Role of periodical cicadas (Homoptera: Cicadidae: Magicicada) in forest nutrient cycles

Forc~st Ecology

Elsevier

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S 1 ( 1992 ) 339-346 B.V.. Amsterdam

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tSBSTRACT Wheeler. G.L.. Williams, K.S. and Smith. K.G., 1992. Role ofperiodical cicadas in forest nutrient cycles. For. &al. Mitnage.. 51: 339-346. idae: .liagictcadu)

(Homoptera:

Cicad-

The relative contribution of an emergence of I3-year periodical cicadas to forest nutrient cycles was investigated in an upland forest in northwes?ern Arkansas during a mass emergence of Brood XIX in 1985. Nymphs were collected from below grourtd at two sites prior to emergence and adults of both sexes were collected at one site as they emerged from the ground and after emergence at a chorus center. Nymphs had higher levels of iron, aluminum, and manganese and lower levels of sodium and nitrogen than adults. Adult females had higher levels of potassium and phosphorus than adult males. Compared with annual litter fail, cicadas in the relatively low-density population studied represented less than 1% of any nutrient flux sampled in the litter fall. The most important ecosystem function of the ctcadas in the forest of this study may be the increase in energy and nutrients available to predators.

JNTRODUCTION

Functional roles ofinsects within forest nutrient cycles are not well defined, but are generally considered to be regulatory (Mattson and Addy, 1975: Q’Neill, 1976; Schowalter, 198 1 1. In general, herbivorous forest insects decrease the resident time of nutrients in a given compartment, e.g. by breakdown of accumulated litter (Reichle et al., 1969; Seastedt and Crossley, 1980)) by return of canopy nutrients to the ground by defoliators through frass (Swank et al., 198 1 ), or by early leaf dehiscence caused by leaf miners (Stiling, 1988 $. In outbreak csnditions, herbivorous insects may have a desiabilizing effect oni the system itself (Mattson and Addy, L975 ), even though their io. G.E. Wheeler, Deparrinent AR 72701, USA. address. San Diego State University,

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l‘uncrional role in decreasing the residence time of nutrients in the standing hiorrasx sUnains the same. The infjucnce ufherbrvarous insects is usually ~~spro~o~~ior~a~lygr 3Icr than their coliective biomass (G’NrilI, 1976 ), and insects themselves do cot maliT important contributions to nutrient pools or fluxes (Schowalter and ‘i:rsssl:y, 1981). However, the periodical cicada (Homeptera: Cicadidae: 111f$~icad~) could be an exception to that generalization. They are relatively :ari.e ;nsecrs (about l QO-700 mg dry wt.), with females about twice as heavy as males ( Brown and Chippendale, 1972 ). According to Dybas and Davis ( I962 jq under favorable conditions periodical cicadas are among the most prodL!ctive herbivores with annual biomass accumulation of I OO--200kg hl;- ’ Three species of periodical cicada (Mugicicndu ussini, Mckgicicnh tkcim, and hlcq$cicada &c&z) arc distributed throughout the eastern dc~~d~:sus forest, and all three species may occur together. Each species has a ?3-year r&e that occurs in the southern range, and a 17”year race in the north ( MarIatt, 19V7; Martin and Simon, 1990). MarPatt ( 1907 ) believed that thete were a total of 30 broods, but more recent work indicaks on!y three acti .e kdods ~fblle 1Y-year race and 12 ofthe 17-year race (Arciiie :t al., 1985; Mark and Simon, 1990). The nymphs occur below ground and feed m root xylem fluids of many plant species (White and Strehl, 1978; Lloyd and White, 1987). White and Strehl ( i978) contribute the cicada’s slow rate of development to ti3e low nutritional value of xylem fluids. They also point out, that by being xylem feeders the cicadas are able to avoid plants’ defenses against herbivores. White and Lloyd ( 1385) found that cicada feeding on fertilized trees, and presumably more nutritious fluids, were larger at crnergence, but the time to emergence was not changed. The insects emerge in late spring or early summer and spend a brief, raucous period as adults. Within 4-6 weeks after emcq+ice, a brood will have disappeared (Marlatt, 1907; Brown and Cbippendal~.:, I 972: Wallis et al., 1990). Males form dense chorus centers which females visit to mate. Population densities vary widely with reported values ranging from about IO n--’ to 370 m-’ (Strandine, 1940; Dybas and Davis, 1962). At the higher population densities, the cicadas themselves may be an important nutrient flus. While it has been shawn that adult cicadas are high in proteins (Brown and ~~i~~c~~da~~, 1972 11and that they are an important food source for birds (SiCKkdirK, 8940; Maraier, 1982; Stewart et al.. 1988; Ke?lner et al., 1990), little is known of their mineral content and consequently their importance as a nutrient flux in forest cycles. Thus, CM i~rposes were to estimate the nutrient content of a popuMion of periodi:,rl cicadas, to compare the flux of nhents from insects with that of forest. litter fall, and to determine if differ~nces exist in nlutricnt content between sexes and life stages within %he ~~~~~at~o~.

ROI LICIT I’ERIC)L)IC‘,\l.

C’I(‘ADAS

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M.4TEKIALrANDMETHODS

Study aLeas were located 15 km east of Fayetteville, Warhington Co., Arkansas in the White River valley. A 16 ha primary site was divided into a grid consisting of five rows of 20, 40 mx40 m sub-plots. The forest was dominated by eastern red cedar (JZU~@WZG virginiana ), which comprised 5 1% of’ the average basal area, followed by post oak (f&emu stellata) (23%) and shagbark hickory (Carya ovata) ( 18%). Cicadas (adults and nymphs), soil, and litter samples were collected at this site. Nymphs also were collected from another emergence about 5 km to the northwest. Cicad as from Brood XIX (mainly M. casir!i) were collected durint: the spring of 1985. Cicada nymphs were dug up ira Garth The sex of nymphs was not determined. Adult malts and females were captured in conical traps (Stewart, 1986) as they emerged during May ,md early June. A large sample of females was collected at a chorus center. Twenty-five nymph skins were collected after emergence from the lower 40 sub-plots at the Durham site. Two litter samples (0. I me2 ) were randomly collected fi l,rn ekch of the lower 40 sub-plots in November, 1984 just after leaf fall and az:ain in October, 1985 just before leaf fall. The first sample was divided ido current leaf fall and old litter and each was weighed separately. The litter was oven dried at 65°C weighed and ground to pass a 20 mesh screen. The litter tur:!over time (in years) was estimated from the ratio of leaf fall to the difference in litter standing crop just after litter fall and 1 year later (Qdum, 197 1). .A composite soil sample was collected from each sub-plot in October, 1985. Insects were frozen until ready for analysis, then oven dried at 65’4, ;nd weighed. Individual insects were dry ashed for cation and phosphorus analyses or digested for nitrogen analysis. Cations were determined by atomic adsorption spectrometry, phosphorus calorimetrically and nitrogen by the micro-Kjeldahl method. The nymph skins were composired into one sample and analyzed for Al, Mn, Fe, K and P. The same analytical procedures were used for iitter and soil samples. Soil was extracted with ammonium acetate (cations except Fe) or Bray’s II (Fe and P). A least-squares analysis for unbalanced #data was used to compare nutrient content between nymphs, adult males and adult females. SAS Procedure GH.M (Statistical Analysis Systems, 1985) was used in at1 statistical analyses. A significance level of 5% was used in all tests. RESULTSANDDlSCUSSllQN

In this study, as in others, adult males were about half the weight of females (Table 1 ). Adult males had a dry weight of 130 mg and females 250 ml; for an average ndult dry weight of 190 mg. The sex ratio of the emerging aGutLlts was 4YYomales and 5 1% females (K.G. Smith, personal communicatron,

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.A comparison _____

of the

Varlabic

nutrierlts

in iitrer fall and periodical Litter fail (g m-‘)

Iron Magnesium Calcium Sodium Potassium Phosphorus h!itrogen

4.3 3.0 38.0 0.4 1.8

I .o 14.8

L WHEELER

ET .AL.

cicada

Cicada (mgm-‘)

Re!ative

0.42 3.9 4.6 2.0 13.9 x.3 121.0

0.0 1 6.1 O.O! 0.5 0.5 0.9 0,s

imponance

( 4/o )

appear to be very high (Table 2). It is not clear why the litter is high in these elements or why the litter production is also high. The amount of eastern red cedar in the forest and the soil level of Ca are possible factors. The turnover of the litter was 12-I 8 months while the release of nutrients from cicadas was probably less than 2 months if vertebrate predators consumed most of the insects. In the case of predation, most nutrients presumably were not retained in the predator biomass, but passed in their feces and were thus readily released to the soil. The cicada population density of this study was comparatively low, 6.7 m-’ (KG. Smith, personal communication, 1985). Lukens and Kalisz ( 1989) found densities of 40 and 170 m-‘, and densities as high as 370 m-’ have been reported (Dybas and Davis, 1962). Thus the data in Table 3 may underestimate the importance of cicadas in more typicaf situations. If a population density of 100 m-’ is assumed, which is within the extremes in population densities reported, cicadas would represent 7% of the Na and K flux, and about 12% for P and N. At greater densities then, the cicadas can indeed be an important pulse it forest nutrient q&s. CONCLUSlONS

It’ymphs lost 20% of their body weight during metamorphosis primarily from the loss of the exoskeleton. The loss of the exoskeleton, which was high in Al and Fe, caused a reduction in concentration of about one-half to twothirds in adults. The loss of the exoskeleton also caused an increase in the N concentration of adults in comparison to nymphs. Adults were higher in Na concentration than nymphs and adult females had higher concentrations of K and P than adult males or nymphs. The increase in nutrient concentration not explainable by the loss of the nymph case was related to adult feeding. In this study, insects were not an important component of rhe annual nutrient flux into the forest litter. Cicadas accounted for less than I% of any

nutrientin the

annual litter fall. This was a function oflow population densi;y (6.7 rnw2 ). With higher population densit& the cicada can be an important aspect in forest nutrient cycles. The importance of cicadas to ecosystem dynamics may be the flux ofeneqy and nutrients into vertebrate predators, particularly bird?. ACKNOWLEDGMENTS

B. Blackburn and E. Smith collected litter and prepared samples for chemical analysis. J. Morrison did the chemical analysis. M. Cassid:; graciously gave the use of his land for this study. This work was funded by National Science Foundation Grant BSR-8408090 and by the University of Arkansas Agricultural Experiment Station.

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Reichle D.E.. Shanks, M.H. and Crossjey. D.A.. Jr.. 1969. Calcium. potassium and sodium content of forest Boor arthropods. Ann. Entomol. Sot. Am.. 62: 5?-62. Statistical Analysis Systems, 1985. SAS User’s Guide: Statistics. Version 5 edn. SAS Institute Inc.. Cat-y. NC. 956 pp. Schovvaitcr. T.D.. 198 1. Insect herbivore relationship to the state of the host plant: biotic regulation of ecosystem nutrient cycling through ecological su ccession. Oikos. 37: I26- 130. Schowalter. T.D. and Crossley, D.A.. Jr.. 1983. Forest canopy arthropods as sodium. potassium. magnesium and calcium pools in forests. For. Ecol. Manage., 7: 143-I 48. Seastedt. T.R. and Crossley, D.A.. Jr., 1980. Effects of microarthropods on the seasonal Gynamits of nutrients in forest litter. Soil Biol. Biochem., 12: 3?7-342. Stewart, V.B., 1986. Bird predation on the 13-year periodical cicada (Homoptera: Cicadidae: Magicicnda spp.) in an Ozark forest community, 1985. MS. Thesis. Dept. of Entomology, Univ. of Arkansas, Fayettevt!le. AR. USA, 62 pp. Stewart, V.B., Smith, K.G. and Stephen, FM.. 1988. Red-winged blackbird predation on periodical cicadas (Cicadidae: .2lagrcicada spp.): bird behavior and cicada responses. Oecologia. 76: 348-352. Stiiing. P.D., 1988. Eating a thin line. Nat. Hist.. 97(2): 62-67. Strandine. E.J., 1940. A quantitative study of the periodical cicada with respect to soil of three forests. Am. Mid]. Nat.. 24: 177-I 83. Swank, W.T.. Waide. J.B., Crossley, D..4., Jr. and Todd. R.L.. i 981. 11wzctdefoliation enhances nitrate export from forest ecosystems. Oecologia, 51: 297-299. WaYis. G.W., Stephen, F.M. and Smith, KG.. 1990. Interactions among Ozark forest birds. canopy arthropods and periodical cicadas. Ark. Farm Res.. 39( 2 ): 3. White. J. and Lloyd. M., 1985. Effect of habitat on size of nymphs m periodical cicadas (Homoptera: Cicadidae: .liagicica& spp. ). .I. Kans. Entomol. Sot.. 58: 605-6 IO. White. J. and Strehi. C.. 1978. Xy!em feeding by F