At the limits: habitat suitability modelling of northern 17-year periodical cicada extinctions

RESEARCHPAPER

At the limits: habitat suitabilitymodelling of northern 17-yearperiodical cicada extinctions(Hemiptera: Magicicada spp.)John R. Cooley1,2,3, David C. Marshall1, Chris Simon1,

Michael L. Neckermann,3 and Gerry Bunker3

1Department of Ecology and Evolutionary

Biology, University of Connecticut, Storrs, CT,

USA, 2Department of Systems Engineering,

Shizuoka University, Hamamatsu, Japan,3Cicada Research Consulting, Storrs, CT, USA

ABSTRACT

Aim Adult periodical cicadas emerge as temporally isolated, synchronized multi-species communities (‘broods’) that are for the most part geographically contigu-ous and that fit together in jigsaw-puzzle-like fashion. Some year-classes of 17-yearcicadas have become extinct within historical times. We investigate two generalcauses for these extinctions – anthropogenic habitat destruction and post-glacialclimate change.

Location Periodical cicadas are confined to the eastern United States, east of theGreat Plains. We document the locations of known periodical cicada extinctions intwo broods of 17-year cicadas in Connecticut, Rhode Island, and upstate New York,USA.

Methods Using additional distributional records of 17-year cicadas, we develophabitat suitability models for all 17-year periodical cicadas, using data layers thatreflect both ecological and anthropogenic factors.

Results Climatological data layers related specifically to annual mean temperatureand temperature during the warmest months make the greatest contributions toour models, and data layers most specifically related to deforestation and habitatfragmentation tend to make much smaller contributions. Two well-documentedextinct populations of periodical cicadas occurred in locations where these modelspredict relatively low habitat suitability for 17-year cicadas.

Main conclusions Our results and other circumstantial evidence discount theimportance of anthropogenic habitat destruction in explaining these particularextinctions.

KeywordsBrood, cicada, change, eastern USA habitat loss, hypsithermal, metapopulation.

*Corresponding: John Cooley, Department ofEcology and Evolutionary Biology, University ofConnecticut, Storrs, CT 06269-3048, USA.E-mail: [email protected]

INTRODUCTION

There has been increasing interest in ecological studies that use

modelling to predict and understand the environmental corre-

lates of species distributions (reviewed in Guisan & Zimmer-

man, 2000; Guisan & Thuiller, 2005; Araújo & Guisan, 2006;

Araújo & New, 2007; Hirzel & Le Lay, 2008; Elith & Leathwick,

2009; Franklin, 2009). These recent reviews have evaluated

methodology, provided insight into the determinants of species

distributions and stimulated debates related to ecological niche

theory, and the effects of climate change on species distribu-

tions. Our study borrows techniques from species distribution

modelling and uses them to investigate habitat suitability for an

unusual group of species locked together in time and space –

17-year periodical cicadas in the genus Magicicada.

Cicadas are hemipteran insects generally known for their loud

diurnal sounds. Only the seven Magicicada species from eastern

North America are documented to be periodical, with locally

synchronized adult emergences. Magicicada are known for long

life cycles of 13 or 17 years and periodic mass emergences of up

to millions per acre, as well as for their dependence on dense

populations (adult densities greater than c. 1 m–2) to prevent

annihilation by predators (Marlatt, 1923; Beamer, 1931; Dybas

& Davis, 1962; Lloyd & Dybas, 1966; Dybas, 1969; Karban,

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Global Ecology and Biogeography, (Global Ecol. Biogeogr.) (2013) 22, 410–421

DOI: 10.1111/geb.12002410 © 2012 Blackwell Publishing Ltd http://wileyonlinelibrary.com/journal/geb

1982a, b; Williams & Simon, 1995; Marshall et al., 2011). The

genus Magicicada is a complex of closely related species belong-

ing to three species groups (-decim, -cassini and -decula),

each with at least two members. Currently, seven species are

described, four with a 13-year life cycle, and three with a 17-year

life cycle, such that each species is more closely related to other

members of its own species group than to others with the same

life cycle (Marshall & Cooley, 2000). Multiple allochronic spe-

ciation events, perhaps in response to climate cues, have been

invoked to explain this unusual situation (Alexander & Moore,

1962; Marshall & Cooley, 2000; Cooley et al., 2001).

Among the more remarkable features of periodical cicada

biology are the ‘broods’, which are regional, often parapatric,

mixed-species year-classes of periodical cicada populations that

are bound to a common emergence timing by their shared strat-

egy of predator satiation. Cicadas in one brood are thus tempo-

rally and spatially isolated from those in other broods. Broods

probably give rise to other broods when life-cycle anomalies

(possibly climate-triggered; Marshall et al., 2003, 2011) cause

large numbers of cicadas to emerge off-schedule (Alexander &

Moore, 1962; Lloyd & Dybas, 1966; Lloyd & White, 1976; Simon

& Lloyd, 1982). In theory, broods that do not maintain high

population densities fail to satiate predators and are eliminated.

Brood declines or extinctions have been a long-running topic of

discussion in the literature on periodical cicadas (Pechumen,

1968, 1984; Maier, 1982; Cooley et al., 2004; Gilbert & Klass,

2006), but well-documented examples of extinction are difficult

to identify against a background of shifting techniques for

keeping records and making maps (Maier, 1985; Marshall, 2001).

In this paper, we consider two potential causes of the decline

of some periodical cicada populations: (1) anthropogenic

habitat fragmentation; and (2) late Holocene climate shifts.

These causes are not mutually exclusive, so we examine them by

developing habitat suitability models based on environmental

variables that reflect climatological, biotic and anthropogenic

factors. Our approach is to represent the known distribution of

periodical cicadas as accurately as possible, to identify possible

environmental correlates of range limits and to observe whether

extinct and declining populations fall outside those environ-

mental tolerances.

MATERIALS AND METHODS

Comparison of recent records with historical records suggests

contraction of the ranges of Broods VI, X, XIII and XIV, espe-

cially along their northern edges (by convention, broods are

designated by Roman numerals). This impression may be due

less to actual range contraction than to the misidentification of

cicada species, the observation of off-schedule ‘straggler’ cicadas

or the tendency for county-based maps to overestimate brood

ranges (Maier, 1985; Marshall, 2001). Unfortunately, many older

records and specimens lack specific locality or collection data,

making it difficult to resolve ambiguities. To avoid such confu-

sion, we applied strict criteria for identifying documented cases

of brood decline and concentrated on two well-documented

cases. Brood VII in upstate New York was once found through-

out the Finger Lakes region but has contracted to a small, albeit

dense, population south of Syracuse (Pechumen, 1968, 1984;

Cooley et al., 2004; Gilbert & Klass, 2006). Brood XI, restricted

to Connecticut, became extinct some time after 1954 (Marlatt,

1923; Dow, 1937; Manter, 1937, 1955, 1974).

We began our study by identifying emergence records for

Broods VII and XI that are supported by field notes (C.S.,

unpublished), specimens or previous publications with clearly

articulated methodologies and mapping criteria (e.g. Pechu-

men, 1968, 1984). We then mapped the most recent scheduled or

expected emergences of Broods VII (2001) and XI (2005) using

GIS technology. Details of the Brood VII map and the method-

ology underlying it are published elsewhere (Cooley et al.,

2004). We searched for Brood XI during its June 2005 emergence

at 74 unique localities in Connecticut and Rhode Island. These

localities were chosen because they had been recorded as having

emergences of Brood XI, they were in proximity to past reported

locations or they were within the same watersheds as past veri-

fiable records (Marlatt, 1923; Dow, 1937; Manter, 1937, 1955,

1974). We also interviewed James Slater (now deceased) of the

University of Connecticut, who along with J. A. Manter made

collections of Brood XI on 10–12 June 1954, and we interviewed

Tom Moore of the University of Michigan, who attempted to

find Brood XI during its expected 1971 emergence. Based on this

information, the last known sighting of Brood XI was in 1954

along the edge of a dairy pasture near the present address of 75

Cowles Road, in the town of Willington, CT, on the east side

of the Fenton River near both the Mansfield and Ashford

town lines (41.86° N, 72.22° W; see Appendix S1 in Supporting

Information).

We collected locality information with handheld GPS units

(Garmin, various models), using the WGS84 map datum. At

each location, we searched for physical evidence of periodical

cicadas (emergence holes, turrets, exuviae or body parts), and

we also listened for singing cicadas. We listened for minimum

5-min periods on warm, sunny, calm days only, in wooded

habitat on dates and under conditions appropriate for chorus-

ing, using methods similar to those in other studies (e.g. Mar-

shall et al., 1996; Cooley et al., 2004; Cooley et al., 2009; Cooley

et al., 2011; Marshall et al., 2011), accepting any direct evidence

of Magicicada as a positive record. Lack of evidence constituted

a negative record. In addition to our verified records, we solic-

ited records from the general public by distributing posters with

photographs of periodical cicadas and offers of a $100 cash

reward in local stores and post offices; we also placed illustrated

flyers in mailboxes near the last known collecting locality. Based

on these results and our examination of historical records, we

compiled a list of 19 localities within Broods VII and XI where

we could be confident that a population had once existed and

was now extinct (Appendix S1).

We tested possible explanations for the disappearance of

periodical cicadas in these locations by constructing habitat

suitability models (HSMs), also called ecological niche models

(ENMs) or species distribution models (SDMs; Guisan & Thu-

iller, 2005). For our occurrence data, we used a dataset that

combined all 17-year cicada species in all 17-year broods. This

Seventeen-year cicada habitat suitability

Global Ecology and Biogeography, 22, 410–421, © 2012 Blackwell Publishing Ltd 411

choice bears some explanation. Although different microhabitat

preferences have been reported for the -decim, -cassini and

-decula species groups (Dybas & Lloyd, 1974) at the c. 1 km2

resolution of our models, all 17-year Magicicada species appear

to have similar general habitat requirements, are treated indis-

criminately by predators and often co-occur (Williams &

Simon, 1995). Furthermore, the species within a life cycle are so

tightly associated that older records often fail to discriminate

among them, and many older records pre-date the last taxo-

nomic revision of the genus (Alexander & Moore, 1962).

Because of these limitations, and because we are interested in

general predictions about where 17-year cicadas can be

expected to live, our analyses group all 17-year species together

and should not be mistaken for models of individual species or

broods. Based on our records, the bounding box for this study

was defined by 49° N, 25° N, -103° W, -67° W, which includes

the 48 contiguous United States east of the approximate line of

20-inch rainfall. No verified historical periodical cicada records

fall outside this area or within 200 km of its edges, although the

edges are near to some unverified (and likely spurious) histori-

cal records.

We used several versions of our dataset to build models. Our

‘full’ 17-year cicada dataset consisted of 11,392 georeferenced,

verified presence records taken during 17-year Magicicada emer-

gences from 1954–2008 and in the Cicada Central database

(http://hydrodictyon.eeb.uconn.edu/projects/cicada/databases/

databases.php). This dataset represents an extensive sampling

effort using methods similar to those described above and

designed to locate the perimeters of various broods. Each pres-

ence record used in this study was obtained or confirmed by

one or more of the authors. The overall range of 17-year cicadas

delineated by our records is similar to the range shown in Mar-

latt’s periodical cicada maps as edited by Simon (Marlatt, 1923;

Simon, 1988). No records of off-cycle or ‘straggler’ cicadas were

included, and all duplicate or geographically coincident records

were removed. The full dataset did include the records of veri-

fied extinct populations. To speed processing, a ‘thinned’ dataset

(Fig. 1) was created by randomly thinning clumped data points

resulting from the use of an automated GPS datalogger in the

most recent field seasons (Cooley et al., 2011). Thinning was

accomplished via construction of a point density contour map

of the ‘full’ dataset; areas that were most clumped on this map

were thinned by a factor of 16. The final thinned dataset con-

sisted of 1737 positive records.

Because some modelling methods make use of both presence

and absence data, we also constructed a ‘known absence’ dataset.

Although the Cicada Central database contains many absence

(‘negative’) records, these records are organized by brood mem-

bership, so they are not necessarily absence records for 17-year

cicadas in general. For instance, many of the absence records for

Brood X (Cooley et al., 2009) fall within the territory of Brood

XIV (Cooley et al., 2011) and vice versa. To select only records

that represent the complete absence of any 17-year Magicicada

brood, we constructed a detailed hull around all positive records

of 17-year cicadas and buffered it to 1 km. We discarded all

absence records falling within the periphery of the 1-km buff-

ered hull, leaving 1388 records in which 17-year Magicicada

were known to be absent. Because these absence records had the

same datalogger biases as the positive records, plus the addi-

tional bias that our absence records were concentrated on areas

in the immediate periphery of our positive records, we thinned

this dataset to 706 observed negative records, using the data

thinning techniques described above. We then constructed a

raster of inferred absences, using a c. 10-km2 grid cell size con-

tained within the bounding box of this study (see above). This

raster was converted to a point shapefile with geocoordinates

placed at the centre of each raster grid. All such points falling

within a 5-km buffered hull of positive data points, or within

Figure 1 Periodical cicada distributionrecords used to create habitat suitabilitymodels. Hatched areas are estimates ofthe placement of Marlatt’s 17-yearMagicicada records (Marlatt, 1923) asrevised by Simon (1988).

J. R. Cooley et al.

Global Ecology and Biogeography, 22, 410–421, © 2012 Blackwell Publishing Ltd412

5 km of an observed absence point, were discarded, leaving 536

inferred absence points uniformly distributed in the study

bounding box and located at least 5 km from any verified pres-

ence or absence record. We used this dataset of 1242 ‘absence’

data points for modelling methods that could make use of both

presence and absence observations.

Our choice of environmental data layers was complicated

by the wealth of data available and the geographic extent of

the study region. We included 19 explicitly climatological data

layers from the WorldClim dataset in our models (Hijmans

et al., 2005) as well as nine additional ecological data layers from

other sources (Appendix S2). These non-climatological layers

reflected broad patterns in forest cover [National Land Cover

database (NCLD) 2001], forest fragment connectivity (NCLD

FrFrg2i1kml_pff), anthropogenic forest fragmentation (NCLD

FrFrg2i1kml_pfa), forest fragmentation (NCLD forfrg1kml),

anthropogenic biomes (NA Anthrome) and human impact

(Human Impact/Last of the Wild). We also included two ecore-

gion datasets that categorize the study region based on land use,

landform, potential natural vegetation, soils and other factors

(Bailey, 1980; Omernik, 1987). All data layers represent current

patterns, not historical conditions or future projections. From

these data layers, we prepared environmental raster datasets in

ArcGIS 9.3, using a c. 1-km2 grid cell size, clipped to the study’s

bounding box to speed processing, reduce file size and reduce

model errors related to an overly large background dataset

(Anderson & Raza, 2010).

A priori choices among the 28 data layers seemed arbitrary,

given the potential interdependence of the datasets and the scar-

city of information about the physiological ecology of periodical

cicadas. For example, since periodical cicadas emerge in the

spring, it might seem tempting to concentrate on variables

related to spring climate; however, it is possible that the cicadas

are most sensitive to summer conditions (when eggs are hatch-

ing) or winter conditions (when the underground nymphs must

avoid freezing). Thus, for our initial models, we used all 28

environmental data layers, and, in effect, we used initial HSMs to

inform variable culling prior to making final models. For our

final models, we selected three high-performing climatic layers

and three high-performing ecological layers. However, these

were not necessarily the six highest-performing layers in our

initial models; rather, our choices were intended to include both

climatological and non-climatological ecological information

and minimize overlap among variables.

We constructed SDMs using several methods, including

random forest, generalized boosting models, classification tree

analysis, multiple adaptive regression splines, generalized addi-

tive models, generalized linear models and artificial neural net-

works, as implemented in the R library BIOMOD (Guisan &

Thuiller, 2005; Moisen et al., 2006; Thuiller et al., 2009). All

methods were optimized according to the receiver operating

characteristic (ROC) criterion, a 50:50 data split for training and

evaluation, and 100 cross-validation runs. Using BIOMOD’s

‘Ensemble.Forecasting’ command, an ensemble forecast of all the

methods, weighted by model score using a default value (1.6),

was made (see Araújo & New, 2007). This ensemble model was

converted into an ArcGIS raster with c. 10-km2 cell size by

kriging.

We also constructed models using the maximum entropy

methods of MaxEnt 3.3.3k (Phillips et al., 2004, 2006; Peterson

et al., 2007; Phillips & Dudík, 2008). MaxEnt models were run

with a default convergence threshold of 10-5 for 1000 replicates,

each time with 25% of the data set chosen randomly without

replacement as training samples, using the ‘Remove Duplicate

Presence Records’ option to reduce the dataset to one observation

per raster cell. For preliminary models, we used the default value

of 10,000 background samples, but for our final model we

increased the value to 50,000. Other MaxEnt options, such as

regularization parameters, were set to default values. The relative

contributions of the different environmental variables were

determined and a jackknife analysis was performed to deter-

mine which variables contained the most unique information.

While the area under the curve (AUC) criterion (Fielding & Bell,

1997) was used to assess model performance, we do not base our

conclusions on comparisons of AUC scores among models.

To judge the support for either anthropogenic or ecological

explanations for periodical cicada extinctions, we considered the

relative importance of various environmental data layers in all of

our models. We also extracted model scores for extant, extinct,

absent and inferred absent locations and determined whether

the extinct populations were located in areas of high or low

predicted suitability.

RESULTS

Searches for Brood VII periodical cicadas are summarized in

Cooley et al. (2004). Despite searching during appropriate times

and conditions, we found no evidence of periodical cicadas

within the reported range of Brood XI (Fig. 2). Although we

were contacted by members of the public who had seen other

insects, and, later in the season, those who had seen cicadas

belonging to the genus Tibicen, no member of the general public

provided any verifiable evidence of periodical cicadas.

All models are well supported (Table 1) and match, with rea-

sonable accuracy, the known range of 17-year cicadas (compare

the hatched area in Fig. 1 with Fig. 3). Although the environ-

mental variables with the greatest predictive power varied

among our analyses, all of the model building methods tended

to place the greatest importance on climatologically oriented

variables related to temperature and precipitation, whereas less

climatologically oriented variables, such as forest fragmentation

and ecoregions, were rarely high scoring. Within BIOMOD, the

method producing the highest scoring model (using the Predic-

tionBestModel) was the random forest (RF) model (Table 1). In

all models, purely climatological variables reflecting tempera-

ture and precipitation made the highest contributions, while the

layers most associated with anthropogenic deforestation (forest

fragmentation classification and land-cover classification) made

only small contributions (Table 1), although the magnitudes of

the variable contributions should be viewed with caution since

the variables are not necessarily independent.



Extinct populations of Broods VII and XI fall in or near areas

where our models predict lower suitability for 17-year cicadas

(Fig. 4). A plot of model values for extant and extinct popula-

tions shows that extinct populations of Broods VII and XI are

low-value outliers in all models (Fig. 5). These differences are

statistically significant; when model scores for extinct and extant

populations are extracted from the thinned-dataset model,

scores for extinct populations are statistically lower for the

MaxEnt model (Mann–Whitney–Wilcoxon test; W = 2405.5, P <0.001) and the summary statistic for the BIOMOD ensemble

models (Mann–Whitney–Wilcoxon test; W = 801, P < 0.001).

Thus, extinct populations of Broods VII and XI fall into areas

where our models predict a lower probability of conditions

appropriate for 17-year Magicicada.

DISCUSSION

In this paper we investigate factors that affect habitat suitability

for 17-year cicadas in the genus Magicicada. It would be inac-

curate for us to use the term ‘species distribution modelling’ to

describe our efforts, because of the quirky biology of periodical

cicadas: Whereas the 17-year cicadas are a group of closely

related and largely co-distributed species that in some respects

function as a single ecological unit, they do not form a mono-

phyletic clade. Even so, these species are locked together in space

and time, and it is the manner in which their shared ecology

binds them together and limits their distribution that we wished

to capture in our models. While the accuracy of HSMs tends to

be greatest for taxa with small geographic ranges, limited eco-

logical tolerance (Hernandez et al., 2006) and data sets of inter-

mediate prevalence (McPherson et al., 2004), we generated

HSMs that accurately represent the distribution of 17-year peri-

odical cicadas, even though their range is large and ecologically

diverse.

Two aspects of our models are relevant to understanding

extinct populations and broods. First, documented extinct

populations of Broods VII and XI were found in areas where our

models predict a comparatively low probability of conditions

appropriate for 17-year cicadas. Second, climatological variables

(e.g. temperature and precipitation) seem to have the greatest

importance in our models, while non-climatological variables

(e.g. land cover and fragmentation) tend to make smaller model

contributions. Taken at face value, these results suggest that

climatological explanations for the increased susceptibility of

periodical cicadas to extinction along the northern edge of their

distribution are more plausible than non-climatological expla-

nations like ‘ecoregions’, anthropogenic fragmentation, forest

connectivity and land-cover classification (see Appendix S2).

The low contribution of the forest fragmentation data layers

to our models was unexpected. To the extent that fragmentation

involves the reduction of existing forests into smaller and

smaller patches, we expect the probability of local extinction to

increase with increasing fragmentation, because periodical

cicadas depend on high community densities of at least tens of

thousands per hectare that decrease per capita predation risk

(Beamer, 1931; Dybas, 1969; Karban, 1982a; Williams & Simon,

1995; Marshall et al., 2011). In addition, forest patchiness has

been found to affect the spatial distributions of periodical

cicadas (Rodenhouse et al., 1997), and Magicicada fecundity

may be lowered in sparse populations (Karban, 1982b). Thus,

scarcity tends to magnify conditions that further depress popu-

lation size leading to demographic time lags that make it diffi-

cult for declining populations to recover. It is possible that the

measures of fragmentation used in our study fail to capture the

importance of fragmentation to periodical cicadas, either

because the resolution of the data layers is too coarse or because

current levels of fragmentation are irrelevant; instead, informa-

tion about fragmentation that occurred in the past might be

Figure 2 Periodical cicada Brood XI2005 search area in Connecticut andRhode Island in 2005. Cross symbolsdenote the absence of periodical cicadas;no positive records of Brood XI werefound in 2005. Black circles are verifiedpositive records of 17-year periodicalcicadas belonging to other broods.Hatched areas are estimates of theplacement of Marlatt’s Brood XI records(Marlatt, 1923) as revised by Simon(1988).

J. R. Cooley et al.


Tab

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264

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more informative. Unfragmented habitat that has regenerated

during the past century following agricultural abandonment

(such as habitat found broadly throughout the north-eastern

states today) may contain few Magicicada populations, as a

legacy of widespread extinction that occurred long ago during

extensive deforestation. Indeed, the last known location of

Brood XI and some of the areas formerly inhabited by VII are

currently forested and classified as intact and interconnected,

while an early 20th century photograph of this area, taken when

the brood was still in existence, shows patchy woodlots and

fencerows (Appendix S3; Favretti, 2003).

One issue raised by our study is why extinction has been well

documented only for Broods VII and XI, when portions of

Broods VIII, X, XIII and XIV occupy similar latitudes. In fact,

similar declines have been reported on the basis of county-level

maps in Indiana (Brood X; Kritsky, 1987) in areas where our

models predict lower suitability for 17-year Magicicada. It is

possible that 17-year populations are in retreat along the entire

northern edge of their range, and the lack of documentation

may be simply an artefact of missing or ambiguous historical

records. Indeed, along the northern periphery of the general

periodical cicada distribution, recent emergences of Broods X,

XIII, XIV and several disjunct populations of various broods on

Long Island (Simon & Lloyd, 1982) have fallen short of their

historically reported ranges (J.R.C., D.C.M. and C.S. unpub

lished data). Reporting biases may also explain the lack of

well-documented declines; for example, the complete extinction

of a peripheral brood such as VII or XI may be far more likely to

be noticed than a local extinction near the centre of a large

brood.

Figure 3 (a), (b). Species distributionmodels based on a thinned 17-yearMagicicada dataset and six variables.White indicates areas where probabilityof conditions appropriate for 17-yearcicadas approaches zero. Shadingindicates areas where conditions have thehighest probability of being appropriatefor 17-year cicadas, with darker shadingindicating higher probabilities. (a)BIOMOD ensemble forecast. (b) Averageof 1000 replicate MaxEnt models.

J. R. Cooley et al.


(a)

Figure 4 (a) Verified extinct populations (crosses) of periodical cicada Broods VII and XI. Dark shading is the MaxEnt model from Fig. 3.White indicates areas where the probability of conditions appropriate for 17-year cicadas approaches zero. Dark shading indicates areaswhere conditions have the highest probability of being appropriate for 17-year cicadas. Hatched areas are estimates of the placement ofMarlatt’s 17-year Magicicada records (Marlatt, 1923) as revised by Simon (1988). (Inset A) Verified extinct populations (crosses) ofperiodical cicada Brood XI in Connecticut and Rhode Island. The background is the MaxEnt habitat suitability model based on thinned17-year periodical cicada dataset from Fig. 3. Hatched areas are estimates of the placement of Marlatt’s 17-year Magicicada records (Marlatt,1923) as revised by Simon (1988). (Inset B) Verified extinct populations (crosses) of 17-year periodical cicada Brood VII in New York. Thebackground is the MaxEnt habitat suitability model based on thinned 17-year periodical cicada dataset from Fig. 3. Black circles are verifiedpositive records of 17-year periodical cicadas belonging to other broods. Hatched areas are estimates of the placement of Marlatt’s 17-yearMagicicada records (Marlatt, 1923) as revised by Simon (1988).

(b)

Figure 4 (b) An enlargement of Inset A.



Another question raised by our models is how the now-extinct

periodical cicada communities became established in the first

place, if indeed the locations of these populations are of low

suitability for 17-year periodical cicadas. It is possible that

improved sampling of periodical cicadas in areas where our

sampling is weak (parts of Indiana, Ohio, New Jersey and Con-

necticut) would have changed habitat suitability estimates for the

extinct populations, though it seems doubtful that improved

sampling would significantly decrease the importance of the

climatological variables. It is also an intriguing possibility that

northern marginal populations of periodical cicadas are relicts

left behind by prior range extension during the drier, warmer

conditions of the Hypsithermal Interval (c. 9000–5000 bp). If

17-year periodical cicadas expanded their range northward

(c)

Figure 4 (c) An enlargement of Inset B.

Figure 5 Scatterplot of habitat suitability model scores for locations of positive records in thinned 17-year Magicicada dataset (blackcircles), verified extinct populations (black crosses), verified absence records (open triangles) and inferred absences (open diamonds). Thehorizontal axis is the score from the MaxEnt average model; the vertical axis is the score from the BIOMOD ensemble forecast.

J. R. Cooley et al.


during these milder conditions, then, as conditions cooled,

northern limital populations could become vulnerable to extinc-

tion as the range of 17-year cicadas returned to a state of climatic

equilibrium and populations became isolated or dwindled below

levels required for predator satiation (see Araújo & Pearson,

2005). If this hypothesis is correct, then local population extinc-

tions should have occurred more often along the northern

Magicicada range limit than along the southern margin, which is

defined by 13-year cicada populations. Now that climatic condi-

tions are warming again, one might predict an expansion, but

climatic extremes (e.g. early warmth followed by late cold shocks)

associated with recent warming may have more of an effect than

the average warming trend (Parmesean, 2006; Knapp et al.,

2008).

An unusual quality of periodical cicadas is that multiple sym-

patric, synchronized species usually emerge together.

While different Magicicada species have somewhat different

habitat preferences (Dybas & Lloyd, 1962, 1974), predators

appear to treat the different periodical cicada species inter-

changeably. In a mosaic of upland forests (preferred by Magici-

cada species in the -decim complex) and lowland drainages

(preferred by Magicicada species in the -cassini complex), one or

more rare species may avoid predator annihilation due to the

local presence of a dense congener (Lloyd & White, 1983). In this

way, two synchronized species may survive predator pressure

where one alone would not. If so, then northern periodical cicada

communities (e.g. Massachusetts, Connecticut, upstate New

York, Michigan and central Wisconsin) may be especially suscep-

tible to extinction, since they typically contain only a single

species – Magicicada septendecim. Future studies could test this

hypothesis more carefully by specifically comparing extinction

rates observed along the northern edge of the 17-year range,

where only M. septendecim is present, and in the south-western

sector, where only Magicicada cassini is present, to regionally

adjacent locations where populations contain multiple species.

The peculiar biology of periodical cicadas means that migra-

tion among spatially-and temporally separated patches should

also be considered. Although the historical treatment of peri-

odical cicada broods is that they are evolutionary units, it may be

more appropriate to consider them as metapopulations, in

which local population patches are interdependent and bound

to a common emergence schedule by predation pressure. Local

patches of the same brood may exchange migrants, and in those

places where broods are adjacent, temporal migration among

patches may occur when cicadas emerge off-cycle (‘stragglers’).

Such spatial and temporal exchanges may be a key factor in

reducing the probability that predators can find and eliminate

all patches of periodical cicadas in a given region. This may be

particularly important where Broods XIV, X, VI and II overlap

(Lloyd & White, 1976; Simon & Lloyd, 1982; Heliövaara et al.,

1994). However, northern populations of 17-year cicadas appear

to be the ones for which replenishment from neighbouring

populations seems least likely, because northern broods and

populations tend to be isolated from all others.

Why are some northern 17-year periodical cicada populations

going extinct? Although their extensive range and broad toler-

ances would seem to make these insects unlikely candidates for a

successful modelling approach, our models do seem to capture

the essentials of the 17-year cicada distribution. Surprisingly,

these models discount the importance of factors such as present-

day deforestation or forest fragmentation in documented Magici-

cada extinctions.Yet as compelling as they seem, these models are

missing something important: They are entirely lacking the kinds

of ecological interactions, such as predator satiation, known to be

important for these species. An extinction that appears to be

imminent underscores this point. Raccoon Grove Forest Pre-

serve, located 36 miles south of Chicago in Will County, IL, is

found within periodical cicada Brood XIII and in an area where

our models predict suitable conditions for periodical cicadas. In

this location in 1956, Dybas & Davis (1962) measured the highest

Magicicada population density estimate ever recorded for a

natural population, over 1.5 million adults per acre for M. cassini.

Yet during the 2007 emergence of Brood XIII, only a handful of

cicadas were reported from the site (L. Yang, University of Cali-

fornia, Davis, CA, USA, unpublished data). While development

appears to have encroached on the forests surrounding Raccoon

Grove, the preserve boundaries have not changed since 1956, and

the overall forest block remains substantial (around 1 km2,

judging from aerial photographs). Although additional factors

may be involved, including a bout of Dutch elm disease that killed

many trees on the floodplain woods after the 1956 emergence

(White & Lloyd, 1975), the increasing isolation of Raccoon Grove

suggests a role for the kinds of species interactions and metap-

opulation dynamics discussed above. The likely extinction at

Raccoon Grove suggests two cautions about HSMs: first, the

accuracy of such models and the validity of conclusions drawn

from them may vary over the range of the model, especially for

widespread species; second, until we find a way to incorporate

species interactions into them, such models will involve signifi-

cant oversimplifications.

ACKNOWLEDGEMENTS

This paper is dedicated to the memory of the late Charles Rem-

ington, of Yale University, who introduced the first author to

periodical cicadas and their vulnerability to extinction. The

National Geographic CRE-sponsored project ‘Making modern

maps of Magicicada emergences’ provided partial funding for

this project. Kathy Hill assisted in collecting records. Cory Merow

and anonymous referees provided valuable comments on earlier

drafts. The UConn Bioinformatics Facility provided computing

resources for this study. This material is based upon work par-

tially supported by the National Science Foundation under grant

nos NSF DEB 04–22386, DEB 05–29679 to Chris Simon. 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 National Science Foundation.

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SUPPORTING INFORMATION

Additional supporting information may be found in the online

version of this article at the publisher’s web-site.

Appendix S1. Verified, extinct populations of periodical cicada

Broods VII and XI.

Appendix S2. Environmental layers used to construct habitat

suitability models for 17-year periodical cicadas.

Appendix S3. Fenton River Valley, looking east towards Willing-

ton, CT along the Boston Turnpike.

BIOSKETCH

John R. Cooley, researcher at the University of

Connecticut, studies the behaviour and evolution of

cicadas. Current information about the cicada mapping

project may be found at http://www.magicicada.org.

Editor: Antoine Guisan



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At the limits: habitat suitability modelling of northern 17-year periodical cicada extinctions