Comparison of the Assemblages of Sap-Feeding (Homoptera-) Inhabiting Two Structurally Different Salt Marsh Grasses in the Genus Spartina1

ROBERT F. DENNO" Department of Entomology and Economic Zoology, Rutgers University, New Brunswick, NJ

ABSTRACT The vegetation of New Jersey tidal salt marshes is composed primarily of 2 grasses; Spartina patens, which occupies a narrow elevational zone of high marsh and Spartina alterniflora, an intertidal species. S. patens forms a dense, persistent, thatch, while S. alterniflora produces only a loose lattice of litter which rapidly decomposes. A comparison between the guilds of sap-feeding insects (for the most part, Delpha- cidae, Cicadellidae, , and Miridae) inhabiting these grasses reveals S. patens housing a much more diverse assemblage of herbivores than S. alterniflora. S. alterni- flora-inhabiting species are exclusively bi- or trivoltine, while on S. patens, sap-feeders possess a greater variety of life history types and show a specialized trend toward urnvoltinism. Removal of only the dead thatch portion of S. patens results in reduced species diversity and evenness of sap-feeders on the living grass system. Trivoltine species, which normally inhabit the upper strata of S. patens, increase their populations on dethatched grass compared to the unaltered grass system. Both empirical and experimental evidence suggests that the complex microstructure and thatch of S. patens provide a more heterogeneous and protective resource which supports a more diverse and specialized fauna of sap-feeders than S. alterniflora.

Murdoch et al. (1972) and Allan et al. (1975), tion of tidal salt marshes along the northeast coast respectively, show that the species diversity of Hom- of North America. S. patens forms a dense persistent optera and correlates with the foliage thatch composed of dead plants from 3 or more pre- height diversity of field vegetation. Also, there is a vious growing seasons, while the dead culms of S. positive correlation between mean vegetation height alterniflora form a loose lattice that decomposes and the richness and diversity of rapidly over the course of the following year (Blum (Homoptera) inhabiting grassland habitats (Morris 1968). To test the prediction that structurally com- 1971, 1974). In addition to the inherent structural plex, thatch-forming grasses house a more diverse complexity of the living portion of vegetation, cer- fauna of phytophagous insects than thatch-free tain plants, particularly some of the grasses, have an grasses, I compared the assemblages of sap-feeding associated basal thatch of dead culms and blades insects residing in S. patens and S. alterniflora. In (Blum 1968). Grasses which produce a persistent order to further investigate this prediction, thatch thatch have an added component of structural diver- was removed from small plots of S. patens and the sity which thatchless species lack. Such grasses may responses of herbivorous insects were measured. provide additional oviposition sites, protection from physical stresses, and refuge from predators or para- Stmcture of Host Grasses sites, characteristics which might increase the re- S. patens (hereafter abbreviated SP) occupies a liability and/or heterogeneity of the resource, lead- narrow elevational zone of well-drained high marsh ing to an increase in the number of resident herbi- above mean high water level (MHW), where it can vores. Furthermore, the presence of a basal thatch grow in extensive pure stands that are occasionally may dictate moisture, temperature and light gradients inundated by tides (Redfield 1972). SP is a slender- along the vertical axis of the living grass system, culmed grass with narrow, convoluted blades (Mob- further increasing the number of microhabitats, and berly 1956, Blum 1968). The culms of SP grow possibly allowing for the coexistence of additional and project through a thick (5-20 cm), dead, hori- phytophagous insects. Morris (1975) substantiated zon of prostrate culms and blades resulting from the this hypothesis in part when he found a more diverse previous years' growth. New culms, shaped like community of Auchenorrhyncha associated with un- vertical awls, first protrude through the thatch in burned areas of grassland than habitats where litter spring. As the season progresses, older leaf-blades was removed by burning. separate from newer, upright ones by bending at the Spartina alterniflora Lois. (Salt Marsh Cordgrass) sheath-blade junction. As subsequent blades fold and Spartina patens (Ait.) Muhl. (Salt Meadow back in this fashion, they make contact with the Cordgrass) are 2 grasses that dominate the vegeta- surface of the dead thatch. By summer, the dead thatch becomes overlaid with an entanglement of 1 This report is a paper of the Journal Series, New Jersey Agric. Exp. Stn., Rutgers-the State University of New Jersey, living leaf-blades. Further prostration occurs in New Brunsw.l.ck, NJ. The study was supported by a grant from summer and faIl, when the culms of SP fold over at the New Jersey State Mosquito Commission. "Received for publication Nov. 16, 1976. Present address: a weak area in the stem which coincides approxi- Department of Entomology, University of Maryland, College Park, MD 20742. mately with that portion of the stem that is included 359 360 ENVIRONMENTAL ENTOMOLOGY Vol. 6, no. 3 in and surrounded by the dead thatch (Blum 1968). height in Aug. was 32.8 cm) and SP. Using a Prostration usually occurs in a mosaic fashion, leav- 38.1 cm diam (=15") standard sweep net, insects ing behind small "islands" of somewhat erect plants. were sampled on 28 dates at approximately one wk If the structure of SP were examined during sum- intervals between March and Dec., 1974. Each mer, one would find an uppermost layer of living, sample consisted of 30 sweeps taken while walking partially prostrate grass overlying a dead horizon of through pure stands of each grass. Five samples dry culms from the previous year. Beneath this were taken from each grass habitat on each date. dry horizon is a layer of entangled moist culms and Swept insects were killed in a large ethyl-acetate jar, blades 2 and 3 yr old. Between the moist layer of transferred to 250 ml alcohol (95 % ethanol) bottles, culms and the marsh surface is a horizon of decaying and returned to the laboratory, where they were grass older than 3 yr. sorted to species and instar, and counted. S. alterniflora, an intertidal grass, occurs through- The advantages of the sweep net over other out most of the elevational range of SP, but also ex- sampling methods lies with its ability to collect large tends to levels far below MHW (Adams 1963, Blum numbers of widely dispersed and fast-moving insects 1968, and Redfield 1972). There are 2 distinct (Southwood 1966). A few species were observed growth forms of S. alterniflora. Near MHW, where to occur primarily beneath the thatch of SP; these the marsh is flat, S. alterniflora grows as a short sap-feeders were probably slighted by the net. In form (hereafter abbreviated SAS), consisting of stiff order to minimize some of the inadequacies of the rosettes of flat, divergent, leaves, that attain a height sweep net as a sampling tool, posed by various of only 1-4 dm. Dead blades and culms of SAS authors (DeLong 1932, Gray and Treloar 1933, and fall in place on the moist marsh to form a loose Beall 1935), samples were taken on clear «50% lattice of litter, which rapidly decomposes over the cloud cover), usually warm (>19°C) days, in dry course of the following year (Burkholder and Born- vegetation within 2 h of noon, when most species side 1957, Squiers and Good 1974). Reduced culm were observed to move into horizons of vegetation density and the lack of extensive thatch allow for sampled by the net. exposure of the marsh surface in SAS habitats. To examine the responses of herbivorous insects Along the depressed borders of natural tidal creeks, to thatch removal, 3 separate square plots, each at elevations well below MHW, tall-form S. alterni- 100 m" and separated from one another by ca. 25 m, flora (hereafter abbreviated SAT) grows, where the were selected in a pure stand of SP. Using electric culms commonly reach heights over 2 m. On most lawn clippers and large knives, virtually all above- New Jersey salt marshes, there are extensive areas ground vegetation (including thatch) was removed of flat high marsh covered by SAS which abruptly from 2 of the plots during the winter (Jan., 1975) intergrade, over the distance of a few meters, into and the unclipped plot was used as a control. Shoots SAT along the depressed margins of creeks. of the perennial grass appeared in both dethatched New shoots of SAS and SP appear in spring, and plots and the control area in spring. To determine maximum, above-ground, living, standing crop is the effect of thatch removal on grass growth and to attained in July or Aug. on New Jersey marshes demonstrate the efficiency of dethatching, I sampled (Squiers and Good 1974, Busch 1975). Maximum both living and dead components of the standing standing crop values for SAS and SP are similar. crop biomass of SP during March, mid-June, and Nixon and Oviatt (1973) report 432 and 430 g again in late July (peak standing crop) in each of dry wt/m", respectively, for SAS and SP on a Rhode the 3 plots. Standing crop was determined by clip- Island salt marsh; Squiers and Good (1974) ob- ping all grass within a randomly tossed 0.047 m" tained a standing crop of 592 g/m" for SAS on a wire quadrat [recommended by Wiegert (1962) as New Jersey marsh; and Busch (1975) also working optimum quadrat size for sampling grass vegetation], in New Jersey, recorded peak standing crop values sorting living plants from dead thatch, drying each of 402 g/m" and 479 g/m" respectively for SAS component at lOO·C for 24 h, and weighing each and SP. portion. Five samples were taken from each plot on each date. Study Site and Methods Insects were sampled on June 17, July 23, Aug. 20 The study site was an extensive salt marsh in the and Sept. 20 by taking 5 samples (10 sweeps/sample) Barnegat National Wildlife Refuge located approxi- in the unclipped and dethatched plots on each date. mately 3 km E. of Manahawkin, Ocean Co., NJ Sweep transects were taken in parallel, nonoverlap- (39·, 42' N. Lat., 74·, 15/ W. Long.). Both SAS ping swaths in each plot, while keeping 1 swath- and SP occurred as a mosaic of large (> 1 ha), pri- width from the plot edge. Captured insects were marily pure stands. By measuring aerial photographs processed according to the method outlined above. with a planimeter, the relative cover of SAS and SP The removal of thatch during the winter, leaving was calculated at 52% and 48%, respectively. SAT little vegetation on the exposed marsh surface, cer- fringed the natural creeks and ditches on the marsh tainly must be viewed as a large scale perturbation. and represented an insignificant percentage of the Exploitation of the living grass in the dethatched total grass cover. plots the following season is completely dependent A sampling area was established which incorpo- on immigration of insects from adjacent source areas. rated a large expanse of both SAS (mean culm To ensure that any differential response by the in- June 1977 DENNO: SAP-FEEDERSINHABITINGSpartina 361

sect community recorded in the clipped areas was and the evenness component of species diversity of due to the absence of thatch and not to retarded sap-feeders were measured throughout most of the rates of recolonization, plots were purposely kept year in SP and SAS (Fig. 1). Except for the winter small, and sampling was not initiated until and early spring months, the number of resident 5 mo following the removal of thatch. species was significantly higher in SP than SAS Herbivore diversity for each sample was measured (F1•224 = 1454.38; P « .001). In both grasses, using the Shannon-Weaver information index (Shan- the only species taken during the winter season were non 1948): delphacids, which overwintered as nymphs. With the s onset of spring, overwintering eggs of Cicadellidae, H' = -1: PI lnpl' Issidae, and Miridae hatched and accounted for most i=1 of the increase in species richness. The richness of where H' is the amount of diversity in a group of sap-feeders in SP increased rapidly in May and species, s is the number of species under considera- reached a peak during early July, after which there tion, Pi is the relative abundance of the it" species, was a steady decline until winter when minimum and InPl is the natural logarithm of Pl' The evenness values were recorded. In SAS, the seasonal trend component of species diversity was measured by the of species richness was similar, but maximum values ratio of observed diversity to the maximum possible were obtained during the fall. diversity for a particular set of species and indi- Sap-feeder diversity (H') was also significantly viduals (Pielou 1966): higher in SP compared to SAS on most sample dates (F , 224 = 1956.98; P .001). There was a con- J' = H'/H max, = H'/lnS, I < < spicuous peak of sap-feeder diversity during May in where J' is evenness, H' is the observed diversity and SP, but values oscillated around 0.7 for the re- InS (=H max=maximum diversity) is the natural mainder of the year. Contrary to the pattern of logarithm of the number of species in the set. Species sap-feeder diversity in SP, diversity was highest diversity (H') has no theoretical upper bound and during winter and early spring in SAS. Throughout is limited only by a finite number of species. Species most of spring and summer, near 0.0 values of sap- evenness, on the other hand, is constrained between feeder diversity were obtained in SAS. Dense popu- o and 1.0. lations of the delphacid, Prokelisia marginata (Van In order to measure the relative success of a Duzee), were primarily responsible for the low phytophagous species in dethatched grass compared species diversity in SAS. to grass having thatch, I used the following index: The evenness of sap-feeding species (1') was SI = Nt+l!At , highest during the spring and winter seasons in both where SI is the index of success, Nt+1, is the density salt marsh grasses. Species evenness was consistently of nymphs at time t+1 and At is the density of low during spring and summer in SAS, and in adults at time t. A number of factors associated summer and early fall in SP. Generally, evenness with the quality of oviposition sites and the suit- was significantly higher in SP compared to SAS ability and harshness of nymphal habitats could lead (F1•224 = 562.59; P < < .001). to small densities of nymphs at time t+1 relative to I examined the relationships of the richness, adult densities at time t, reducing the success of diversity, and evenness of sap-feeders with the sea- the species, and documenting the inferior nature of sonal growth pattern of each respective host grass. a particular habitat for insect development. The This was accomplished by correlating sap-feeder validity of the index is dependent upon the assump- richness, H', and l' with corresponding seasonal tion that the number of adults present at time t is values of living, above-ground, standing crop biomass representative of those adults which potentially could of both grasses. Standing crop values for SP and contribute to the density of nymphs at time HI. To SAS were taken from Busch (1975), who sampled best meet this assumption, the time interval t+l-t the same marsh during the same year as I did. should approach the generation time of the species The correlation between sap-feeder richness and so that the nymphs measured are indeed the off· grass standing crop was significant in both SP spring, and not the contemporaries, of the adults. (y=3.409 0.209x, n=28, r=.816, P .01) and Because of irregularities in the sampling interval + < SAS (y= 1.938 0.096x, n=28, r=.531, P .01) t+l-t, the absolute value of the success index (SI) + < (Fig. 2). The same correlation using sap-feeder is trivial, but the magnitudes of indices can be used to compare the relative success of a species under diversity (H') was not significant with either SP 2 or more different conditions as long as the same (y=0.650 + 0.002x, n=28, r=0.67, P > .05) or time interval is used and the generations of the spe- SAS (y=0.169 - 0.009x, n=28, r=-.356, P > .05). cies developing under both conditions are relatively Evenness was negatively correlated with grass stand- synchronous. ing crop in SP (y=0.591 - 0.014x, n=28, r=-.578, P < .01) and SAS (y=0.220 - O.020x, n=28, r=- Results .450, P < .05) (Fig. 3). Comparison of Sap-feeder Richness and Diversity The structure of each respective guild of sap- Between Grass Associations feeders exploiting SP and SAS is summarized in The number of resident species, species diversity, Fig. 4, where species are ranked according to their 362 ENVIRONMENTAL ENTOMOLOGY Vol. 6, no. 3

10 r./) Q) '0 Q) 0.5 l.J)

d z

A M J J A s o N I (/') I t.. ~ Q) .•.... 'ii'i10 'U L. Q) Q) .~ ~ 0 r./) .5 a. Q) C'O '0 Q) (/) a. l.J)

A M J J A s o N FIG. l.-Seasonal patterns of sap-feeder richness, diversity (H'), and evenness (J') in the salt marsh grasses, Spartina alterniflora and S. patens. Statistical intervals surrounding means are Least Significant Intervals (LSI). Graphical nonoverlap of intervals connotes significance among means at the 5% probability level. abundance in each habitat. Eleven residents, that minuta McDermott (), Eriococcus n. sp. developed at least one generation of adults per year, (Eriococcidae), Aphelonema simplex (Uhler) (Issidae), (4 Delphacidae, 4 Cicadellidae, 1 Issidae, 1 Erio- and Amplicephalus simplex (Van Duzee) (Cicadel- coccidae, and 1 Pentatomidae) were sampled in SP. lidae), which were not as abundant as D. detecta, Only 5 sap-feeders (3 Delphacidae, 1 Cicadellidae, but had a seasonal total of individuals > 1000. The and 1 Miridae) were sampled on SAS. The dominant lack of subdominant residents in a community com- herbivores in both grasses were delphacids, Delpha- pletely dominated by P. marginata was primarily codes detecta (Van Duzee) in SP and Prokelisia responsible for the low species diversity and equit- marginata (Van Duzee) in SAS. The SP association ability of the sap-feeding guild in SAS compared also supported a series of subdominants, Tumidagena to SP. June 1977 DENNO: SAP-FEEDERS INHABITING Spartina 363

Assemblage of Sap-feeders Inhabiting Spartina patens thatch. During cold weather active stages descended The seasonal density patterns of nymphs and into the thatch. adults of each species were monitored. Particular Neomegamelanus dorsalis (Metcalf) (Delphaci- attention was paid to the number of generations that dae), has a life history similar to D. detecta, but developed each year, the proportion of the year was a very uncommon species (Fig. 5). Overwinter- during which active stages occurred, and the over- ing nymphs matured to a small population of adults wintering stage and its location in the grass. during late May. Two larger peaks of adult density The seasonal abundance of the nymphs and adults occurred during July and Sept. Active stages were of the , D. detecta, is pictured in Fig. 5. taken during every month of the year. N. dorsalis Overwintering took place primarily as 4th or 5th also occurred primarily in the upper strata of the instars. The occurrence of 1st instars only after the grass and active stages were seldom observed within appearance of adults in spring is strong evidence or beneath the thatch horizon. Tumidagena minuta McDermott passed the winter that eggs are not present on the marsh during the as 4th instars in the thatch of SP. Although active winter months. Peaks of adult density occurred stages were collected all year, this planthopper was during May, early July and late Aug. for this tri- bivoltine, with peaks of adult abundance occurring voltine planthopper. The largest population of adults in late May and again during late July (Fig. 5). was achieved in July during the 2nd generation, Nymphal populations increased throughout the sea- although adult levels remained high until mid-Sept. son, attaining a maximum in late Oct. The genera- Nymphal populations increased throughout the grow- tions of T. minuta were far more discrete than those ing season of the grass, peaking in late Sept. Active of D. detecta, probably due to a more synchronized instars were sampled year-round. pattern of oviposition during the earlier part of Nymphs and adults of D. detecta were observed the season. to inhabit primarily the upper strata of the grass Although nymphs and adults of T. minuta occur- system consisting of seed heads and both erect and red on the upper parts of the grass, they were also matted culms and blades above the horizon of dead observed within the thatch and beneath the thatch

- 8 S. patens(·) r=.816 - - (/) L (J) 7 U (J) Lf 6 ro0- \.J)

(/) .~ U (J) Q. \.J) 2-- o

o d o z 1 o S.alterniflora (0) r = .531 o o 5 10 15 20 Live Standing Crop Biomass g dry wt.1.04m2

FIG. 2.-Relationship between sap-feeder richness and the live standing crop biomass (g dry wt./.04m2 of Spar tina altemiflora and S. patens. 364 ENVIRONMENTAL ENTOMOLOGY Vol. 6, no. 3

• • • .7 S. patens (.) r=-:578

(/') L Q) 'U Q) ~ Q. (lj If)

(" """') '-" • • (/') • (/') Q) • c c • • Q) 0 ill 0 S.alterniflora(o) 0 0 r=-.450 0 • 0 .1 0

0 0 0 o 0 0 0 0 0 0 0 0 00 5 10 15 20 Live Standing Crop Biomass g dry wt./.04m2

FIG. 3.-Relationship between the evenness (1') of sap-feeding species and the live standing crop biomass (g dry wt./.04m") of Spartina alterniflora and S. patens. associated with the new tillers sprouting from the peared in May. A. simplex was bivoltine, with peaks crown. Because of this distribution, the relative of adult density occurring in late June and Sept. population of T. minuta was probably underesti- Active stages were absent during the winter and mated. early spring months. A 4th delphacid, Megamelus lobatus Beamer, also Four leafhoppers, Destria bisignata (Sanders and occurred in SP. Unlike the already dis- DeLong), Amplicephalus simplex (Van Duzee), cussed, field observations documented that M. lobatus Hecalus lineatus (Uhler), and Paraphlepsius sp. de- remained beneath the surface of the thatch for most veloped on SP. All 4 species overwintered as eggs of its life history, surfacing only occasionally, which deposited in grass culms or blades. The seasonal explained its sporadic and rare appearance in sam- patterns of abundance for the nymphs and adults ples. The largest number of adults was taken during of 3 of these leafhoppers are shown in Fig. 6. late Oct. and Nov., but 2 other small peaks of adults D. bisignata was a rare bivoltine species with adults appeared during early July and late Aug. Except for most common during early Sept. and Nov. Both the fall generation, adult occurrence was followed by adults and nymphs were collected as late in the sea- the patchy appearance of nymphs. The absence of son as Dec. Am. simplex was the most abundant nymphs during the winter season and the appear- of the 3 leafhopper species. A single generation of ance of 1st instars during late spring suggests that nymphs first appeared in May and adults were most while M. lobatus is trivoltine, it differs in its life abundant during early July. Seasonal displacement history from the other delphacids because eggs are between Am. simplex and D. bisignata was evident. the overwintering stage. Nymphs of the rare H. lineatus were most abundant Density trends for the nymphs and adults of during June and one generation of adults appeared Aphelonema simplex (Uhler) (Issidae) are pictured in the summer months. Active stages of Am. simplex in Fig. 5. Winter was passed as eggs deposited in and H. lineatus were absent during fall, winter and the grass culms; these hatched and nymphs first ap- early spring. Paraphlepsius sp. was the rarest of the June 1977 DENNO: SAP-FEEDERS INHABITING Spartina 365

20 • • III S.patens S. alterniflora 15 (ij D. bisignata \0 -6 100,000 'S: 5 '6 .!: 10.000 1000 • Am. simplex "6 100 10 1000 5 H.lineatus 100 .0 'iii c: 10.000 0'" 10 \ODD Eriococcus n. sp. 100

'0 Dd Tm Er As AmMI Db Nd Rs HI Pa PmDd Sa Tu MI

5 Species Rank R.saucla . FIG. 4:-Annual total of individuals for each sap-feed- mg species (pooled weekly means), ranked in order of descending importance in. each gra~s type. Dd=Delpha- I A N , codes detecta, Tm=TUlmdagena mml/ta, Er=Eriococcus FIG. 6.-Seasonal distribution of the densities of n; sp., As=Aphelonema simplex, Am=Amp!icephall/s sImplex, MI=Megamelus lobatus, Db=Destria bisignata, nymphs (solid lines) and adults (dashed lines) of 5 sap-feeders inhabiting Spar/ina patens. Diamonds indi- N.d=Neomegamela~lUs dorsalis, Rs=Rhytidolomia sal/- cate adult generation peaks. Cia, H~=:=Hecalu~lmeatus, Pa=Paraphlepsius sp., Pm= Proke/lSla margmata, Sa=Sanctanus aestuaril/m Tu= Trigonotylus uhleri. ' due probably to a combination of dispersal, mor- tality, and settling deep into the grass where they leafhoppers, but a very few nymphs and adults of overwintered. Apparently, larger nymphs become this univoltine species were swept during June and active again in April when they move to the new July. grass shoots to complete development. At this time A number of species of Homoptera-Sternor- they are again retrieved in samples as evidenced by rhyncha were collected on SP, but most, because of a spring peak of nymphs prior to the appearance either their sessile or cryptic habits, were not amen- of adults. Two other coccoids inhabited SP, but were not able to sweep net sampling. Only Eriococcus n. sp. was captured. Small numbers of both adult males captured in samples. Odonaspis sp. nr. litoralis and females appeared during May, followed in early Ferris (Diaspididae) was quite common under the !une by .a large flux of crawlers that developed leaf-sheaths near the crown of the grass. Sacchari- mto 2nd mstars by July (Fig. 6). After July, the coccus n. sp. (Pseudococcidae) was uncommon, but population of nymphs in samples decreased rapidly, small, patchy, populations were encountered in the inflorescences of SP during fall. There are undoubt- edly other coccoids which occur on the salt marsh grasses . 10.000 • • One last member of the sap-feeding guild was a '000 large stink bug, Rhytidolomia saucia (Say). There was 100 one summer generation of nymphs which reached 10 a peak during the end of June (Fig. 6). Nymphs were preceded in spring and followed in fall by 10 small numbers of adults, suggesting that R. saucia N dorsalis overwinters during the adult stage, probably within ?:' • the thatch of SP. 'iii ...... '.... c: The species of sap-feeders exploiting SP can be 8'0.000 divided into several different life history categories. '000 There are "perpetual species" that are present on 100 the salt marsh as active nymphs or adults through- '0 out the year. All delphacids except M. lobatus are ASlmplex "perpetual species," and are either trivoltine (D. 1000 • • 100 detecta, and N. dorsalis) or bivoltine (T. minuta). 10 .....•.•.. -- Eriococcus n. sp. and R. saucia develop a single I 0 I N I generation during the year and overwinter as nymphs and adults, respectively. FIG. 5.-Seasonal distribution of the densities of In addition to "perpetual species," there are also nymphs (so,lid Ii~~s) and adults (dashed lines) of 4 sap-feeders mhabltmg Spartina patens. Diamonds indi- "seasonal species" that are active on the marsh for cate adult generation peaks. only a portion of the year. "Seasonal species" in 366 ENVIRONMENTAL ENTOMOLOGY Vol. 6, no. 3

SP are trivoltine (M. lobatus), bivoltine (A. simplex spring suggests that the generation of D. detecta and D. bisignata), and univoltine (Am. simplex, H. may be abortive and that SAS may be an inferior lineatus, and Paraphlepsius sp.), and undergo an host plant for development. The occurrence of extensive period of inactivity as eggs during winter. D. detecta on SAS during the cold months was the primary factor responsible for the winter increase in Assemblage of Sap-feeders Inhabiting Short-form species diversity. Spartina a1terniflora One leafhopper, Sanctanus aestuarium (DeLong The seasonal fluctuations in the densities of and Sleesman), occurred at low densities in SAS nymphs and adults of P. marginata, the dominant (Fig. 7). Two generations of adults were produced, herbivore, are shown in Fig. 7. Winter was passed one in June and a 2nd during Sept. The winter was primarily as 3rd or 4th instars beneath the loose passed as eggs, probably deposited in the dead culms lattice of dead culms, in rolled dead leaf-blades, or in of SAS. sheltered blade axils of the dead rosettes. Fifth The cryptic green mirid, Trigonotylus uhleri instars began molting to adults in early April, and (Reuter), was also bivoltine and overwintered as the 1st generation of adults reached maximum den- eggs deposited in the vegetation. First instars ap- sity in mid-May. July and Sept. peaks of adult abun- peared in May and 1st-generation adults were most dance marked the 2nd and 3rd generations. Nymphs abundant during June (Fig. 7). A 2nd peak of were present in SAS during every month of the year. adult abundance was evident in Aug. and Sept. M. lobatus occurred uncommonly in SAS as well Two coccoids occurred very infrequently on SAS, as SP. However, the external appearance of the but were not taken in samples. Haliaspis spartinae SP- and SAS- entities differed in some respect. In- (Comstock) inhabited the adaxial surface of the dividuals taken from SP were consistently smaller leaf-blades of primarily SAT, but was never observed and lighter in color than those residing in SAS. in the study area. An unusual, undescribed genus of The life history of M. lobatus in SAS was, however, Pseudococcidae was found between the leaf-sheath similar to that in SP. There were multiple genera- and culm at the crown of SAS plants. The distribu- tions, probably 3, with adults and nymphs most tion of these 2 coccoids was patchy and individuals abundant during Sept. and Oct., and overwintering could be located only after an extensive search. took place as eggs. The diversity of life history strategies possessed D. detecta, which was the dominant species in SP, by the sap-feeders inhabiting SP, is lacking in SAS. also occurred on SAS (Fig. 7). Macropterous adults P. marginata, like most of the delphacids in SP, was (most salt marsh delphacids exhibit wing-polymor- a trivoltine "perpetual species," which overwintered phism, see Denno 1976), appeared in SAS habitats as nymphs. M. lobatus was trivoltine, S. aestuarium during mid-Sept., and a small population of nymphs and T. uhleri were bivoltine and all passed the winter followed in Oct. By the following April, nymphs as eggs. Although both "perpetual" and "seasonal were absent in most samples. In May, at which time species" occurred in SAS, there was a notable the spring generation of adults peaked in SP, residual absence of univoltine sap-feeders. numbers of predominantly macropterous adults oc- curred in SAS. D. detecta was absent from most Effect of Thatch Removal on the Herbivore Fauna summer samples. The near absence of adults in of Spartina patens Seasonal changes in the amount of thatch and standing crop of living grass were measured in the unclipped control and dethatched plots (Fig. 8). 10,000 • • • P marginata From March-July there was a gradual decrease in 1000 the biomass of dead thatch on the unclipped plot. 100 ._------"" Very little thatch remained after clipping on either 10 experimental plot and, as the season progressed, there was no evidence that plant debris was trans- • • • D. detecta 100 ported onto the dethatched plots by tides or winds.

10 Green shoots had not yet appeared in any of the £ ,--- .•. ,. '.. c: plots by March. By June, considerable growth had QJ'" 0 15 • occurred, but the biomass of living vegetation was 10 significantly larger in the unclipped plot compa~ed to 5 the thatch-free areas. During July, when maximum

10 live standing crop occurs for SP, the live biomass sampled on one of the clipped plots was not signifi- 5 cantly different from that found on the unclipped plot. However, the avg live standing crop of grass on the 2nd thatch-free plot was lower than that recorded for the other 2 plots. This was not a FIG. 7.-Seasonal distribution of the densities of generalized vegetational response, but was attribut- nymphs (solid lines) and adults (dashed line~) of 4 sap-feeders inhabiting Spartina alterniflora. Diamonds able to a low area in the center of the plot where indicate adult generation peaks. grass growth was thin and patchy, resulting in a June 1977 DENNO: SAP-FEEDERS INHABITING Spartina 367

values of species diversity in the clipped plots were Dead Thatch Living Plants 90 primarily due to decreases in species evenness (I') 20 (Fig. 9). Both species diversity and evenness de- N clined throughout the season, when in Sept. values E I"- ,A,I near 0.0 were attained. <;f , I 60 , I 0 D. detecta had significantly higher densities of -.: +---1\\'1 /C1 I 2nd-generation nymphs during July and 3rd-genera- Ot IY I I U1 10 I tion adults in Aug. on both dethatched grass plots C I QJ 30 I " --I compared to the unclipped area (Fig. 10). There 1i1 I ,/r1"<::2' a. I , , were no consistent differences in the densities of I , lIi either adults or nymphs of D. detecta among the c, U ,/ ,,/ ,,/ I ' , plots on any of the remaining sampling periods. I-!-,' 0 0 I:i'------:£.,[ ./ 0 0 . .~ Similarly, N. dorsalis produced larger populations of C2 2nd-generation nymphs in Aug. and 2nd-, and 3rd- March June July March June July generation adults during July and Sept. on the de- FIG. 8.-Live and dead standing crop biomass of thatched grass plots (Fig. 10). Sparlina patens (g dry wt./.047m') sampled during While some of the sap-feeders increased their March, June, and July in both dethatched plots (el and C.) and the unclipped plot with thatch (U). One stan- populations during at least part of the year on de- dard error surrounds the means for dead standing crop. thatched grass, other species were adversely affected. LSls for living grass as in Fig. ]. Populations of 1st-, and 2nd-generation adults of T. minuta during June and July, respectively, and 1st-, and 2nd-generation nymphs during July and reduced avg standing crop figure during July. The Sept., respectively, were significantly smaller on patchiness of grass standing crop in this clipped dethatched grass than on grass with thatch (Fig. 11). plot was evidenced by a coefficient of variation of Very few nymphs or adults of A. simplex were 54.5%, compared to 33.2% and 29.6% calculated ever swept in either dethatched plot during the for the other dethatched plot and uncIipped plot, sample periods (Fig. 11). A. simplex overwinters as respectively. When sweep-netting insects, this thin eggs in the dead grass culms, and it was not surpris- area was avoided whenever possible. ing to find low densities of 1st-generation nymphs On each of the 4 sampling dates, the species and adults during June in the clipped areas, but this diversity (H') of sap-feeding insects was significantly condition also prevailed through the 2nd generation lower in plots where the thatch was removed (July and Aug.), implying that adults avoided the (F:), 48 = 127.76; P « .001) (Fig. 9). Depressed colonization of dethatched areas entirely.

11= Thatch Sap Feeders B= Clipped1 (Jl ~ "0 I 8= Clipped2 (1) I 1.5 n (1)' ~ .v) I • (fI L • .6m ~ < (1) (:) 1.0 G ::J V) El • ::J Q) • B • (1) 'u B • (fI • • .3 (fI 2i.5 • BG • • I • • L lI) Btl • B ~ BEl Btl a Sa 0 - 0 June July Aug. Sept. June July Aug. Sept. FIG. 9.-Species diversity (H') and evenness (1') of sap-feeding species measured during June, July, Aug., and Sept. in the control plot with thatch and both dethatched plots. LSls as in Fig. L 368 ENVIRONMENTAL ENTOMOLOGY Vol. 6, no. 3 B D. detecta adults 3000 nymphs 900 G EJ 2000 600 a B • 1000 188 300 G • =88 • IGG P =88 • la. (/) 0 • c Q) N.dorsalis nymphs adults 0 15 15 ~

10 10 B 5 5 ~ 0 88 I I 0 I June July Aug. Sept. June July Aug. Sept.

FIG. lO.-Densities of the nymphs and adults of Delphacodes detecta and Neomegamelanus dorsalis measured during June, July, Aug., and Sept. in the control plot with thatch and both dethatched plots. LSls as in Fig. I. Plot legend as in Fig. 9.

The cicadellid, Am. simplex, also overwintered as nymphs produced by 2nd-generation adults. By the eggs in the dead grass culms, which were removed end of the season, either the number of offspring with dethatching, resulting in significantly smaller produced by 3rd-generation adults or the number populations of 1st-generation nymphs during June of offspring surviving was significantly lower on in the thatchless grass plots compared to the un- grass without a thatch. The success of the offspring clipped area (Fig. 11). However, during July and of both 1st-, and 2nd-generation adults of T. minuta Aug., there were no significant differences in the was significantly poorer in dethatched grass than density of adults among the plots, suggesting that grass with thatch. It is unlikely that reduced adults freely recolonized the clipped area. density on dethatched grass was the result of emigra- The relatively low sap-feeder diversity and even- tion because delphacid nymphs, especially early in- ness values recorded on dethatched grass were due stars, are extremely sessile (Lindsten 1961, Raati- to increases in the population size of D. detecta kainen 1967). and/or reduced densities of T. minuta, A. simplex Predators and Parasites and Am. simplex. Indices of success (SI) were calculated at 3 and 2 In order to dismiss the possibility that predation time periods respectively for populations of D. de- was more severe on dethatched grass than grass with tecta and T. minuta occurring on both dethatched thatch, resulting in smaller populations of T. minuta grass plots and the unclipped control (Fig. 12). The and A. simplex, I examined the densities of predators offspring of 1st-generation adults of D. detecta were and parasites swept from all plots. Wolf spiders more successful on dethatched grass compared to (Lycosidae) were by far the most abundant predators SP having a thatch. However, there was no signifi- collected in SP. Mirid bugs in the genus Tytthus, cant difference among the plots in the success of the known egg predators of Homoptera, also occurred June 1977 DENNO: SAP-FEEDERS INHABITING Spartina 369

sporadically in samples. An analysis of variance in the genus Pseudogonatopus, which devefops pri- performed on the pooled densities of these predators marily on the nymphs of delphacids, were occasional- found no significant differences among the 3 plots ly swept from SP. Fluxes in the population density of a particular parasite, which is presumably special- (F2 48 = 3.02, P > .05). Had there been a main plot effect, it is unlikely that a general feeding preda- ized in its feeding habit, could account for the re- tor, like a lycosid spider, could account for the duced population levels of Homoptera recorded on selective demise of the populations of T. minuta and the dethatched grass. However, all of the above A. simplex on dethatched SP, while the population parasites were uncommon «5 individuals/sample) size of D. detecta remained large (Aug. and Sept. and there were no apparent differences in the den- of Fig. 10 and 11). sities of these insects between dethatched and un- Chrysopophagous nr. american us (Perkins), an clipped plots. Therefore, it is unlikely that the dif- encyrtid wasp which develops on Cicadellidae, 2 ferences in the responses of the various homopterans mymarid wasps, Polynema sp. and Gonatocerus sp., to dethatching are attributable to either predation parasites of the eggs of Homoptera, and a dryinid or parasitism.

200 Am. simplex nymphs adults • 10 100 I~~ 5 EI Abs. Abs. Abs. Abs. I~ Abs. T minuta nymphs adults 900 • 600 • ~ • l/) • c B <1.> 0 300 B B I B B B IB 0 • A.simplex nymphs adults • • 40 • • 20 • I • o June July Aug. June July Aug. Sept. FIG. It.-Densities of the nymphs and adults of Amplicephalus simplex, Tumidagena minuta, and Aphelonema simplex measured during June, July, Aug., and Sept. in the control plot with thatch and both dethatched plots. LSls as in Fig. 1. Plot legend as in Fig. 9. Abs=Absent. 370 ENVIRONMENTALENTOMOLOGY Vol. 6, no. 3

D. detecta T minuta (/)150 (/) 7~ I 3- § 4- 2 . ::J - If) 100 5- I • - 3- • .2- -0 X ~ 3- 1 C1> 50 I 1:J 2- .1- c I 1- BE] I ~~ J/Jn A/J S/A J/Jn S/J d FIG. 12:-In~ices of success calcu.lated at 3 and 2 time intervals, respectively, for Delphacodes detecta and Tumi- ageJna mlnJuta ill the control plot With thatch and both dethatched plots. LSls as in Fig. 1. Plot legend as in Fig 9 Jn= une, =July, A=Aug. S=Sept. . .

Discussion explain the differences in sap-feeder diversity be- tween SP and SAS habitats. First, few species may The data show that SP houses a much more com- be able to adapt to habitats that are rigorous and plex community of sa{rfeeding insects than does SAS. The species richness, diversity (H'), and even- continuously subjected to stress (Sanders 1968, Mac- Arthur 1972). However, the elevational difference ness (1') are higher, and there is a larger variety of between the sites occupied by SP and SAS is slight, life history strategies possessed by the sap-feeders on and although SAS incurs flooding at a greater fre- SP. An obvious trend toward the reduction of the quency and for a longer duration, neither habitat number of generations produced each year by some is com~letely inundated except by high spring or of the sa{rfeeders is evident in SP that is not char- acteristic of SAS-inhabiting species. Univoltine leaf- ~torm tides. Cameron (1976), taking samples dur- mg and after flooding, showed that periodic tidal hoppers (Am. simplex, H. lineatus, and Paraphlepsius inundation had little effect on the number of species sp) and .Hemiptera (R. saucia) occur only on SP, or the structure of the insect community in general. whIle their counterparts on SAS (S. aestuarium and Ne~ertheless, it is not the normal regime of tides T. uhleri) are bivoltine. Only trivoltine fulgoroids which seems potentially destructive to the insect occur on SAS, while the fulgoroid fauna of SP i?habitants, but the intense pounding action of storm consists of both bi- and trivoltine species. The tides and waves, and it is likely that in SAS habitats d~min.ant herbivore in both grasses is a "perpetual," where plant distribution is diffuse and thatch is tnvoltme delphacid; D. detecta in SP and P. mar- ~ca~ty that insect mortality during such catastrophies ginatq in SAS. IS high. The dense thatch found in SP may buffer ~arious hypotheses have been suggested to ex- the action of storms and confer greater reliability plam discrepancies in the richness or diversity of to the resource, allowing for the coexistence of more the insect community on different plant species. sap-feeding species. Davis and Gray (1966) reasoned Plants with certain physical or biochemical char- similarly when they concluded that Distichlis (a salt acteristics are known to prevent or dissuade feeding marsh grass similar in structure to SP) sustains a by many insects and subsequently house a very larger insect fauna than SA because it provides for specialized community of herbivorous insects (Tan- greater protection from physical factors. ton 1962, Agarwal 1964, Pathak 1969, Feeny 1970, MacArthur (1972) has suggested that there are 1975, Caswell et al. 1973, Southwood 1973, Root more species where the environment is complex and 1975). However, from what evidence exists, there therefore more readily subdivided. SP, with its dense are no blatant differences in the nutritional quality, enta~glement of living and dead plant parts, certainly scheme of carbon-fixation, or leaf microstructure prOVides a greater diversity of microhabitats, which between SP and SAS that would explain the dis- co~ld ~ of potent.ia.l use to sap-feeders for feeding, crepancies in the guilds of sap-feeders on these two OVipOSition,and hldmg. As grass biomass increases grasses (Caswell et al. 1973, Anderson 1974, de la to a maximum during the summer, there is a com- Cruz and Poe 1975). mensurate increase in structural diversity (Blum Two alternatives seem possible when attempting to 1968). This is especially true in SP after leaf-blade June 1977 DENNO: SAP-FEEDERS INHABITING Spartina 371 and culm prostration takes place. As plant structural nymph, resource utilization can begin as soon as diversity increases, the coexistence of additional sap- suitable conditions for development occur. Com- feeder species, which specialize on the various plant- pared to "perpetual species," "seasonal species" parts, is allowed, probably explaining the positive which occur actively for only a few months during correlation between herbivore richness and grass the year (e.g., the univoltine homopterans Am. sim- biomass. Cameron (1972) also surmised that the plex and H. lineatus) are relatively specialized in summer increase in the vegetational diversity of Spar- their use of resources along a seasonal time con- tina toliosa Trin. was primarily responsible for the tinuum, and relinquish, in part, the potential for packing of additional species of phytophagous in- high rates of population increase. sects onto this Pacific Coast salt marsh grass. The particular strategy of a species is ultimately When the structural complexity of SP was reduced determined by the reliability of its resources (South- by removing thatch, the diversity of sap-feeders de- wood et al. 1974). Where host-plant resources are creased. This was primarily due to increases in the unreliable, that is small, poor in quality, ephemeral, populations of D. detecta and/or population de- or occur in rigorous habitats, a generalized strategy creases of T. minuta, A. simplex and Am. simplex. on the part of exploiting insects is usually favored. Following winter dethatching, spring nymphal popu- As the reliability of the resource base increases, lations of A. simplex and Am. simplex were small, selection should favor the efficient use of that re- suggesting that the persistent mat of dead SP culms source with the development of a specialized utiliza- provides a reliable overwintering site for eggs and tion strategy (Pianka 1970, Southwood et al. 1974). encourages the residence of "seasonal species." SAS, If SP is more reliable than SAS, one might expect which forms only a loose, lattice-work of dead culms, to find more specialized sap-feeders there. Even houses fewer "seasonal species," none of which be- though both grasses were dominated by "perpetual comes very abundant (e.g., S. aestuarium and T. species," with apparently high reproductive capa- uhleri) . cities, univoltine seasonal specialists occurred only Indices of success were significantly lower for in SP. There was a common tendency for these T. minuta on dethatched grass compared to SP with univoltine species to develop as nymphs during May thatch, indicating either the relative failure of both and June. This is probably the result of selection Ist-, and 2nd-generation adults to find suitable ovi- pressures which synchronize feeding and develop- position sites or the reduced survival of their eggs ment with optimum resource conditions. Optimum or nymphs. D. detecta showed a somewhat different conditions for SP occur during May and June when response to dethatching. Proportionately larger num- the grass is nearing maximum productivity and still bers of offspring were either left by 1st-generation very fresh, not having deteriorated due to natural adults or survived on dethatched SP during early senescence or feeding and oviposition by the bi-or summer, but by fall, this pattern changed and the trivoltine species which reach maximum population offspring of 3rd-generation adults were proportion- densities later in the season. ately more successful on grass with thatch. The re- When the natural structure of the SP habitat was duced success of D. detecta on dethatched grass is altered by removing thatch, population increases probably attributable to characteristics of the senesc- were observed only for the trivoltine, "perpetual ing host-plant or physical mortality factors which species," D. detecta and N. dorsalis, presumably be- take a greater toll on the nymphs at the end of the cause of their opportunistic strategies. "Seasonal season on the exposed grass. The lack of consistent species" and "perpetual species" with fewer annual differences in the densities of predators, especially generations (T. minuta), having specific feeding, spiders, between dethatched and natural grass sug- oviposition, and substrate requirements, which were gests that predation is probably not responsible for altered or destroyed with dethatching, showed popu- the reduced success of D. detecta on dethatched lation decreases. grass during fall. All empirical and experimental evidence supports When SP is dethatched, the portion of the living the contention that the complex microstructure and grass system once contained within and beneath the dense thatch of SP combine to form a more hetero- thatch becomes readily accessible and it is not sur- geneous and less rigorous resource which subsequent- prising to find population increases in those species ly supports a more diverse and specialized assem- (D. detecta and N. dorsalis) which occupy the upper blage of sap-feeding insects than SAS. plant strata. Likewise, dethatching destroys those microhabitats contained in and below the thatch, Acknowledgment and subsequently, populations of T. minuta which I thank B. D. Denno for processing the many partially reside in the thatch horizon were reduced. samples, P. Barbosa and K. V. Yeargan for helpful "Perpetual species," which are present as active comments on the manuscript, E. E. Grissell (Florida forms year-round, must necessarily be adapted to a Deprtment of Agriculture and Consumer Services), broad set of changing biotic and physical conditions J. L. Herring, J. P. Kramer, A. S. Menke, and D. R. when occurring in a temperate region. Advantages Miller (Systematic Entomology Laboratory, IIBIII, to producing multiple generations each year and ARS, USDA) for determining the various species of being "perpetual" lie with the potential for high sap-feeders, predators, and parasites, and C. Varnum rates of population increase. By overwintering as a for typing the final manuscript. 372 ENVIRONMENTAL ENTOMOLOGY Vol. 6, no. 3

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