Seventeen-year (periodical) cicadas, appearing rarely, regularly, and in great numbers in the U.S., even in residential areas, offer an opportunity for anyone to study varied aspects of abundant, available life. Generally, when one approaches wild animals in their environment, they run, fly, swim, slither, or scamper away to hide. And with many animals in nature it may be difficult to get a large sample size for statistical study. Yet these cicadas, easily found and examined once they emerge, generally do not flee. They seemingly offer themselves in cooperation with one’s interest to reach out, count, observe, photograph, study life. They are harmless. And like L’l’ Abner’s Shmoos, one might even eat them (many natural predators do).
They have perhaps the most long-lived of any insect's nymph stage. They are unique, earning that adjective: in no place of the world outside the U.S. do 17-year or 13-year cicadas exist. They are underground for years without people's awareness. And at a time of well-documented biological loss, and worldwide extinction, their super-abundance may appear to many of us to be oddly, uniquely, reassuring. They can bring out in us a childlike curiosity.
What is also special about them is their scarcity most times and places, that they appear rarely, so we could not tire of them in our lifetime. And, because of their periodicity and spectacular numbers, we can remember them along with particular epochs of our own lives, from childhood to old age.
One springtime when they appeared, I found myself walking along on the sidewalk each morning counting them, and in the process of maintaining records, stumbled upon a phenomenon of animal behavior I didn't know existed. . . .
In this whimsical illustration by Feodor Rojankovsky, from John Langstaff's classic version of the folk lyrics, "Frog Went A-Courtin'," two maiden ants hurry to a wedding.
Periodical cicadas, Magicicada septendecim, spring 2004, arriving in the neighborhood.
Writers often wish they could add information or realizations to their published text. This website allows me to make such improvements. Below is my peer-reviewed publication from The Maryland Entomologist -- with added details in the Abstract and the 4th and 5th paragraphs of Methods, and inclusion of Figure 9 to the Results.
September 2020 The Maryland Entomologist 7(4):17–30
Protandrous Arrival in a Population of the Periodical Cicada Magicicada septendecim (Linnaeus) (Hemiptera: Cicadidae) in Montgomery County, Maryland
Caleb M. Kriesberg
ABSTRACT: Differences in number and arrival time of male and female adult periodical cicadas, Magicicada septendecim (Linnaeus), Brood X, in a small geographic area of Maryland in 2004, are described and discussed. Newly emergent cicadas were counted, by sex, along various suburban streets. A probable incidence of protandry—the emergence of adult males before adult females—was observed. Data analyses by test of proportions show that for some of the first days of counting, in one of the two sample sites and in both sites combined, the disproportionate appearance of adult males was statistically significant, while for the last few days, the disproportionate appearance of adult females was also statistically significant. In one of the two sites and in both sites combined, significantly more females than males for the season as a whole were also observed. Regression analysis of daily male/female ratios for both sites combined supports a protandrous emergence pattern for the season as a whole. Though this study appears to confirm previous findings, there is little discussion in the literature on protandry in periodical cicadas, and no other study on this subject and species with detailed methodology for daily sampling, particularly in an urban or suburban setting. It might be useful to conduct field counts of periodical cicadas in a variety of locations to discover where such protandry may or may not occur. It is believed that this mode of protandry is adaptive for the species, and that it evolved to enhance survivability or reproductive opportunity for both sexes.
INTRODUCTION
Once every 17 springtimes in certain parts of the United States, periodical cicadas (Hemiptera: Cicadidae) emerge in massive numbers (Figure 1). The various populations are called broods, numbered according to their cycles. Brood X of the three 17-year species appears in Mid-Atlantic states and in some proximate areas west. Magicicada septendecim (Linnaeus) is the predominant Brood X species in the study area (Simon 1996).
Figure 1. Magicicada septendecim: mass emergence of nymphs from the ground. (Maryland, Michael J. Raupp, 15 May 2004)
While in the nymph stage (Figure 1), the cicadas emerge from holes in the ground; then, about 30 minutes to an hour later, they metamorphose into adults. After separating from the nymphal skin, they are almost completely white for about 40 minutes. They darken to black gradually, but their bodies remain relatively soft for about four days the “teneral” period (Figure 2), during which time the males cannot sing, the females cannot lay eggs, and neither acquires its full adeptness at flying (Cooley and Marshall 2001).
Figure 2. Magicicada septendecim: newly eclosed teneral. (Maryland, Michael J. Raupp, 16 May 2004.)
During the first week of emergence, their large numbers and poor escape behavior make them desirable prey (Williams and Simon 1995). But after an initial time-span, predators may become satiated from eating the cicadas, and net predation declines (Karban 1981, Williams and Simon 1995).
The females can readily be distinguished from the males by the ovipositor. The males eventually chorus loudly in trees (Figures 3 and 4). Studies have indicated that males can mate more than once, but females typically only once (Williams and Simon 1995, Cooley and Marshall 2001, Saisho 2010).
Figure 3. Magicicada septendecim: male, ventral view of abdomen. (Note: this specimen is a four-year early emergent of the 2021 Brood X; Maryland, Michael J. Raupp, 24 May 2017.)
Figure 4. Magicicada septendecim: female, ventral view of abdomen showing ovipositor. (Note: this specimen is a four-year early emergent of the 2021 Brood X; Maryland, Michael J. Raupp, 29 May 2017.)
“Protandry is the emergence or arrival of males before females into a seasonal population and is widespread among both plants and animals” (Holzapfel and Bradshaw 2002; see also Morbey and Ydenberg 2008). Note that in biological science, another, very different meaning of protandry is “sequential hermaphroditism,” in which males become females, i.e., “the individual changes sex at some point of the life history. If the initial sex is male, the condition is known as protandry” (Warner 1975). This latter meaning of protandry is not the subject of this study.
In 1958, Tinbergen (1969) reported this phenomenon of differential arrival of males and females for the Snow Bunting, Plectrophenax nivalis (Linnaeus) (Passeriformes: Calcariidae). Protandry has been analyzed by researchers studying the European Pied Flycatcher, Ficedula hypoleuca (Pallas) (Passeriformes: Muscicapidae) (Canal et al. 2012). Entomological examples have been reported for a butterfly, Black Swallowtail, Papilio polyxenes Fabricius (Lepidoptera: Papilionidae) (Lederhouse et al. 1982); for the Pitcherplant Mosquito, Wyeomyia smithii (Coquillett) (Diptera: Culicidae) (Holzapfel and Bradshaw 2002); for a grasshopper, Sphenarium purpurascens Charpentier (Orthoptera: Pyrgomorphidae) (Cueva del Castillo and Núñez-Farfán 2003); and for a parasitic wasp, Trichogramma evanescens Westwood (Hymenoptera: Trichogrammatidae) (Doyon and Boivin 2006). This writer may also have observed protandry in the Fowler’s Toad, Anaxyrus fowleri (Hinckley) (Anura: Bufonidae), in Chevy Chase, Maryland, about 3 km (1.9 mi) due west of this cicada study area; over successive years, on the first evening of spring emergence, the toads were observed converging on a pond, with a statistically significant preponderance of males, in an apparently random sample count, showing a male to female ratio of approximately 5:1.
A report by Charles V. Riley (1869), the 19th century naturalist and later employee of the United States Department of Agriculture, describes the 1868 17-year periodical cicada’s habits, mainly in Missouri and Maryland. Riley’s study supplies us an early reference to protandry in Magicicada. It observes, “As is the case with a great many other insects, the males make their appearance several days before the females, and also disappear sooner.”
The observation of protandry has been mentioned in more recent studies outside of Maryland for several cicada genera and species, for example, Magicicada septendecim, M. cassinii (Fisher), and M. septendecula Alexander and Moore (Dybas and Lloyd 1974, Whiles et al. 2001); the Chorus Cicada, Amphipsalta zelandica (Boisduval) (Logan et al. 2014); Meimuna mongolica (Distant) (Hou et al. 2015); and the Giant Cicada, Quesada gigas (Olivier) (de Carvalho Andrade et al. 2017).
Studying Brood X M. septendecim in a Western Maryland apple orchard in 1953, Graham and Cochran (1954) apparently observed protandry, “During the first week of emergence there were more males than females.” The Graham and Cochran study, which includes data on sex ratios, was based on a site located approximately 64 km (40 mi) northwest from this study’s area. Protandry in Maryland for M. septendecim was also suggested by Michael J. Raupp (in litt., 19 May 2004).
This paper, after outlining methodology, describes protandry as observed in the study location, and discusses the survival and reproductive value of the phenomenon for male and female cicadas.
METHODS AND STUDY SITES
Newly metamorphosed adult cicadas, tenerals, were counted near and on streets and sidewalks of three suburban blocks, in an approximately seven square block area, subsequently divided into two study sites, in Silver Spring, Maryland (Figure 5). The count for this statistical study was taken from approximately 0800 to 1000 hours daily, from 14 May 2004—four days after their first appearance—until 23 May 2004. On the last day of the count, the number of newly metamorphosed adults had been declining for six days and a total of only five were found in the second sample site. During the study, the researcher walked the same route once each morning. Whenever a soft white or near-white adult cicada was found, its sex was recorded. (Generally, it should be methodologically possible to augment the data sample by counting the tenerals late at night, as well. But in the residential area of the study, walking the route nightly in the darkness with a flashlight might well prompt concerns from the residents.)
Figure 5. The two locations where periodical cicadas, Magicicada septendecim Brood X, were counted in Silver Spring, Maryland, May–June 2004.
It was assumed this method would produce a random count because at any moment of this brief adult cicada emergence period, neither sex would have a higher mortality rate than the other (John R. Cooley, in litt., 12 September 2005). Statistical analyses were conducted comparing the proportion of male and female newly eclosed adult cicadas found for each day, in each site, and for the season as a whole, using the hypothesis test of a single proportion (McClave and Sincich 2000). The changing daily proportions were also portrayed with regression analysis (Frost 2020).
It was important to count only teneral cicadas, because once the cicadas begin to fly, the sexes may selectively disperse to different heights, and the females are easier to find and count than the males, i.e., males gather in trees to chorus (Lloyd and Karban 1983).
In the early study providing numbers for protandry (Graham and Cochran 1954), for some days in succession, the researchers counted emergent cicadas by placing a wire cage beneath an orchard tree, and tallying the numbers of males and females that appeared in the cages; they checked the cicadas that had emerged every five days, instead of each day. This counting of cicadas emerging around trees within a cage appears to be a valuable method for collecting data on cicadas in rural settings.
In a more recent study, Dybas and Lloyd (1974) thoroughly compare and report habitat preference among the three species of Magicicada by counting nymphal skins and dead adults, and quantify in field notes the preponderance of male nymphal skins on the first days of records. Though it is possible to identify the sex of the cicada by examination of the nymphal skin, one must be careful to be sure what day that cicada emerged, and to correctly identify the species. Their study examined M. septendecim nymphal skins for several days in rural Ohio, reporting a protandrous ratio of male and female emergent cicadas.
In this suburban study area, though personal observation indicated that the predominant Brood X species was M. septendecim, some adults of M. cassinii were found in very small numbers, and their calls heard, near the study sites.
RESULTS
According to the hypothesis tests of single proportions, the number of newly emerged adult male cicadas found for both sites combined was significantly greater than the number of females at α = 0.05 on the first and third day of counting, which is evidence of protandry. The number of newly emerged adult female cicadas found was significantly greater than the number of males at α = 0.01 for the ninth and tenth days of counting (Figure 6).
When separating out the two sites to replicate the experiment, we see evidence for protandry at Site 2, but not at Site 1. At Site 1, there were significantly more females than males at α = 0.05 on the sixth and seventh day—but no statistically significant number of males at the start of the season, hence no protandry there (Figure 7). But at Site 2, there were significantly more males than females at α = 0.05 on the first and third day—evidence for protandry (Figure 8). If we group days 1 through 3 at Site 2, at approximately α = 0.01, we again see there was a significantly greater number of males than females at the start of the season.
Even without statistical analysis, the differential seemed apparent in one instance, though not at a day or site that was statistically significant. On 16 May 2004, the fifth day from first counting, one fence had clinging to it 15 metamorphosing males and only one female. Three days later, the same fence was covered with new adult females and no males.
Figure 6: Total Number of male and female newly metamorphosed adult periodical cicadas, Magicicada septendecim Brood X, found on successive mornings on 14–23 May 2004 in a fixed route of random sampling of a neighborhood of Silver Spring, Maryland. A total of 548 newly metamorphosed males and 700 newly metamorphosed females were found. According to hypothesis tests of single proportions, the number of males is significantly greater than the number of females at α 0.05 for days 1 and 3, and the number of females is significantly greater than the number of males at α 0.01 for days 9 and 10. On days 1 and 3, this result is evidence for protandry. At α 0.01, there are also significantly more females than males for the season as a whole.
Figure 7: At Site 1, number of male and female newly metamorphosed adult periodical cicadas, Magicicada septendecim Brood X, found on successive mornings on 14–23 May 2004 in a fixed route of random sampling in Silver Spring, Maryland. A total of 444 newly metamorphosed males and 585 newly metamorphosed females were found. According to hypothesis tests of single proportions, the number of females is significantly greater than the number of males at α 0.05 for days 6, 7, and 9.
Figure 8: At site 2, number of male and female newly metamorphosed adult periodical cicadas, Magicicada septendecim Brood X, found on successive mornings on 14–23 May 2004 in a fixed route of random sampling, in Silver Spring, Maryland. A total of 104 newly metamorphosed males and 115 newly metamorphosed females were found. According to hypothesis tests of single proportions, the number of males is significantly greater than the number of females at α 0.05 for days 1 and 3 and at approximately α 0.01 for days 1–3. This result is evidence for protandry.
Basic regression analysis can give us a look at the whole season’s protandrous arrival at Sites 1 and 2 combined (Figure 9). Typically for the emergence, there is the maximum preponderance of males at the start, a 1:1 ratio in the middle, and the maximum preponderance of females toward the end. An R square score that is close to value of one generally means that a straight line can readily be drawn through the data array, and the data fit the hypothesized relationships (Frost 2020).
Figure 9. Male:Female ratios of emergent adult Brood X Magicicada septendecim cicadas found on successive mornings, plotted by day, reported with regression analysis.
There was another observation on adult sex ratios. Over the entire season, at Site 1 and at both sites combined, at α = 0.01, there were also significantly more newly emergent females than males found. This observation is consistent with the finding of significantly more female than male M. septendecim cicadas by other researchers: Graham and Cochran (1954) in Maryland, and Jacobs (1953) in Indiana. Hunter and Lund (1960) in Georgia found significantly more female M. cassinii but not significantly more female M. septendecim. But in the other studies, unlike in this study, the question arises whether the researchers were counting only newly emergent cicadas. Other researchers reported male:female cicada ratios of 1:1 for the season (Williams and Simon 1995). Simon (1996) suggested that “temporary biases may occur” in the sex ratios in some areas.
The newly emergent cicadas were found in greatest density under red maple, Acer rubrum L. (Aceraceae); black oak, Quercus velutina Lam. (Fagaceae); and scarlet oak, Q. coccinea Münchh. Proximate to high numbers of cicadas were also flowering dogwood, Cornus florida L. (Cornaceae); black cherry, Prunus serotina Ehrh. (Rosaceae); and
black locust, Robinia pseudoacacia L. (Fabaceae). The physical environment had remained fairly stable during the previous 17 years, though, across the street from one part of the study site, two large trees were cut down about 10 days prior to cicada emergence, not preventing the nymphs beneath from emerging.
Observed in the general area during the study, the principle agents of cicada mortality were cars and pedestrians; House Finches, Haemorhous mexicanus (P. L. Statius Müller) (Passeriformes: Fringillidae), and Northern Mockingbirds, Mimus polyglottos (Linnaeus) (Passeriformes: Mimidae); Eastern Gray Squirrels, Sciurus carolinensis Gmelin (Rodentia: Sciuridae); domestic cats, Felis catus Linnaeus (Carnivora: Felidae); domestic dogs, Canis lupus familiaris Linnaeus (Carnivora: Canidae); fungi; arrested metamorphosis; wasps (Hymenoptera); and spiders (Araneae).
DISCUSSION
Reporting of protandry has tended to focus on benefits to either males or females, and theoretical arguments have become increasingly mathematical. The principle endures that natural selection acts on individuals, but it produces changes in populations.
Protandry is most often described from the male’s point of view. “Early emerging males risk death before mating and late-emerging males miss opportunities to mate” (Holzapfel and Bradshaw 2002). Since female periodical cicadas typically mate only once, male cicadas would need to emerge early enough to find available females, mate with the first females that appear, and mate with as many as possible. Among the males there develops “an intense scramble competition for mates” (Cooley and Marshall 2004). Early arrival is especially advantageous if there are enough other males present to reduce the probability of any one male being preyed upon. “For any given male, the optimal emergence time may depend on the mean and distribution of emergence of other males” (Holzapfel and Bradshaw 2002). A strategy of emerging in large numbers is “selectively advantageous to individual cicadas” (Williams and Simon 1995). Natural selection would favor males that arrive early, if they were in large numbers, because they would have more mating opportunities.
But factors could act on female cicada timing of emergence, as well. According to Cueva del Castillo and Núñez-Farfán (2003), “the possible advantage of the time of emergence for females in their mating success in protandrous insect species” might be studied. Females would have increased chance of mating success “if female maturation occurs when the population…is biased to males.” Protandry could be viewed not just as males arriving early but as females arriving late. Predator satiation after male emergence also could give a survival advantage to females emerging late. These rationales are listed by Morbey and Ydenberg (2008) in their review of overlapping hypotheses explaining protandry: there could be a selection for males to arrive early for multiple mating opportunities and simultaneously a selection for females to arrive late because of the mating benefits of finding many males and also the survival benefits of waiting and avoiding predation. Those late-arriving female cicadas need not wait to hear singing for a day or even a few hours compared to earlier-arriving females.
Researchers have sought to discover, through testing hypotheses in the field and laboratory, which possible evolutionary explanation for protandry might best be represented by which species (Doyon and Boivin 2006, Canal et al. 2012). Morbey and Ydenberg (2008) conclude, what seems to be a current consensus about insects and other arthropods, that “the most important contributing factor selecting for protandry seems to be the maximization of mating opportunities with females, especially virgin females.”
Saisho (2010) adds a somewhat different analysis of female cicadas and protandry. Pointing out that female cicadas in the nymph and teneral stage may have oocytes not yet developed, Saisho reasons that the eclosion, or emergence, of the female cicada might be relatively delayed if the cicada is not yet ready to mate. “It is often said that it takes times to grow eggs in the females’ abdomens, which causes the shift of the eclosion period.” Saisho also recalls that male cicadas can mate more than once while females mate only once, and includes this feature in mathematical modeling. From mathematical modeling, Saisho infers, as have other investigators, that it is apparently to the cicada’s reproductive advantage for females to delay arrival and mating relative to males. Saisho’s consideration of developing oocytes can also correspond theoretically to one of the Morbey and Ydenberg (2008) hypotheses for protandry; they hypothesize that an “indirect” cause of protandry through “constraint” on one of the sexes could correlate with or lead to the differential arrival time.
It might be interesting to inquire whether protandry in M. septendecim is typical, or repeats in a geographic area from one generation to the next, and, if not, to consider why protandry is not found among certain populations of periodical cicadas. Certainly, protandry may not always occur in M. septendecim. Alexander and Moore (1962) recall a site in Ohio in 1959 where almost all the season’s cicadas emerged in a few hours on a single night.
It might also be rewarding to investigate whether the finding of more female than male periodical cicadas at a site for the season as a whole might coincide with the finding of protandry—this correlation was not found consistent in this study. Frank (1983) cautions that there are many possibly conflicting factors that influence overall sex ratios (see also Wade et al. 2003).
Additional study sites might provide a more fine-grained picture to substantiate the possible absence of protandry in the periodical cicada for some areas. Scientific investigators and all those curious about nature are invited to observe the return of the 17-year Brood X cicadas, emerging in some locales next year. Comparing different study sites and regions and implementing a protocol similar to the one used in this study, researchers could collect data on sex ratios, and specifically protandry for further study.
ACKNOWLEDGMENTS
The author wishes to thank John R. Cooley (Assistant Professor in Residence, Department of Ecology and Evolutionary Biology, University of Connecticut, Hartford, CT) who commented on an early draft of this manuscript; Michael J. Raupp (Professor Emeritus, Department of Entomology, University of Maryland, College Park, MD) for information on natural history and for allowing the use of his M. septendecim Brood X photos; Eugene J. Scarpulla (Editor, The Maryland Entomologist) for assistance with research; Chris Simon (Professor, Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs, CT) for reviewing this manuscript and providing her helpful information on natural history, as well as the history of natural history; and an anonymous reviewer for providing constructive feedback. The author also acknowledges with gratitude the late Wade H. Pugh, III (Adjunct Professor, Mathematics, Statistics, and Data Science, Montgomery College, Rockville, MD) for his review of data analysis.
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DATA APPENDIX
Both Sites Combined
Day 1 P̂ = 43/67 = 0.642 Proportion of males > 50%
Z = 2.32 p value 0.0203 Significant at 0.05
Day 3 P̂ = 68/111 = 0.613 Proportion of males > 50%
Z = 2.77 p value 0.0176 Significant at 0.05
Day 9 P̂ = 16/80 = 0.200 Proportion of males < 50%
Z = -5.37 p value 8 x 10-8 ≈ 0 Significant at 0.01
Day 10 P̂ = 6/44 = 0.136 Proportion of males < 50%
Z = -4.82 p value 1.4 x 10-6 ≈ 0 Significant at 0.01
Overall P̂ = 544/1228 = 0.443 Proportion of males < 50%
Z = -4.00 p value 0.0007 Significant at 0.01
Site 1
Day 6 P̂ = 67/165 = 0.406 Proportion of males < 50%
Z = -2.41 p value 0.0158 Significant at 0.05
Day 7 P̂ = 78/185 = 0.421 Proportion of males < 50%
Z = -2.31 p value 0.0330 Significant at 0.05
Day 9 P̂ = 16/77 = 0.208 Proportion of males < 50%
Z = -5.16 p value 8 x 10-8 ≈ 0 Significant at 0.01
Overall P̂ = 444/1029 = 0.431 Proportion of males < 50%
Z = -4.40 p value 0.00001 Significant at 0.01
Site 2
Day 1 P̂ = 24/36 = 0.667 Proportion of males > 50%
Z = 2.00 p value 0.0455 Significant at 0.05
Day 3 P̂ = 24/32 = 0.750 Proportion of males > 50%
Z = 2.83 p value 0.0047 Significant at 0.01
Days 1–3 P̂ = 56/81 = 0.690 Proportion of males > 50%
Z = 3.44 p value 0.0006 Significant at 0.01
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