Benefits of Dispersal in Patchy Environments: Mate Location by Males of a Wing-Dimorphic

Gail A. Langellotto; Robert F. Denno

Ecology, Vol. 82, No. 7. (Jul., 2001), pp. 1870-1878.

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http://www.jstor.org Wed Apr 25 10:28:23 2007 Ecology, 82(7), 2001, pp. 1870-1878 0 2001 by the Ecological Society of America

BENEFITS OF DISPERSAL IN PATCHY ENVIRONMENTS: MATE LOCATION BY MALES OF A WING-DIMORPHIC INSECT

GAILA. LANGELLOTTOAND ROBERTF. DENNO Depar-tment of Entomology, Unzversi~of Ma~ylanrl.College Park, Ma~ylancl20742 USA

Abstract. Dispersal dimorphisms, in which both flight-capable and flightless adults occur in the same species, are commonplace in . Such dimorphisms are seen as reflecting a balance between the benefits and costs of flight and wing reduction or loss. In heterogeneous habitats, theory predicts that fitness trade-offs can favor the evolution of a dispersal dimorphism in which both flight-capable and flightless morphs are retained in the same population. Despite the wealth of theory, howevel; there has never been an explicit field assessment of how habitat heterogeneity directly influences the reproductive success of the flight-capable and flightless wing forms of an insect species. The objective of this research was to investigate how variation in habitat heterogeneity (vegetation structure) and female density influence mate location and thus the potential for reproductive success by the male wing forms of a salt marsh inhabiting insect, the planthop- per Prokelisia dolus. By placing unmated females in the field at different densities and in sparse and contiguous vegetation, we were able to compare the ability of male wing forms to locate stationary mates. Our data show that both vegetation structure and female density differentially influenced the ability of the male wing forms to locate mates. Flight-capable males located females and acquired matings far more frequently in sparse vegetation, whereas flightless males discovered females more often in contiguous vegetation. Flight-capable males located fe- males more effectively at low female densities, whereas flightless males discovered females more efficiently at higher female densities. Thus, natural variation in vegetation structure and female density are two important factors which combine to influence the mating success of each male wing form. We conclude that habitat heterogeneity in concert with the known reproductive penalties imposed by flight capability (reduced siring ability) interact to favor the persistence of the dispersal polymorphism in males of this species. Key words: clispersal; ,flightlessness; rnate location; plcrntizopper; Prokelisia dolus; trade-off between jight capability ancl reproclzccrion; wing polymorphism.

INTRODUCTION risk of mortality associated with the flight process itself Dispersal by flight is considered essential for the @off 1984, 1990, Zera 1984, Denno et al. 1989, Denno success of insects exploiting transient habitats (South- and 1990, Roff and 1991, Wagner wood 1977, Harrison 1980, Roff 1990, Denno et al, and Liebherr 1992). Such energetic costs are frequently 1991, 1996, Roff and Fairbairn 199 Zera and Denno imposed on reproduction, and are most easily assessed 1997). a is also to facil- in wing-dimorphic insects which occur as both flight- itate the search for mates, scattered food resources, and and (Roff 1984, Denno et ". 1989, 1991). In females of wing-dimorphic crickets, optimal oviposition sites ( D et al,~ 19g1,~ ~ ~and f ~ f Fairbairn 1991, Wagner and Liebherr 1992, Denno seed bugs, and , for flight- 1994,~).In theory, dispersal can have a strong stabi. wing form often exhibits reduced lizing influence on local population fluctuations, and it extended age to first re~roduction,or reduced offspring is viewed as a central process in metapopulation dy- size compared to the flightless morph (Roff 1986, Sol- namics (den B~~~ 1981, ~~~l~~1990, ~~~~~~~i~~1995, heck 1986, Denno et al. 1989, Roff and Fairbairn 1991, Denno and Peterson 1995, Hanski and Kuussaari 1995). and 1997). *lthough it has proved M ~ dispersal~ also directly~ influences~ ~ gene flow~ difficult~ to demonstrate,, a growing body of literature and the genetic structure of populations (Pashley et al. Suggeststhat too pay the price abil- 1985, Preziosi and Fairbairn 1992, Peterson and Denno ity (Zera and Denno 1997, Langellotto et al. 2000). For 1997, 1998). instance, flight-capable males of a variety of insect taxa ~ i ~however,~ ~does ~not occur~ ~ withoutl costs,, are less aggressive in male-male interactions (Ichikawa costs such as the inherent expense of wings and flight 1982), (NovOtn~1995), repr0- muscles as well as the direct energetic penalties and ductively mature later in life (Utida 1972, Fujisaki 1992), attract fewer females and acquire fewer matings Manuscript received 23 June 2000; accepted 6 July 2000; final (Cres~i1988, Kaitala and Dingle 1993, Crnokrak and version received 1 August 2000. Roff 1995, 2000, Novotny 1995, Langellotto et al. 1870 July 2001 MATE LOCATION BY MALE PLANTHOPPERS 1871

2000), or sire fewer offspring (Langellotto et al. 2000) is probably essential for males to move among plants than their flightless counterparts. Thus, there is wide- in search of calling females (see Ichikawa and Ishii spread evidence for a trade-off such that dispersal abil- 1974, Hunt and Nault 1991). Third, confined on a single ity constrains reproduction and vice versa (Roff and host plant in a rival-male setting, flightless males own Fairbairn 1991, Zera and Denno 1997). a mating advantage over macropterous males because When the demands for flight relax, reduced dispersal they acquire most of the matings (Langellotto et al. capability or the loss of wings altogether can result 2000). Moreover, a trade-off between reproduction and (Roff 1990, Denno et al. 1991, 1996, Denno 1994~). dispersal capability has been demonstrated for male Most frequently, flightlessness or reduced dispersal planthoppers (Novotny 1995, Langellotto et al. 2000). ability is observed in insects which occupy persistent In P. dolus, brachypterous males sire twice as many habitats (Roff 1990, Denno et al. 1991, 1996, Denno offspring as macropterous males when females are 1994b, Zera and Denno 1997). In heterogeneous hab- abundant (Langellotto et al. 2000). What remains un- itats, however, theory predicts that fitness trade-offs known is how habitat heterogeneity and female density may favor the evolution of a dispersal dimorphism in might directly influence the mating success of the male which both flight-capable and flightless morphs occur wing forms, and in particular what environmental pa- in the same population (Harrison 1980, Roff 1984, rameters might favor flight-capable males in acquiring 1986, 1996, Denno et al. 1991, Roff and Fairbairn mates. Specifically, we hypothesize that flight-capable 1991, Denno 1994b, Ott 1994). Such dimorphisms are males will locate mates more effectively than flightless commonplace in the insects (Harrison 1980, Zera 1984, males in noncontiguous vegetation and when females Roff 1986, Denno et al. 1989, Roff and Fairbairn 1991, are rare. By comparing the ability of the male wing Zera and Denno 1997), and are seen as reflecting a forms to locate females under variable conditions, we balance between the costs and benefits of flight capa- seek to elucidate the benefits of dispersal in patchy bility and wing reduction (Fairbairn 1988, Denno et al. habitats. Such information is essential for understand- 1991, Roff 1996). Moreover, the observed frequency ing the selective forces associated with habitat hetero- of the flight-capable morph in the population is thought geneity that favor the persistence of flight polymor- to reflect the strength of selection for dispersal (Roff phism~. 1984, 1986, Fairbairn 1988, Denno et al. 1991, 1996). NATURALHISTORYOF STUDYORGANISMS Although the reproductive penalties associated with Planthopper population biology and plant flight are well documented in wing-dimorphic insects, heterogeneity there has never been an explicit field assessment of the benefits of dispersal in the context of mate location in Prokelisia dolus is an abundant sap-feeding herbi- heterogeneous habitats. vore (densities up to 1000 adults/m2) on the intertidal The objective of this research was to investigate how marshes along the Atlantic and Gulf Coasts of the Unit- variation in habitat heterogeneity (vegetation structure) ed States, where it feeds in the phloem of the perennial and female density influence mate location and thus grass, Spartinn alternijora (Denno et al. 1996). Al- though population densities of this multivoltine plant- the potential for reproductive success by the male wing hopper can be high, they also fluctuate dramatically forms of the salt marsh-inhabiting planthopper, Pro- kelisia dolus (: ). We selected (Denno and Roderick 1992, Denno et al. 1996). P. dolus occurs primarily in meadow and panne (mud the male sex to study, because only males actively dis- flat) habitats on the high Spnrtina marsh (Denno et al. perse in search of mates in planthoppers (Claridge 1996). Here, Spartina grows in extensive pure stands, 1985, Heady and Denno 1991, Heady 1993). Several but its structure varies tremendously (Adams 1963, characteristics of planthoppers suggest that vegetation Redfield 1972). Meadow vegetation is composed of a structure and female density might influence mate lo- dense bed (up to 3000 stems/m2) of entangled short cation of the male wing forms of these sap-feeding rosettes 10-40 cm in height (Blum 1968, Denno and herbivorous insects. First, flight-capable (macropter- Grissell 1979, Dobel et al. 1990; Fig. 1A). Within the ous) and flightless (brachypterous) males differ dra- Spartina meadows are mud pannes, on which. short- matically in their ability to move within and between form Spnrtina plants grow at a much lower density habitats, with macropters able to disperse over much (Redfield 1972, Dobel et al. 1990; Fig. 1B). Conse- larger distances (Denno et al. 1989, Denno 1994n). quently, P. dolus inhabits two structurally discrepant Second, vegetation structure is intimately linked to vegetation types, the contiguous meadow vegetation mate location in planthoppers because the sexes com- comprised of a dense entanglement of interdigitating municate acoustically via plant substrate-borne vibra- stems and blades, and the non contiguous panne habitat tions whereby males move to locate stationary, calling with sparsely growing plants which frequently do not females (Claridge 1985, Heady and Denno 1991, Heady touch (Redfield 1972), 1993). Both sexes can detect each other from distances up to 1 m, but only if the vegetation remains in physical Planthopper nzobility and wing ,form deternzination contact between the calling individuals (Ichikawa and Populations of Prokelisia dolus are composed of both Ishii 1974). Thus, in noncontiguous vegetation, flight flight-capable macropters and flightless brachypters GAIL A. LANGELLOTTO AND ROBERT F. DENNO Ecology, Vol. 82, No. 7

FIG. 1. Prokelisia dolus inhabits two structurally different Spurtinn habitat types: (A)contiguous meadow vegetation composed of a dense entanglement of interdigitating stems and blades, and (B) noncontiguous mud panne vegetation consisting of sparsely growing plants that frequently do not touch with reduced wings (Denno 1994~).On average, 8- neighboring but slightly separated plants do not detect 36% of adults are macropterous in Atlantic coast pop- each other's presence (Ichikawa and Ishii 1974, Ichi- ulations (Denno et al. 1996). Macropters and brachyp- kawa 1976). ters differ dramatically in their ability to move within Although the attraction signals produced by plant- and between habitats with macropters able to disperse hoppers are species specific, there is no difference in over much larger distances (Denno et al. 1989, Denno call structure between the wing forms of either sex in 1994~). P. dolus or for any other planthopper studied (Ichikawa Wing form in all dimorphic planthoppers studied and Ishii 1974, Ichikawa 1976, Claridge 1985, Heady thus far is determined by a developmental switch which and Denno 1991). Sexually mature males and virgin responds to environmental cues (Denno and Roderick females call spontaneously on their food plants. After 1990, Denno et al. 1991). However, the sensitivity of sensing each other, they begin to alternate calls in a the switch to cues is heritable and under polygenic duetting fashion (Ichikawa and Ishii 1974, Ichikawa control (Denno and Roderick 1990, Denno et al. 1991, 1976, Claridge 1985, Heady and Denno 1991). During Denno 1994~).For P. dolus, the production of mac- duetting, males move toward stationary females, and ropterous forms is density dependent in both sexes and after locating a female, courtship ensues followed by is associated with crowded conditions (Denno et al. mating (Ichikawa and Ishii 1974, Ichikawa 1976, 1991, 1996). Heady and Denno 1991). Planthopper mating system and acoustical communication Study sites In Prokelisia dolus, as in all planthopper species, acoustic communication is essential for locating mates The ability of the male wing forms of Prokelisia (Claridge 1985, Denno et al. 1991, Heady and Denno dolus to locate females was studied in the field on mid- 1991, Heady 1993). Both males and females commu- Atlantic salt marshes located at Elliott Island (Dorches- nicate through substrate-transmitted vibrations, where- ter County, Maryland), Wallops Island (Accomack by calls are produced by vibrating their abdomens County, Virginia), and Tuckerton (Ocean County, New (Claridge 1985).Vibrations are transferred to the host Jersey). These marshes consist of large expanses of plant through the legs or mouthparts (Claridge 1985). short-form Spartina alternijlora growing in both mead- Planthoppers sitting on the same host plant or on ad- ow and salt panne habitats. The stem density (number/ jacent plants in physical contact can sense each other's m2)of Spartina in our experimental meadow and panne calls from as far away as I m (Ichikawa and Ishii 1974, habitats was 418 t- 80 and 105 i- 24 respectively (mean Ichikawa 1976). However, planthoppers sitting on 5 1 SE). July 2001 MATE LOCATION BY MALE PLANTHOPPERS 1873

Mating success of nzale wing forms in contiguous vegetation) and study site (Wallops Island and Elliott and norzcontiguous vegetation Island) on the proportion of macropterous males in the population (macropterous maleslmacropterous males + To compare the ability of ambient male wing forms brachypterous males) was assessed using ANOVA of Prokelisia dolus to locate females and secure mat- (SAS 1990). Proportions were angular transformed pri- ing~in both meadow (contiguous vegetation) and panne or to analysis. A Fisher's exact test on counts was used habitats (noncontiguous vegetation), an experiment to test if the observed number of each male wing form was conducted on the high marsh near mean high water acquiring the mating (I) differed between contiguous level. Virgin female brachypters (4-5 d old) were and noncontiguous habitats, and (2) differed from an placed in both habitat types by clip-caging them in- expected frequency based on the relative density (num- dividually onto selected Spartina plants. Cages were ber of individualslm2) of each male wing form in a made by fixing a section of clear plastic tubing (2 cm habitat (SAS 1990). long and 1.5 cm in diameter topped with organdy gauze) to the top half of a hair clip. The lower half of Mate location by male wing forms at diferent the clip was fitted with a foam rubber disk (1.5 cm in female densities diameter) that sealed the cage when clipped shut over The ability of the two male wing forms to locate a leaf blade (see Langellotto 1997). Caged females females under different density conditions was tested were placed 1 m apart in the field by clipping the cages experimentally in the field at Tuckerton and Elliott Is- onto plants in the noncontiguous habitat and onto plants land. Individual virgin females (brachypters) were of similar size in the contiguous habitat. All females caged in the field at three relative densities (low, me- were set in place between 1000 and 1100 EDT. Prior dium, and high) in meadows of Spartina on the high to the placement of experimental females in the field, marsh. The three female density treatments were all resident planthoppers were removed (aspirator) achieved by placing three sizes of plastic rings (0.25 within 15 cm of the clip-caged females. In all, 19 fe- m2, 0.5 m2, and 1.0 m2) into the field in a triangular males were placed into each habitat type at Wallops arrangement with a 2 m spacing distance. Rings were Island on 4 August 1995 and another five females were constructed of 1 cm diameter PVC pipe. Before placing positioned in each habitat at Elliott Island on 16 July female planthoppers around the rings, the area (5 m 1996. surrounding the three-ring set up) was thoroughly vac- One day prior to placement in the field, all females uumed (D-vac insect vacuum) to remove resident plant- were marked with orange florescent powder (BioQuip, hoppers. Subsequently, eight virgin females were clip Gardena, California, USA) so that they could be dis- caged onto a Spartina leaf equidistantly around the tinguished from any resident females which colonized perimeter of each ring. In addition, 10 marked males the local area. After 5-7 min of settling time, clip cages (orange florescent powder, BioQuip) of each wing form were removed and ambient males (both wing forms) (2-3 d old) were caged over Spartina at the center of were allowed access to the released females. The wing each ring. The density of 20 marked males caged over form of the resident male which located and success- two or three Spartina stems in the center of each ring fully mated with the experimental female was recorded. represented a relatively low planthopper density (Den- To assess matings, all females were checked in 5-min no and Roderick 1992). Thus, there should be a rela- intervals between 1000 and 1400 EDT. Of the 24 fe- tively small effect of release density on male dispersal males placed into each habitat, 15 were mated in the in this experiment. contiguous habitat and 12 were mated in the noncon- Using the three ring-size treatments, we were able tiguous habitat. to establish three different female densities. The small- At each location (Wallops Island and Elliott Island) est ring represented a high-density situation, within and on the same date as the experiment was conducted, which males did not have to travel far (28.3 cm) to ambient wing form densities (number of individuals1 reach tethered females. In contrast, the largest ring rep- m2) were also assessed by sampling each habitat type resented a low density situation, where males had to near the experimental area with a D-vac suction sam- travel much further (56.4 cm) to locate the caged fe- pler (Rincon-Vitova Insectaries, Ventura, California; males. These three treatments (low, medium, and high) see Denno et al. 1985). In all, seven samples were taken converted into absolute densities of 4, 8, and 16 fe- in each habitat type at Wallops Island on 4 August maleslm2 respectively. 1995, and five samples were taken per habitat on 16 Males were given -15 min to settle on the Spartina July 1996 at Elliott Island. One sample consisted of before the release cage was removed at 1000 EDT. eight, 10-s placements of the D-vac head over Spartina Following cage removal, rings were checked every 5 vegetation. These data were taken so that the observed min during a 4-h period for any marked male which mating success of the male wing forms could be com- arrived to court the caged females. The following data pared with their expected mating success based on their were recorded: (1) the number and wing form of all relative abundance in each habitat in the field. The arriving males, and (2) the number of different females effect of habitat type (contiguous vs. noncontiguous each individual male approached and courted. Four full 1874 GAIL A. LANGELLOTTO AND ROBERT F. DENNO Ecology, Vol. 82, No. 7

TABLE1. Density (number of individuals/mz) and propor- erated by averaging the abundances of the male wing tional abundance (brachypters/[brachypters + macropters]) of the brachypterous and macropterous males of Prokelisia forms from Wallops Island and Elliott Island. rlolus in contiguous (meadow habitat) and noncontiguous Macropterous males located females and secured (mud panne habitat) Spartiflu at Wallops Island, Virginia, matings much more frequently than brachypterous USA, on 4 August 1995, and Elliott Island, Maryland, males in the noncontiguous panne habitat, where they USA, on 16 July 1996. obtained 10 of the 12 observed matings (83%). By Number of Number of contrast, the reverse situation occurred in the contig- brachyp- macrop- Proportion of uous meadow habitat where macropterous males ob- terous terous brachypterous tained none of the 15 qbserved matings (0%). This Location males/m2 males/m2 males result occurred in spite of the fact that several mac- Contiguous Spartino (meadow habitat) ropterous males were seen to visit plants on which Maryland 83 i 12 33 t 5 0.71 t 0.10 experimental females were placed. Overall, the fre- Virginia 36 ? 13 20 5 6 0.64 5 0.22 Grand mean 55 t 11 25 ? 4 0.69 + 0.14 quency of male wing forms which obtained matings Noncontiguous Spartincl (mud panne habitat) differed significantly between meadow and panne hab- Maryland 31 i- 8 23 i 5 0.57 i- 0.15 itats (Fisher's exact test, P < 0.001). Virginia 17 5 6 16 i 7 0.52 i 0.18 The mating success of each male wing form could Grand mean 23 i 5 19 i 5 0.55 ? 0.12 not be explained by its relative abundance in the hab- Note: Values are means i 1 SE. itat. For example, macropterous males obtained 83% of the matings in the noncontiguous habitat even though they were relatively less frequent in this area replicates (three female density treatments each) were (45% of all males, 19/m2) than brachypterous males placed in the field at Tuckerton on 20 July, 3 August, (23/m2). The observed mating frequencies of the two 21 August, and 7 September 1996. wing forms in the noncontiguous panne habitat differed Categorical data analysis of counts (summed across significantly from expectations based on their relative replicates) was used to test if the observed frequency abundance (Fisher's exact test, P = 0.024; Fig. 2A). of arrivals of the two male wing forms to unmated Similarly, the observed mating frequencies of the females differed across the three female-density treat- two wing forms in the meadow habitat differed sig- ments (CATMOD procedure, SAS 1990). An assump- nificantly from expectations based on their relative tion of this analysis is that observations (courtings) are abundance (Fisher's exact test, P = 0.009; Fig. 2B). independent occurrences. Although a few males were Macropterous males acquired no matings in the mead- observed courting more than one female, only the first ow habitat despite the fact they comprised 31% (251 courting attempt was included in the analysis. Maxi- m2) of all males in this contiguous habitat (Fig. 2B). mum-likelihood chi-square and probability values are Likewise, brachypterous males secured all matings (n reported for the comparison. = 15) in the meadow habitat where their frequency was Planthopper culture and host plant husband^ 69% (55/m2). The virginity of males and females used in experi- Mate location by male wing forms at different ments was ensured by determining the sex of fifth instar female densities nymphs and establishing single-sex colonies of nymphs The ability of the two male wing forms to locate a prior to their adult molt (see Langellotto et al. 2000). female in the meadow habitat differed significantly Newly eclosed virgins were removed from the nymphal across the range of female densities (x2 = 8.25, df = colonies on a daily basis, placed in a uniform age cohort 2, P = 0.016; Fig. 3). When female density was high, of male or female virgins and allowed to mature before brachypterous males located females more than twice they were used in experiments. Spartina seedlings used as frequently (75% of all arriving. males) as macrop- in the experiments (20-25 cm in height) were potted terous males. At low female density, the opposite pat- in sand (6.5 cm diameter pots) and maintained in plas- tic-lined flats (1.0 X 0.7 m) filled half way with water so that sand was continuously wet yet seedlings were TABLE2. Analysis of variance results for the effect of hab- never inundated (see Denno et al. 1985). itat (contiguous Spnrtif7a meadow vs. noncontiguous Spar- tino on mud panne) and location of study site (Wallops Island, Virginia, vs. Elliott Island, Maryland) on the pro- portional abundance of brachypterous males (brachyptersl Mating success of nzale wing forms in contigzious [brachypters + macropters]) in populations of Prokelisin and noncontiguous vegetation dolus.

Because there was no effect of site (Wallops Island Source of variation df MS F P and Elliott Island) or its interaction with habitat on the Habitat 1 0.0443 1.36 0.2580 proportional abundance of the two male wing forms (P Location 1 0.0229 0.70 0.4124 > 0.05; Tables 1 and 2), the expected mating frequency Habitat X Location 1 0.0068 0.21 0.6519 Error 20 0.03265 of each male wing form in each habitat type was gen- MATE LOCATION BY MALE PLANTHOPPERS 1875

1 Observed Matings results for the wing-dimorphic planthopper, Prokelisin A El Expected Matings doliis, demonstrate that changes in both vegetation I n, structure and female density shift the mate-locating ad- vantage from one male wing form to the other. Mac- ropterous males located females or secured matings more frequently than expected in sparse panne vege- tation (Figs. IB, 2A) and under conditions of low fe- male density (Fig. 3). By contrast, brachypterous males obtained many more matings than expected in contig- uous, dense vegetation (Figs. lA, 2B), and they found females more effectively under relatively high-density conditions (Fig. 3). The mating advantage of the bra- chypterous male has been further documented under confined conditions in the laboratory (Langellotto et al. 2000). Vegetation structure influences the effectiveness of the substrate-borne communication system which planthoppers use to locate mates (Ichikawa and Ishii 1974). As long as plants remain in contact, males of P. dolus can sense calling females and locate them by walking (Heady and Denno 1991, Heady 1993). Thus, in contiguous vegetation with virgin females frequent, brachypterous males of P. dolus owned a mating ad- "." vantage, most likely because of their tendency to locate Brachypter Macropter and arrive at calling females before rival macropters (see Langellotto et al. 2000). However, as female den- Male Wing Form sity decreases in contiguous vegetation, mate location FIG.2. Observed and expected mating success of the male wing forms (brachypter and macropters) of Prokelisia d0ll4~ in (A) noncontiguous habitats (Spnrtina on mud pannes) and Brachypter (B) contiguous habitats (Spurtinu meadows) at Wallops Is- Macropter land, Virginia, and Elliott Island, Maryland, USA. In the non- contiguous habitat, brachypterous males acquired signifi- cantly fewer matings and macropterous males acquired sig- nificantly more matings than expected (Fisher's exact test, P = 0.024). Brachypterous males acquired significantly more lnatings and macropterous males acquired significantly fewer matings than expected in the contiguous habitat (Fisher's ex- act test, P = 0.0094). The expected frequency of matings for each wing form in the two habitats was based on their relative densities in each habitat (see Table 1). tern occurred whereby macropterous males located fe- males six times as frequently (83% of all arriving males) as brachypterous males. Macropters located mates more frequently (7 1%) at intermediate female High Medium Low densities. These results underscore the advantage of Female Density flight capability when males must move considerable FIG.3. Number of brachypterous and macropterous males distances among plants to locate widely dispersed fe- that located caged virgin females placed into Spnrtinn mead- males. ows at low, medium, and high densities. The ability of the two male wing forms to locate a mate differed significantly across the range of female densities (x2 = 8.25, P = 0.016). In heterogeneous habitats, dispersal polymorphisms When female density was high, brachypterous males located females more than twice as frequently as did lnacropterous in insects are promoted in theory by a balance between males. At low female density, the opposite pattern occurred, the costs and benefits of flight capability and wing re- and macropterous males located females six times as fre- duction (Fairbairn 1988, Denno et al. 1991, 1996, Roff quently as did brachypterous males. The three female den- 1996). Nevertheless, it has proved difficult to directly sities were established by caging eight virgin females around the periphery of three sizes of plastic rings: 1.0 m2 (low assess the components of habitat heterogeneity which female density), 0.5 m2 (medium density), and 0.25 m2 (high confer advantage and disadvantage to the flight-capable density). The experiment was conducted on a salt marsh at and flightless morphs of wing dimorphic insects. Our Tuckerton, New Jersey. 1876 GAIL A. LANGELLOTTO AND ROBERT F. DENNO Ecology, Vol. 82, No. 7 becomes more problematic because males can only and "low" densities) are macropterous males advan- sense calling females for distances up to one meter taged. (Ichikawa and Ishii 1974). This probably explains why Female density per se is not the essential factor macropterous males of P. dolus were much more ef- which influences the mating success of the male wing fective at locating rare females than were brachypter- forms of planthoppers. Although males of P. dolus can ous males even though the vegetation was contiguous mate multiply, females usually mate only once in life (Fig. 3). and are thereafter unreceptive to courting males (Heady In noncontig~lousSpartina, where plants are sparse and Denno 199 1, Heady 1993). Consequently, female and do not touch, wings are apparently essential for density may be high in the population, but effective mate location because brachypterous males apparently mate density will be low if most females have mated. do not move among isolated plants in their search for This condition probably occurs on the marsh toward females (see Ichikawa and Ishii 1974). Thus, macrop- the end of each adult generation when most females ters should be favored in noncontiguous vegetation be- are likely mated (see Heady 1993). In effect, virgin cause of their ability to fly among plants and locate females may be very scarce and macroptery in males calling females (Ichikawa and Ishii 1974, Hunt and may be essential for locating them. Thus, dispersal may Nault 1991). Indeed, macropterous males of P. dolus be retained in species such as P. dolus even though the were much more successful in acquiring matings than habitat itself is for the most part persistent (Hamilton brachypters on the sparsely vegetated mud panne hab- and May 1977, Denno et al. 1996). itats on the salt marsh (Fig. 2A). To the best of our knowledge, these results with P. Thus, macropterous males possess a clear mating dolus provide the first direct demonstration of how hab- advantage over brachypters in sparse vegetation and itat heterogeneity favors a dispersal polymorphism. under conditions of low female density. Planthoppers Differences in both vegetation structure and changing commonly face very low mate densities in newly col- female density on the salt marsh, coupled with an un- onized habitats (Kuno 1979, Denno and Roderick derlying trade-off between dispersal capability and re- 1990). It is important to note that planthoppers do not production in males (see Langellotto et al. 2000), dic- usually mate before they disperse and that colonizing tate the success of the two male wing forms. For this females colonize new habitats as virgins (Denno and planthopper, the reproductive penalties associated with Rodeiick 1990). Thus, although macropters of plant- flight capability are realized in contiguous vegetation hoppers such as P. dolus are produced under high- when unmated females are frequent. Under these con- density conditions, they often disperse from such hab- ditions, flightless males gain the mating advantage. In itats to colonize other areas where mates are rare. contrast, the inherent reproductive advantage of the One may ask why brachypterous males gain a mating flightless morph is negated when mates are rare and in advantage under high-density conditions when they are sparse vegetation where flight is necessary for mate produced under less crowded circumstances. High and location. Notably in this system, habitat heterogeneity low density are relative terms, and the answer to this dictates mating success as much as heterogeneity in apparent paradox lies in the difference in scale at which resource availability (variation in female density), be- mate location and the triggering of macropters have cause patchiness of vegetation affects a planthopper's been assessed (see Denno and Roderick 1992). The ability to locate mates. female densities we used to assess mate location were 4, 8, and 16 females/m2, which represented our "low," "medium," and "high" densities. These densities are We thank Deborah Gordon, David Hawthorne, Charles Mit- ter, Derek Roff, Barbara Thorne, and two anonymous re- all low considering that the adult density of P. dolus viewers for their insightful suggestions on earlier drafts of can exceed 1000/m2 (Denno et al. 1996). Using the this report. Micky Eubanks, Deborah Finke, Mark Fox, An- conversion factor of 418 Spavtina stems/m2 in meadow drea Huberty, John Losey, and John McAllister provided us habitats, our female densities translate into 0.01, 0.02, with technical assistance. We are most grateful to all of these colleagues. This research was supported by National Science and 0.04 femaleslstem. The triggering of macropters Foundation Grants DEB-9209693 and DEB-9348071 to RFD. occurs at a much higher density than any of those we used in our mate location experiment. For example, when P. dolus was raised at a density of 1 individual1 Adams, D. A. 1963. 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