd et al. 1983; Marshall and Cooley 2000; Cooley et al. 2001; Simon et al. 2000 Marshall et al. 2003). Lineage “A” is found in M. neotredecim and M. septendecim, and lineage “B” is found only in M. tredecim (Martin and Simon 1988, 1990; Cooley et al. 2001). Where M. neotredecim and M. tredecim co-occur in Broods XIX and XXIII, these lineages are in contact and display positive as-sortative mating and a striking pattern of reproductive character displacement in M. neotredecim calling song pitch (Marshall and Cooley 2000, Simon et al. 2000, Cooley et al. 2006).
This pattern suggests that these lineages have a history of selection against interbreeding. The two mitochondrial lineages also come into contact wherever M. septendecim in Brood X (or Broods II, VI, IX, or XIV) is in contact with M. tredecim (Broods XIX or XXIII), although co-emergences occur only once every 221 years. One hypothesis is that there are undiscovered patterns of reproductive character displace-ment along this contact zone; however, it is also possible that co-emer-gences are too rare to cause sufficient divergent selection on mating signals. Where we mapped Illinois and Indiana in detail, we found no evidence of reproductive character displacement within Brood X; across its range, M. septendecim chorus pitch from 2004 Brood X was between 1.29 and 1.37, well within the 1.25–1.50 kHz range reported for this species (Fig. 5; Marshall and Cooley 2000). Our unpublished data suggest that overlap between Brood X and the 13-year broods is minimal. In Maryland, no Brood X emergences were reported in St. Mary’s County, which contains 17-year Brood II and the only known
Maryland localities for 13-year Brood XIX (Fig. 2; Zyla 2004). In southern Indiana, Broods X and XXIII have a complex microparapatric relationship, including at least one area of slight overlap in the same woods; in Illinois, Brood X does not currently contact Broods XIX or XXIII, nor does it contact 17-year Brood XIII (unpublished data).
Our map is a single-generation map of Brood X as it emerged in 2004. We urge caution in making inferences about range changes based on differences between our map and other published maps. Al-though range contraction could explain some discrepancies between our map and earlier maps, other explanations include the incomplete sampling of our map, the lower precision of earlier maps, and the tendency of cross-generational data sets to accumulate erroneous records (Marshall 2001). Although this map, by itself, cannot resolve past questions about range change, it will be useful as a baseline map for future emergences of Brood X and all adjacent broods. Any differences between a map based on the 2021 emergence and this 2004 map, especially in areas where we have identified the brood boundary with positive and negative records, would be strong evi-dence for range changes.
AcknowledgmentsSteve Chiswell, Richard Crist III, Amy Faivre, Andrew Martin,
Margaret Pfiester, Michael Sitvarin, Jessee Smith, Paige Swientisky, Jennifer Webb, and Zachary Zyla provided assistance in the field. We also thank the owners of our research sites. This work was made possible by a National Geographic grant to JC, a NASA Grant NAG5-12416 to Muhlenberg College, Grants to GK from The College of Mount St. Joseph, and National Science Foundation Grants. DEB 99-82039, NSF DEB 04-22386, DEB 05-29679, DEB 06-19012 (REU), and DEB 07-20664 to CS. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the NSF. CS would like to dedicate this paper to the memory of her father Walter W. Simon in recognition for his help in collecting many broods of cicadas and for first introducing her to Magicicada when she was 12 years old.
Fig. 4. Detail of 2004 Brood X emergence in the eastern United States. Verified posi-tive records are shown
in dark green; unverified positive records collected
from the public are shown in light green. Verified negative records are shown in dark gray, and unverified negative records are shown as open circles.
American Entomologist • Volume 55, Number 2 111
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Fig. 5. Verified positive records where M. septendecim chorus recordings were taken and analyzed. At each location, M. septendecim choruses were recorded with a Marantz digital recorder or a Sony DAT recorder sampling at 48 kHz. Recordings were not filtered, but background noise (pops, traffic, voices, etc.) was edited out, and 1–2-min samples were analyzed using Canary 1.2 (Cornell Bioacoustics Laboratory, Ithaca, NY). The dominant frequencies (pitch-es) of representative locations are shown in kHz.
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discussion, but the consensus is that stridu-lation is a defense against predators. At least one competing hypothesis, however, led to yet another appearance of kissing bugs in popular culture (Askew 1971). According to a front page story in the U.K. Guardian that ran on June 7 1966, the United States Pentagon was reported to be “planning to send bed-bugs [sic] to help to win the war in Vietnam...Their plans are based on the fact that bed-bugs scream with excitement at the prospect of feasting on human flesh [sic!] ...a sound amplification system would enable the GI, sweating through the jungles of South Vietnam, to hear the anticipatory squeals of a captive bed-bug as it detects the Vietcong lying in ambush ahead. Tests have apparently shown that a large and hungry bed-bug will appropriately register the pres-ence of a man some two hundred yards to its front or side, while ignoring the person carrying it in a specially devised capsule” (The Guardian 7 June 1966).
There are so many biological improb-abilities in the Guardian account that it’s hard to believe that such a proposal was ever seriously considered by the Department of Defense—although it must be noted that this same War Department was accused by the Nazi government in 1942 of plotting to drop
15,000 Colorado potato beetles onto German potato fields to destabilize German food supplies (leading to the establishment of a Kartoffelkaferabwehrdienst (Potato Beetle Defence Service) in Kruft), and by the gov-ernment of the German Democratic Republic in 1950 of actually dropping thousands of Colorado potato beetles in the southwest part of the country to demoralize a nation fond of its potato dumplings (Garrett 1996). For one thing, most estimates of the distance from which blood-sucking bugs can detect a human blood meal are in the range of 10 to 20 feet, not 200 yards; moreover, it’s unclear how or why bugs would ignore a potential blood meal almost underfoot in preference to a meal two football fields away, and there’s no evidence that bugs can differentiate between allies and hostile forces. Finally, what adaptive value there might be to a bug of announcing its presence by squealing in anticipation while stalking its prey is a mystery; it would seem such squeals are completely inconsistent with the stealth strategy displayed by the group as a whole. If nothing else, any Viet Cong within earshot would know of the presence of an American soldier immediately upon hearing the squeal. It would seem, then, that the amplified scream of a kissing bug could instead be a signal for the American soldier to kiss his butt goodbye. 7
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JohnR.Cooley, Lecturer at Yale University, studies the behavior and evolu-tion of cicadas. Current information about the cicada mapping project may be found at www.magicicada.org. GeneKritsky, a Professor at the College of Mount St. Joseph, has written a number of books and papers about pe-riodical cicadas. MartenEdwards is a mosquito physiologist and teaches entomology as an Associate Professor at Muhlenberg College. JohnD.Zyla studies both periodical and annual cicada distribution in the Mid Atlantic states and runs the Mid-Atlantic Cicadas website (www.cicadas.info). DavidC.Marshall is a postdoctoral associate in the Simon Lab at the University of Connecticut (UConn) studying the behavior and evolution of singing insects. KathyB.R.Hill studies phylogenetic relationships of world cicada species and cicada behaviur in the Simon Lab at UConn. RachelKrauss studied cicadas in the Simon Lab as part of her BSMS degree at UConn. ChrisSimon, a Professor at UConn, studies molecular systematics and evolution of cicadas worldwide and uses cicadas as model organisms to study the origin, spread, and maintenance of biodiversity.