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Emergence of Periodical Cicadas (Magicicada cassini) From a Kansas Riparian Forest: Densities, Biomass and Nitrogen Flux MATT R. WHILES1,3,4, MAC A. CALLAHAM, JR.2, CLINTON K. MEYER1, BRENT L. BROCK2 AND RALPH E. CHARLTON1 1
Department of Entomology, Kansas State University, Manhattan 66506 2Division of Biology, Kansas State University, Manhattan 66506
ABSTRACT.—The 1998 emergence of 17-y periodical cicadas (Magicicada cassini) on Konza Prairie Research Natural Area (KPRNA), Kansas, was quantified using emergence trap transects and counts of emergence holes. Emergence density, biomass (emergence production) and associated nitrogen flux were estimated for the entire 100 ha gallery forest of Kings Creek, the major drainage network on KPRNA. Emergence commenced on 22 May 1998 and lasted for 24 d, with 87% of the individuals emerging within the first 9 d. Males dominated early during the emergence, and the sex ratio for the entire population was estimated at 54:46 male:female. Average emergence abundance and biomass estimated from trap transects located in low areas where cicadas were most abundant were 152/m2 and 34.9 g ashfree dry mass (AFDM)/m2, respectively. Based on emergence hole counts, average density and biomass for the 59 ha of gallery forest where cicadas emerged were 27.2 individuals/m2 and 6.3 g AFDM/m2, and emergence hole densities .100/m2 were evident in low areas of the drainage. Emergence density generally decreased with increasing elevation in the catchment. Belowground to aboveground N flux associated with M. cassini emergence in high density areas was ;3 g N/m2, and the average for the entire emergence area was 0.63 g N/ m2. The total number of individuals that emerged from the Kings Creek riparian forest was estimated at 19.6 million, which represents 4.6 metric tons AFDM and ;0.5 metric tons N. This linear, fragmented, gallery forest of the Flint Hills supports a high density of M. cassini, and an emergence event constitutes a significant belowground to aboveground flux of energy and nutrients. Thus, the periodical cicada may be an exception to the notion that insects generally do not represent important resource pools at the ecosystem level.
INTRODUCTION Although the importance of insects often transcends their relatively small size, their function in ecosystems generally is considered regulatory (Mattson and Addy, 1975; O’Neill, 1976; Kitchell et al., 1979; Seastedt and Crossley, 1984; Wallace and Webster, 1996), and most invertebrates ostensibly do not represent significant resource pools at the ecosystem level (Schowalter and Crossley, 1983). The regulatory functions attributed to insects usually are associated with feeding and egestion. Detritivores increase material and energy cycling rates through comminution of organic particles, which increases surface area, leaching, microbial activity and decomposition (Seastedt and Crossley, 1984, 1987); herbivores damage living plant tissues, resulting in enhanced leaching and/or greenfall (Tukey, 1970; Seastedt et al., 1983; Schowalter et al., 1986; Risley and Crossley, 1988); and predators can exert top-down control in systems (Hunter and Price, 1992; Moran et al., 1996). Frass production by herbivores and detritivores also can enhance energy and material cycling (Swank et al., 1981; Anderson and Ineson, 1983). Although herbivorous species often have only a nominal 3
Corresponding author Present address: Department of Zoology, Southern Illinois University, Carbondale 62901–6501. Telephone: (618) 453-7639; FAX: (618) 453-2806; e-mail:
[email protected] 4
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impact on ecosystem processes, their influence can be magnified greatly during outbreaks (Swank et al., 1981; Hollinger, 1986). Periodical cicadas (Homoptera: Cicadidae) are relatively large insects that can emerge in astonishing numbers. Although adult emergence occurs infrequently in a given area, their large size and high densities suggest that they may represent a significant resource and important flux of nutrients and energy from belowground to aboveground habitats (Brown and Chippendale, 1973; Wheeler et al., 1992; Williams and Simon, 1995). This flux is the end result of 13 or 17 y of energy and nutrient accrual in the belowground environment. Thus, periodical cicadas may be an exception to generalizations about arthropod consumers. Documented impacts of cicadas include changes in soil structure and distribution (Scully, 1942; Luken and Kalisz, 1989); increased moisture in upper soil layers (Anderson, 1994); and positive (numerical) responses by vertebrate predators (Leonard, 1964; Steward et al., 1988; Stephen et al., 1990; Krohne et al., 1991). Krohne et al. (1991) also presented evidence for increased survivorship of juvenile shrews during a periodical cicada emergence year. Wheeler et al. (1992) examined the significance of periodical cicadas for nutrient cycling in an Arkansas forest during a 1985 emergence event and found that they did not account for a significant flux of nutrients, including nitrogen and phosphorus (,1% of annual litterfall). However, their study examined a region of forest with relatively low cicada emergence density (6.7/m2) and they hypothesized that significant effects may be evident in areas with higher densities. In contrast, Dybas and Davis (1962) measured emergence densities as high as 370/m2 for a mixture of Magicicada spp. in northern Illinois and Luken and Kalisz (1989) reported densities of 40–170/m2 for emergence sites in northern Kentucky. These studies demonstrated that emergence densities of periodical cicadas can differ greatly and the significance of an emergence event to local energy and material budgets may vary accordingly. The objectives of this study were to quantify the 1998 emergence of brood IV 17-y periodical cicadas in a gallery forest in the Flint Hills region of Kansas and to assess the significance of this emergence for material and energy cycling. Because forests in this tallgrass prairie region are relatively narrow ribbons confined to riparian corridors, we had the unusual opportunity to examine closely periodical cicada emergence in a discrete forested area. We hypothesized, based on prior observations of the magnitude of the emergence in riparian forests of eastern Kansas, that periodical cicada emergence in this region represents a significant redistribution of energy and nutrients from belowground to aboveground habitats. METHODS Study area.—This study took place in the gallery forest of Kings Creek on the Konza Prairie Research Natural Area (KPRNA) in northeastern Kansas (398059N, 968359W). The Kings Creek catchment encompasses 1630 ha, including ;100 ha of gallery forest. The KPRNA is located in the Flint Hills region, which is predominately tallgrass prairie dominated by warm-season grasses mixed with a variety of forbs. Along mid- to high-order streams, relatively narrow gallery forests are present and are dominated by bur oak (Quercus macrocarpa), chinkapin oak (Q. muehlenbergii), elms (Ulmus spp.), hackberry (Celtis occidentalis) and others. Knapp et al. (1998) provide a detailed description of the KPRNA. Emergence traps.—Five emergence trap transects were established in randomly selected regions of gallery forest along lower Kings Creek on 19 May 1998 (Fig. 1). Orientations of transects were also selected randomly. Transects 3–5 consisted of 8–10 screen (0.32 cm mesh) traps (2500 cm2 sampling area, ;0.9 m high) placed 10–20 m apart in a line. Screen
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FIG. 1.—Map of the Kings Creek catchment (outlined in white) on KPRNA showing major drainages. Locations of emergence trap transects are indicated by numbers. Gallery forest appears as darker areas along drainages
traps were constructed by forming screening into a cylinder that was fastened with rivets and securing it to the ground with 15 cm nails. Lids constructed from the same material were placed on top of each and the edges were folded to grip the trap bodies. Emergence trap transects 1 and 2 consisted of 10 and 14 plastic traps (638 cm2 sampling area), respectively, placed ;10 m apart in a line. Plastic traps were constructed from inverted 19 liter plastic buckets with the bottom and ca. 70% of the cylinder removed and replaced with 1 mm nylon mesh to reduce condensation. Traps were placed in the field 3 d before the highly synchronized emergence commenced. All traps were checked daily after installation through peak emergence and every 2 d as emergence waned. Adult cicadas and nymphal exuviae collected in traps were sexed, counted and frozen for mass and nutrient analysis. Data from emergence traps were used primarily to examine emergence phenology and sex ratios. Voucher specimens from emergence traps were placed in the Kansas State University Museum of Entomology and Prairie Arthropod Research, Manhattan. Individual mass and nitrogen estimates.—Ten each of Magicicada cassini adult males, adult females and nymphal exuviae were randomly selected from emergence trap collections and processed to obtain gender specific dry mass (DM) and ash-free dry mass (AFDM) estimates by oven-drying (55 C for 4 d), weighing, ashing (500 C for 4 h) and then reweighing.
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Additional subsamples of 10 males, 10 females and 10 nymphal exuviae were analyzed for total N content. These specimens were freeze dried under high vacuum for 72 h and then ground to fine powder with a mortar and pestle. Subsamples of the fine powder from each specimen were weighed into tin capsules and %N was determined by combustion on a Carlo Erba C/N analyzer. Gender-specific DM, AFDM and total N (total N based on DM) were calculated by adding the respective value of an exuviae to that of adult males and females. These values were applied to data from emergence traps and emergence hole counts (see below) for estimating mass and N fluxes. Emergence hole counts and oviposition scars.—Rectangular sampling frames were used to estimate emergence density across the entire Kings Creek gallery forest. On 31 May 1998, as the cicada emergence waned, teams of two to three investigators walked assigned sections of the Kings Creek gallery forest and dropped a 0.1 m2 sampling frame at ;5 m intervals in a random direction. Vegetation and detritus were removed carefully, and all emergence holes within the frame were counted. Each periodical cicada emergence hole corresponds to the emergence of 1 individual (Dybas and Davis, 1962), and these holes are distinct from those of other large burrowing invertebrates such as Oligochaetes and Scarabaeidae (Coleoptera). Further, Magicicada cassini emergence occurs well before that of other cicadas found on KPRNA (Callaham et al., 2000). The 100 ha of gallery forest in the Kings Creek drainage was divided into 35 sections that ranged in size from 0.01–12.2 ha, and investigator teams were assigned to sections. Before surveying assigned areas, investigators calibrated hole-counting methodology together. Because forests on KPRNA are riparian, our approach to sampling involved walking parallel to the stream. In upper reaches of the drainage, where the forest narrows (,50 m on each side of the stream), 1 investigator walked each side of the stream. In lower areas, where the gallery forest is wider (.50 m ,130 m on each side), 2–3 three investigators, separated equidistantly from each other as they sampled, walked each side of the stream. A total of 1238 frame counts were made in the 100 ha of gallery forest. Emergence patches were digitized into a GIS, and average density of holes (5average number of individuals emerging/m2) was calculated for each section of the forest. Total emergence from each forest section was calculated as the product of the average number of emergence holes/m2 and the area of the section. The sex ratio estimated from total emergence trap collections was used to apply gender-specific individual mass and N values to hole count data. On 15 and 16 June 1998 all upper reaches of the Kings Creek gallery forest were examined for the presence of Magicicada cassini oviposition scars. This was a qualitative assessment in which terminal twigs of trees were examined in the field for scars left by ovipositing females and/or females were observed in the act of ovipositing. Because periodical cicadas emerge before other cicadas present on Konza, we attributed fresh oviposition damage to M. cassini females. When oviposition damage was found in areas where emergence did not occur (i.e., absence of emergence holes), locations were recorded. RESULTS Emergence phenology and sex ratios.—Emergence trap data and field observations indicated that Magicicada cassini emergence on KPRNA commenced on 22 May 1998 and lasted 24 d. However, 87% of the individuals emerged within the first 9 d (Fig. 2). A somewhat protandrous emergence pattern was evident (Fig. 2) and males formed chorusing centers in selected trees soon after emergence. Mating pairs were first observed on 30 May and oviposition scars on twigs were present by 2 June. By 4 July all chorusing had stopped and no living M. cassini were evident on KPRNA. Based on emergence trap collections of a
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FIG. 2.—Emergence sequence of Magicicada cassini on KPRNA showing total numbers collected in emergence traps over 3-d intervals and sex ratios
total of 440 individuals, males constituted 54% of the M. cassini population in the Kings Creek gallery forest. Individual mass and N content.—The average (6SE) mass of adult male Magicicada cassini (0.149 6 0.009 g AFDM) was ;55% that of females (0.264 6 0.009 g AFDM). Exuviae contributed an additional 0.03 6 0.002 g AFDM to the mass of each sex. Both male and female adults were ;3% ash, whereas exuviae averaged 26% ash. Average (6SE) percent N was slightly higher for males (11.2 60.2%) than females (10.9 6 0.3%), but because of higher female mass, total N of females (29.8 mg DM) was 1.7X that of males (17.4 mg DM). Average N content of exuviae was 7.9 6 0.9%, so each exuviae represented an additional 3.3 mg DM of N added to adult values. Emergence production patterns.—Three of the five transects of emergence traps were located in areas where Magicicada cassini emerged. No cicadas were captured in the two transects located on the north branch of Kings Creek (transects 4 & 5, Fig. 1). Of the three transects where cicadas were captured, the one located lowest in the drainage (transect 1, Fig. 1) had the highest average (6SE) emergence density (263 6 36/m2) and biomass (59.7 6 8.2 g AFDM/m2). Transects 2 and 3 had emergence densities of 150 6 15.7 and 42.8 6 6.4/m2, respectively. Average emergence density and biomass for these three transects were 152/m2 and 34.9 g AFDM/m2, respectively. This represents an average of 1.45 g AFDM/m2 daily emergence production over 24 d in areas of the gallery forest where M. cassini emergence occurred. Emergence holes were completely absent from only one section of substantial gallery
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FIG. 3.—GIS coverage of the Kings Creek drainage basin on KPRNA showing interpolated Magicicada cassini emergence density and production and associated N flux
forest located on the north branch of Kings Creek (where emergence traps in transects 4 and 5 failed to catch cicadas) and the uppermost reaches where the gallery forest dwindled (Fig. 3). Average emergence hole densities across the 34 sections (total of 59 ha) of gallery forest where Magicicada cassini emerged ranged from 2.3–116.4/m2, corresponding to 0.53–27 g AFDM/m2. Averages (6SE) for the entire area where emergence occurred were 27.2 6 4.7 individuals/m2 and 6.3 6 1.0 g AFDM/m2. Thus, average annual emergence production in the Kings Creek gallery forest during 1998 was 6.3 g AFDM·m2/yr. Areas of highest emergence density were confined to lower Kings Creek and emergence values decreased in upper reaches of the drainage (Fig. 3). Belowground to aboveground N flux associated with M. cassini emergence in high density areas was ;3 g N/m2, and the average for the 59 ha emergence area was 0.63 g N/m2 (Fig. 3). Based on emergence hole counts, we estimated the total number of individuals that emerged from the Kings Creek riparian forest was 19.6 million, which represents 4.56 metric tons AFDM and ;0.5 metric tons N. Oviposition patterns.—Qualitative assessment of oviposition scars revealed that female Magicicada cassini dispersed and oviposited over a greater area than where they emerged. Trees in all upper reaches of the gallery forest, including areas with no evidence of emergence (no emergence holes or exuviae evident), had fresh oviposition scars on them by mid June. This included the north branch of Kings Creek and isolated groups of trees at the uppermost reaches of the drainage.
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DISCUSSION The emergence density estimates from this study generally fall within the range reported previously for periodical cicadas. The 27.2/m2 average (based on emergence hole counts) for emergence areas in the Kings Creek gallery forest exceeds the 6.7/m2 reported for a forest in northern Arkansas by Williams et al. (1991), but is within the range of 2–52/m2 recently estimated for Ohio forests (Rodenhouse et al., 1997). If data from only our emergence traps in areas where cicadas emerged are considered, the average value of 152/m2 is substantially higher than these prior estimates. However, the emergence trap and hole count estimates from this study are both much lower than the 370/m2 reported by Dybas and Davis (1962) in northern Illinois. The disparity between estimates from emergence traps and emergence hole counts is most likely related to the spatial scale associated with each approach. The three transects of emergence traps that caught cicadas were located along lower Kings Creek, where Magicicada cassini emergence density was highest. Hole counts took place across the entire gallery forest and integrated a range of topography and cicada emergence densities, including upper reaches where emergence density was low. Had we counted holes only along lower Kings Creek, where densities often exceeded 100/m2, we would have obtained a much higher overall estimate. Similarly, the 370/m2 density reported by Dybas and Davis (1962) was for lowland forest only, and they estimated a much lower emergence density of 33/m2 in upland forest. Our estimates, based on emergence holes, also are conservative because some cicadas were still emerging when we counted holes. Emergence trap data indicate that 87% of cicadas had emerged by the day we counted holes. Thus, actual emergence density and production for our study site could have been ;13% higher than we estimated. The relatively high emergence densities we observed in much of the Kings Creek gallery forest may be related to the shape of forest stands in this region. Previous investigations of periodical cicadas have noted a preference for forest edges (Lloyd and White, 1976; Lloyd and Karban, 1983), and Rodenhouse et al. (1997) recently demonstrated that emergence density of periodical cicadas in forest fragments in Ohio was highest in forest edges. On KPRNA, as with the rest of the Flint Hills, tallgrass prairie dominates the landscape, and hardwood forests generally are confined to stream valleys. Thus, forest distribution in the Flint Hills region is linear, and edges are maximized (edge/area of the lower Kings Creek gallery forest 5 0.02). The linear nature of forest patches in the Flint Hills also may have influenced periodical cicada species composition. Periodical cicada emergences often include 2–3 species (e.g., Dybas and Lloyd, 1962; Rodenhouse et al., 1997). However, based on positive identification of specimens from traps, and chorusing heard in the drainage, the emergence in the Kings Creek gallery forest consisted exclusively of Magicicada cassini. This species is known to favor forest edges and linear forest stands, whereas the larger species of 17-y periodical cicada, M. septendecim, prefers interior forest (White, 1980; Rodenhouse et al., 1997). Magicicada septendecim was observed by us and other investigators (R. J. Elzinga, KSU Entomology, pers. comm.) in a more extensively forested area near KPRNA during the same time as our study. Edge/area ratios, determined from USGS Digital Ortho Quarter Quadrangles, were 0.01 for the area near KPRNA where M. septendecim were abundant, and 0.02 for the lower Kings Creek gallery forest where M. cassini dominated. Our study indicates that periodical cicada emergences are significant events. At least for this region, the periodical cicada is an exception to the notion that insects rarely represent significant resource pools at the ecosystem level. Emergence production was 23–29 g AFDM·m2/yr in areas of lower Kings Creek (Fig. 3), and periodical cicadas are a rich source
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of protein (Brown and Chippendale, 1973). Further, periodical cicadas have no sophisticated predator defense mechanisms (Brown and Chippendale, 1973; Steward et al., 1988) and many predators are known to feed on them (Karban, 1982; Maier, 1982; Strehl and White, 1986; Steward et al., 1988; Kellner et al., 1990; Stephen et al., 1990; Krohne et al., 1991; Williams and Simon, 1995). We observed periodical cicadas in guts of creek chubs (Semotilus atromaculatus) collected from Kings Creek, coyote (Canis latrans) scats composed primarily of periodical cicada parts, and numerous birds and invertebrates feeding on cicadas. Emergence production of periodical cicadas during 1998 exceeded estimates of insect emergence production from even the most productive habitats on KPRNA. Gray (1989, 1993) quantified emergence production of aquatic insects from various reaches of Kings Creek and showed a positive correlation with insectivorous bird densities. Gray (1989) estimated that average daily aquatic insect emergence production ( June–Aug.) was 20.3 mg DM/m2, which is three times the terrestrial insect production in tallgrass prairie, based on estimates calculated from Scott et al. (1979). Thus, tallgrass prairie streams represent ‘‘hot spots’’ of invertebrate production during the growing season and insectivores respond positively. Average daily emergence production of periodical cicadas across the entire Kings Creek gallery forest during the 24-d emergence was 263 mg AFDM·m2/d and approached 1 g AFDM·m2/d in high-density areas. These values greatly exceed those reported for stream insects on KPRNA, but the temporally discrete nature of periodical cicada’s emergence diminishes its apparent significance. Nonetheless, it represents a relatively large pulse of insect biomass into the aboveground environment which, when occurring, greatly exceeds estimates for other insect groups on KPRNA. Predators that are present during years of periodical cicada emergence likely exploit this abundant resource and benefit, as is the case with aquatic insect emergences. Nitrogen is a limiting nutrient in the tallgrass prairie, and periodical cicada emergence on KPRNA represents a significant N flux. Average total N flux associated with the 1998 periodical cicada emergence represents ;40% of annual bulk precipitation inputs (dryfall 1 wetfall) (Blair et al., 1988), which are the primary sources of ‘‘new’’ N entering the tallgrass prairie ecosystem. In lower areas of the gallery forest, where cicada emergence was quite high, associated N flux exceeded estimates of annual bulk precipitation inputs for KPRNA by as much as 2X and approached estimates of N annually translocated from belowground to aboveground by plants (Blair et al., 1988). Similar to translocation by plants, N flux associated with cicada emergence is not an input of ‘‘new’’ N to the system, but represents movement of material from belowground to aboveground. Nitrogen translocated to the aboveground environment by cicada emergence is available immediately to a wide variety of secondary consumers, whereas N in plant tissues enters herbivore and/or detrital pathways. Because periodical cicadas are associated with trees, the N flux we quantified was limited to the gallery forest. However, gallery forests in this region are small patches in a sea of tallgrass prairie (gallery forest 5 7% of the land cover on KPRNA, Knight et al., 1994), and the two habitats are not independent. Periodical cicadas were observed throughout KPRNA by the end of the emergence period, including areas with few or no trees. Within the Kings Creek gallery forest, N flux associated with the periodical cicada emergence was significant compared with forest cycling processes. Previous attempts to quantify the significance of periodical cicadas to forest nutrient cycles compared nutrients in cicada biomass to that of forest litterfall. Wheeler et al. (1992) closely examined an emergence in northern Arkansas and quantified these pools. Because emergence density was relatively low and annual litterfall was relatively high in their study site, cicada nutrient reserves did not appear significant (0.8% of N in annual forest litterfall). In our system, where annual
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litterfall is relatively low in the less dense gallery forests and cicada emergence production was relatively high, periodical cicadas accounted for a much higher percentage of N. Leaf litterfall in the Kings Creek gallery forest averages 311 g DM/m2 (Briggs et al., 1989) and postabscission leaf litter from the mix of trees in this forest averages ;1% N (Killingbeck, 1984). Thus, annual leaf litterfall N in the Kings Creek gallery forest is ;3.1 g/m2 and the N flux associated with periodical cicada emergence production averaged 20% of this. In lower areas of the drainage, where cicada emergence production was highest, cicada N flux was nearly equal to N in annual litterfall. Hamburg and Lin (1998) estimated that total N flux associated with throughfall in a northeast Kansas forest during a growing season was 128 mg/m2. This represents only ;20% of the average N flux associated with periodical cicada emergence during our study and a much smaller fraction of the flux that occurred in high density areas of lower Kings Creek. Although this emergence happens only once every 17 y, a significant below- to aboveground flux of N is apparent when it does. Emergence density and production varied greatly across the gallery forest we examined. Much higher densities were evident along lower Kings Creek and values generally decreased farther up into the catchment. Although this pattern appears to contradict observations that Magicicada cassini prefer forest edges, a maximum edge/area threshold may exist (50.04 for forests along upper reaches of Kings Creek), and other factors such as soil depth could override effects of forest stand morphology. Upper areas of the drainage generally have shallow, rocky soils that hinder forest development (Ransom et al., 1998) and are less suitable for large burrowing invertebrates. James (1982) found that Oligochaetes, another important group of subterranean macroinvertebrates, were also most abundant in the deeper soils of low areas on KPRNA. The absence of cicadas in the gallery forest of the north branch of Kings Creek was an interesting exception to the overall pattern of highest cicada densities in lower areas of the drainage. Lower reaches of the north branch are lower in elevation than many patches of the south branch where cicadas were still abundant. Like other low areas on KPRNA, the north branch of Kings Creek also has a well-developed gallery forest (see Figs. 1 and 3). However, Abrams (1986) found that forested areas on the lower north branch of Kings Creek were dominated by oaks, whereas other lower reaches of the gallery forest were dominated by hackberry, followed by oaks. In addition, the basal area in the north branch forest was lower than lower Kings Creek and upper areas of the south branch. Thus, tree species composition, and/or underlying physical factors may have influenced emergence patterns we observed on KPRNA. One of the most striking changes to occur on KPRNA in the last 100 y is the expansion of the gallery forests (Briggs et al., 1998). From 1939–1985, gallery forest on KPRNA expanded by 57% (Knight et al., 1994). Aerial photographs reveal that some upper reaches of gallery forest on the south branch of Kings Creek where cicadas emerged in 1998 were not forested in 1939. Forest expansion in the Flint Hills resulting from fire suppression might be facilitating local range expansion of these insects. However, some areas of forest on KPRNA may not have been colonized yet because colonization by an insect that emerges only once every 17 y would be expected to proceed slowly. Although this is an appealing explanation for the lack of periodical cicadas on the north branch of Kings Creek, aerial photographs as old as 1939 (time enough for three emergence events before 1998) reveal a well-developed gallery forest in this area. Thus, other mechanisms discussed above are more likely precluding cicadas from this particular area. Our field observations revealed that Magicicada cassini oviposited on trees throughout the Kings Creek drainage, including the north branch and many upper reaches where emergence did not occur. Sampling in the year 2015 will reveal if periodical cicadas are expanding their range on KPRNA and/or
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if factors other than forest cover (e.g., soils, topography, flooding frequency) influence survivorship of nymphs and render some forest stands uninhabitable. Acknowledgments.—M. Flinn, A. Gesche, J. Jonas, D. Kitchen and W. Rogers assisted with the onerous task of sampling cicada emergence holes. G. Hoch provided valuable assistance with all aspects of this project. J. M. Blair, C. Carlton, J. R. Nechols, S. B. Ramaswamy and an anonymous reviewer provided valuable comments on early drafts of this manuscript. This project was funded in part by a grant from the National Science Foundation to the Konza Long Term Ecological Research. KPRNA is owned by the Nature Conservancy and managed by the Kansas State University Division of Biology. This is contribution 00–68-J from the Kansas Agricultural Experiment Station.
LITERATURE CITED ABRAMS, M. D. 1986. Historical development of gallery forests in northeast Kansas. Vegetatio, 65:29–37. ANDERSON, D. C. 1994. Are cicadas (Diceroprocta apache) both a ‘‘keystone’’ and a ‘‘critical link’’ species in lower Colorado River riparian communities? Southwestern Nat., 39:26–33. ANDERSON, J. M. AND P. INESON. 1983. Interactions between soil arthropods and micro-organisms in carbon, nitrogen and mineral element fluxes from decomposing leaf litter, p. 413–432. In: J. E. Lee, S. McNeill and I. H. Rorinson (eds.). Nitrogen as an ecological factor. Blackwell Scientific Publications, Oxford. BLAIR, J. M., T. R. SEASTEDT, C. W. RICE AND R. A. RAMUNDO. 1998. Terrestrial nutrient cycling in tallgrass prairie, p. 222–243. In: A. K. Knapp, J. M. Briggs, D. C. Hartnett and S. L. Collins (eds.). Grassland dynamics: Long-term ecological research in tallgrass prairie. Long-term ecological research network series. Oxford University Press, New York. BRIGGS, J. M., M. D. NELLIS, C. L. TURNER, G. M. HENEBRY AND H. SU. 1998. A landscape perspective of patterns and processes in tallgrass prairie, p. 48–66. In: A. K. Knapp, J. M. Briggs, D. C. Hartnett and S. L. Collins (eds.). Grassland dynamics: Long-term ecological research in tallgrass prairie. Long-term ecological research network series. Oxford University Press, New York. ———, T. R. SEASTEDT AND D. J. GIBSON. 1989. Comparative analysis of temporal and spatial variability in above-ground production in a deciduous forest and prairie. Hol. Ecol., 12:130–136. BROWN, J. J. AND G. M. CHIPPENDALE. 1973. Nature and fate of the nutrient reserves of the periodical (17 year) cicada. J. Insect Physiol., 19:607–614. CALLAHAM, M. A., JR., M. R. WHILES, C. K. MEYER, B. L. BROCK AND R. E. CHARLTON. 2000. Feeding ecology and emergence production of annually emerging cicadas (Homoptera: Cicadidae) in tallgrass prairie. Oecologia, 123:535–542. DYBAS, H. S. AND D. D. DAVIS. 1962. A population census of seventeen-year periodical cicadas (Homoptera: Cicadidae: Magicicada). Ecology, 43:432–444. ——— AND M. LLOYD. 1962. Isolation by habitat in two synchronized species of periodical cicadas (Homoptera: Cicadidae: Magicicada). Ecology, 43:444–459. GRAY, L. J. 1993. Response of insectivorous birds to emerging aquatic insects in riparian habitats of a tallgrass prairie stream. Am. Midl. Nat., 129:288–300. ———. 1989. Emergence production and export of aquatic insects from a tallgrass prairie stream. Southwestern Nat., 34:313–318. HAMBURG, S. P. AND T. LIN. 1998. Throughfall chemistry of an ecotonal forest on the edge of the great plains. Can. J. For. Res., 28:1456–1463. HOLLINGER, D. Y. 1986. Herbivory and the cycling of nitrogen and phosphorus in isolated California oak trees. Oecologia, 70:291–297. HUNTER, M. D. AND P. W. PRICE. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology, 73:724–732. JAMES, S. W. 1982. Effects of fire and soil type on earthworm populations in a tallgrass prairie. Pedobiologia, 24:37–40. KARBAN, R. 1981. Flight and dispersal of periodical cicadas. Oecologia, 49:385–390. ———. 1982. Increased reproductive success at high densities and predator satiation for periodical cicadas. Ecology, 63:321–328.
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ACCEPTED 28 FEBRUARY 2000
