Behavioral Ecology Behav Ecol Sociobiol (1987) 21:157-162 and Sociobiology ? Springer-Verlag 1987

The timing of calling, movement,and mating in the field crickets Gryllusveletis, G. pennsylvanicus,and G. integer

B. Wade French and William H. Cade Departmentof Biological Sciences, Brock University, St. Catharines,Ontario, L2S 3A1, Canada

Received December 23, 1986 / Accepted June 22, 1987

Summary. The temporal relationships between Methods and movement were studied in nat- mating, calling, G. integer commonly occurs in central Texas from spring to ural habitats at different densities in the field crick- fall and was studiedfrom April to August, 1986, at the Bracken- ets, Gryllusveletis, G.pennsylvanicus and G. integer. ridge Field Laboratory, The University of Texas, Austin. In There was variation between and within species, southern Ontario, G. veletis is sexually mature from May until but males showed increased at late July, whereas G. pennsylvanicusis sexually mature from generally calling until October G. veletis and dawn a decline early August (Alexander 1968). followed by during the day. Mat- G. pennsylvanicuswere studied on the campus of Brock Univer- ings were also more frequent at sunrise in most sity, St. Catharines, Ontario, from June to September 1983 observations, and male and female movement de- and 1984. clined near dawn. Female movement and sexual receptivityare closely related to levels of male call- Outdoor arenas ing and movement. All studies were carriedout in outdoor arenas placed in natural habitats. Arenas were constructedof concrete walls (G. integer) or aluminum siding (G. veletis and G. pennsylvanicus) and measured approximately 13.5 x 13.5 x 1.2 m. The arenas contained naturally occurring grasses and other herbaceous Introduction plants which were routinely cut to a height of approximately 4 cm to facilitateobservations. To preventbird entry, the arenas The calling song of male field crickets attracts con- were completely covered with orchard bird netting supported females. Males also search for females in by posts. The mesh was large enough to allow crickets to enter. specific Plastic flags were used to divide the arena into 25 quadrats, the vicinity of calling males. Male searching and each approximately2.7 x 2.7 m. Cricket shelters were provided calling behavior apparently evolved in the context consisting of a hole in the soil approximately4 cm deep covered of male-male competition and female choice, and by a piece of plywood, 24 x 24 cm. One shelter was placed in males should call and search when females are the center of each quadrat. Flat stones approximately 12 x 12 cm were at the of a side of most Cade placed midpoint quadrat receptive (Alexander 1975; 1979a, adjacent to a wall. The soil was moistened daily since crickets 1980; Otte 1977; Walker 1983a). With few excep- require moist soil for oviposition and they drink water from tions (Forrest 1983; Walker 1983b), however, very the soil and vegetation. little is known about the relationship between fe- male and the of male receptivity nightly timing Collecting crickets cricket calling and searching behavior under field conditions. Very few observations have been con- G. veletis and G. pennsylvanicuswere collected as nymphs and ducted on crickets and other active an- adults in St. Catharines.Crickets were brought into the labora- nocturnally tory and kept at 25-30? C and 30-35% relative humidity. The imals throughout the night. The research reported photoperiod was 12 h light and 12 h dark. Females and male here was intended to test the hypothesis that the nymphs were housed in separate terraria. All terraria were timing of male searching and calling behavior checked daily for newly molted adults, and individual adult coincides with the of under males were placed in 500 ml cardboard cups. Food (Purina closely timing mating Cat vials of and shelter field conditions in the field veletis Chow?, lettuce), cotton-plugged water, crickets, (egg cartons) were provided. G. integer were collected in the and G. pennsylvanicusin Ontario, and G. integer field or when attracted to taped broadcasts of G. integer song in Texas. or to electric street lights (Cade 1979a, b). Also, male and

This content downloaded from 142.66.3.42 on Tue, 23 Jul 2013 15:10:33 PM All use subject to JSTOR Terms and Conditions 158 female G. integer routinely flew into the arena, probably in The linear distance travelledby males between surveyswas response to males calling within. One hind wing was removed used to assess movement as an indicator of searchingbehavior. from each male and female cricket, thus preventing G. integer Cricketshad to travel at least 60 cm in the arena before move- from flying out of the arena. Individual crickets were marked ment was scored. This was the minimum detectable displace- distinctively(Walker and Wineriter1981), but data on individ- ment allowed for transferringa cricket's location in the arena ual variationin mating behavior are reportedelsewhere (French to its location on the arena map. The movement of females 1986). Hindwing removal and marking has no effect on survi- was also determinedin the same manner, since female locomo- vorship or the duration of nightly calling of male G. integer tion and phonotaxis vary with sexual receptivity(Cade 1979c; (Cade unpublished).A series of observationsbegan by releasing Loher 1979a, b, 1981). males and females into the center or under randomly chosen burrowsof the arena about 3-5 h before sunset. The population density of G. integerwas maintained at approximately5 males Results and 5 females. Since population density may affect calling be- havior (Alexander 1961, 1968, 1975), two densities were used 24 h observations in G. veletis and G. pennsylvanicus:a low density of 5 males and 5 females and a relatively higher density of 20 males and Frequency distributions of matings, movement, 20 females. After an introduction the density was maintained and are in 1 for G. veletis at both densi- at approximatelythe initial level by adding previouslycollected calling Fig. crickets that were held temporarilyin the laboratory, or num- ties. There were too few matings at low density bering crickets that flew into the arena in G. integer.Attracted for statistical testing, but all matings occurred dur- G. integer were removed if not needed to maintain the appro- ing the day. Female movement and male calling priate density. Replicatesfor the same species at the same densi- were significantly different from random at low ties were performed as follows: 3 samples at low density of with most at and near sun- 9, 10 and 4 nights for G. integer; 1 sample of 10 nights at density activity night high density, and 2 samples of 10 nights each at low density rise. (Statistical data are summarizedin Table 1 for for G. veletis; 2 samples of 10 and 19 nights at high density, all populations). Male movement was randomly and 1 sample of 9 nights at low density for G. pennsylvanicus. distributed with respect to time in the low density The replicateswere combined for statistical analysis since most G. veletis did not samples had homogeneous variances(French 1986). populations. Matings vary signifi- cantly at high density in G. veletis. In contrast, female and male movement and the number of Observations and data collection callers were statistically different from random dis- Arenas were observed from 22.00 to 08.00 h (approximately 1.5 to 3 h past sunset to 2 to 3 h past sunrise). Sunset times Gryllusveletis were approximately19.53 h and sunrise times were approxima- I-I Low Density- 24 h 04.47 h local time for G. 19.15 h and 05.23 h local HighDensity - 24 h Matings A tely veletis, 6- 6 time for G. pennsylvanicus,and 20.00 h and 05.00 h local time for G. integer. These sunset and sunrise times were estimated from the average of the sunset and sunrise times on the first and last days of the month. A single observation over a com- plete 24 h cycle was also performed once for G. veletis and . G. at each At the of each I I.I.. pennsylvanicus density. beginning night a complete survey of the arena was conducted using a H30- | FemaleDisplacement B headlamp to ascertain each cricket's location. Crickets were readily visible under the shelters or in the grass. Locations of cricketswere marked on maps of the arena. A complete inspec- 153 i5 tion of the arena was made every h and a new map used to record cricket positions. Calling behavior was ascribed to a particular male if he was the only one in a given location at the previous and follow- Z 18- I Calling Males C ing check of male positions. If more than one male was in a shelter, it was possible to raise the shelter and, although the male stopped calling, observe which male had his wings still raised in the calling position. Males disturbedin this way usual- ly resumed singing after a few min. If calling was heard from a position where no male had been observed previously, we - 45 Sunrise n D identifiedthat male and marked his position on the map. Every MaleDisplacement 5 min we recorded the production of calling song for males of known identity. To determine the number of calling males 30 1I Sunset in each male who called for at least one 5 min interval h, any 15 was scored as a caller. This practice produces a conservative estimate of the total duration of calling. In all cases, however, males called during several of the 5 min intervalsavailable each 23 02 05 08 11 14 17 20 were considered to have occurred h (French 1986). Matings Time of when a copulation was observed or a female possessed a fresh Day (h) spermatophorewhile in the immediatepresence of a single male. Fig. 1 A-D. The 24 h activity patterns for G. veletis

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Table 1. Summary of x2 values and significance levels for G. veletis, G. pennsylvanicus(at low and high density observations over 24 h and 10 h) and for G. integerobservations over 10 h

G. veletis G. pennsylvanicus G. integer

Low N High N Low N High N Low N

Matings 24h -- 2.5(1) 4.9(1)* lOh 21 (9)* 35.9 (9)8* 11.9(9) 45.4 (9)** 46.9 (9)** Female movement 24 h 26 (7)** 37.8 (7)** 3.6 (5) 31.2 (7)* 10h 41.1(9)** 149.9 (9)** 24.2 (9)** 213.9 (9)** 48.8 (9)** Male movement 24 h 1.9 (7) 59.3 (7)** 6 (5) 13.6 (7) 10h 16.9 (9) 60.6 (9)** 11.5(9) 115.6(9)** 37.6 (9)** Calling 24 h 13.7 (7)* 45.6 (7)** 4 (3) 38.1 (7)* 10h 4.0 (9) 27.4 (9)** 14.5 (9) 124.6 (9)** 41.7 (9)** ** * P<0.05, P<0.01, ( )=df

Gryllus pennsylvanicus pennsylvanicusare in Fig. 2. Mating was statisti- non-random at low and occurred at r- Low - 24 h cally density, Density Matings A and near sunrise. There were no HighDensity - 24 h night significant differences in the number of crickets moving or calling at low density. Although there were too 2- few matings for statistical analysis at high density in G. pennsylvanicus,matings occurredat night and near sunrise. Female movement and male 45- FemaleDisplacement B calling did vary significantly. Most females moved during 30 the day, whereas males called primarily at night with a peak just before sunrise. Male movement - 151 was not statistically different from random.

Z Males C 30- Calling Nightly (10 h) observations Figure 3 displays the temporal distributions of ac- tivities for both densities of G. veletis. Matings var- ied significantly and peaked soon after sunrise at Sunrise MaleDisplacement D low density. Female movement was also statisti- 40- Sunset cally significant and peaked a few hours before sunrise. The number of males calling and moving 20 did not vary significantly with time. At high den- sity, G. veletis matings peaked at sunrise and the distribution was statistically significant. Male and 23 02 05 08 11 14 17 20 female movement also showed significantvariation Time of Day (h) with peaks occurring a few hours before sunrise. was non-random Fig. 2A-D. The 24 h activity patterns for G. pennsylvanicus Calling behavior significantly and peaked at sunrise. The temporal distributions of mating, move- tributions. Most female movement occurred at ment and calling are presented in Fig. 4 for G. night, whereas males continued to move at sunrise pennsylvanicus. Female movement was the only with a decline during the day. Calling peaked at variable showing statistical significanceat low den- sunrise and was commonly observed for the first sity, and this activity declined near sunrise. At high few hours of daylight. density, however, all activities varied significantly. Data on mating, movement and calling in G. Mating and calling peaked near sunrise, whereas

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Gryllus veletis Gryllus integer Low Density- 23 Matings A 20- 0 Low Density-20 Nights Matings A Nights 20 * HighDensity - 10 Nights

10 10

120- FemaleDisplacement B 80 FemaleDisplacement B

60 40 E I

Z1-53~~~~~~ ~~~Calling Males C CallingMales C z70 z 80-_

35 40

MaleDisplacement D 120- MaleDisplacement D 80 Sunrise Ii B I - -Sunrise

60- 40-

2 3 4 5 6 7 8 9 10 11 2 3 4 5 6 7 8 9 10 11 Time Since Sunset (h) Time Since Sunset (h) Fig. 3A-D. The 10 h activity patterns for G. veletis Fig. 5A-D. The 10 h activity patterns for G. integer

Gryllus pennsylvanicus movement by both sexes was most pronounced a Low Density- 9 Nights few hours before dawn. -35~~~~~~ ~Matings A 5 * HighDensity - 29 Nights Figure 5 presents data from the low density G. integer population. All cricket activities showed 10 statistical departure from random distributions. Calling and mating were frequently observed soon after dawn. Female movement was most pro-

~~190 L L I I I FemaleDisplacement B nounced during the night and declined after sun- 110 rise. Male movement was relatively constant until dawn and then declined sharply. 30

Discussion 250_. Male G. veletis, G. pennsylvanicus,and G. integer called more at and at dawn than in the 100 night day- 20 light hours. Alexander and Meral (1967), however, found that male G. veletis and G. pennsylvanicus continued singing in the day, and changed from - 250 MaleDisplacement D night to day singing when nightime temperatures Sunrise were below 10? C. Such low temperatures were 200 | showed ? rarely observed in our study. Cade (1979 a) 80-I i an increase in behavior at sunset in field 30 11111 calling populations of G. integer, and our data confirm these earlier observations. The onset of calling in 3 4 5 6 7 8 9 10 11 12 male field crickets, Teleogrylluscommodus, is close- Time Since Sunset (h) ly tied to photoperiod and under circadiancontrol. Fig. 4A-D. The 10 h activity patterns for G. pennsylvanicus Under laboratory conditions of constant light or

This content downloaded from 142.66.3.42 on Tue, 23 Jul 2013 15:10:33 PM All use subject to JSTOR Terms and Conditions 161 constant darkness, males began calling about 24 h tion is from only 1 sample, however, and the 10 h later than the previous day when the photoperiod observations may therefore be more accurate. In was 12 h light and 12 h dark. When the photoperi- the 24 h and 10 h observations on G. veletis, and od was maintained at 12 h light and 12 h dark the nightly observations on G. integer, female males called 2 h before darkness until 2 h before movement declined following sunrise at the time the onset of light (Loher 1972). of highest mating frequency. In this connection, Calling increased at dawn in field populations female cricket locomotion and phonotaxis is re- of G. integer in our study, but previous observa- duced by mating in T. commodus (Loher and tions showed that dawn calling does not occur at Rence 1978; Loher 1981), G. integer and G. veletis very low densities when males are isolated at long (Cade 1979c) in laboratory experiments. distances from each other (Cade 1979a). Dawn Male movement occurred throughout the 24 h calling in G. veletis and G. pennsylvanicuswas also and 10 h observations. Significant variation was influenced by density as the number of calling found in the G. veletis high density 24 h observa- males occurred randomly with time in the low den- tion where male movement declined following sity 10 h observations on both species, and in the sunrise. Concerning the 10 h observations, a more 24 h data on G. pennsylvanicus.At high densities regular pattern occurred in high density popula- males called more at dawn in 10 and 24 h observa- tions of G. veletis, G. pennsylvanicusand in the tions. Dawn calling reflects the commencement of only density of G. integer studied: male movement signaling by some males who remained silent the declined at approximately 8-9 h after sunset, the previous night (Cade 1979a). Occurrence of silent hours just before and after sunrise and the time or satellite male behavior is more common in high when mating and calling occurredmost frequently. density populations thus contributing to the den- Male movement may reflect searching for females sity dependent aspect of dawn calling. and other factors including foraging and interac- Walker (1983a) described different patterns of tions with other males. In any case our data sug- male calling behavior with time and hypothesized gest that male field crickets reduce their movement that males should call at a time when females are and start calling when females are most receptive most likely to mate. Extensive calling throughout to mating. the night with a peak in activity near dawn corre- The selective factors leading to increased fe- sponds to Walker's category of extended mating male mating at dawn are not clear. One possibility sprees. Our data showed that matings occurred is that female crickets postpone mating during randomly throughout the 24 h in the G. veletis high times when the cost of mating is high due to acous- density population, although over 50% of the mat- tically orienting . Female tachinids, Euphasiop- ings at the high density occurred just before and teryx ochracea, deposit larvae on and near calling after dawn. At low density, however, all matings male G. integer, and the cricket subsequently dies. were in the day. Interpretationof the all day obser- Flies are especially active right after sunset with vations is limited by sample size. The nightly obser- reduced activity at sunrise. Crickets also become vations on G. veletis showed sunrise peaks in mat- parasitized by walking over larvae which adhere ing frequencies, and G. pennsylvanicusmated more to the host (Cade 1975, 1979a, 1984). Female G. often before and after sunrise. integer may reduce the probability of parasitism Sunrise peaks in mating were also observed in by E. ochracea by mating at dawn when flies are G. integer. The timing of calling and female sexual less active. G. veletis and G. pennsylvanicusare not receptivity in G. pennsylvanicus,G. veletis and G. parasitized,however, by acoustically orienting flies integer are closely correlated, and these data sup- in our study area (Cade and Wyatt 1984). port Walker's hypothesis that male crickets call Female choice of mates should also be impor- primarilyat times when females are most receptive. tant in determining when males sing (Walker Courtship song increases at dawn in G. veletis and 1983a). In the mole crickets, Scapteriscus vicinus G. pennsylvanicus,thus supporting the finding that and S. acletus, and short-tailed crickets, A. arbor- mating activity is most pronounced at sunrise in eus, males call for only 2 h or less after sunset, these species (Zuk 1986). the time when females are phonotactic (Forrest In the 24 h observations on G. pennsylvanicus, 1983; Walker 1980, 1983b). Different patterns oc- most female movement occurred in the daylight. cur in T. oceanicus(Loher and Orsak 1985), Anuro- A different pattern was observed in the 10 h repli- gryllus muticus (Walker and Whitesell 1982), and cates on G. pennsylvanicus where most female Gryllodes supplicans (Sakaluk 1987), where males movement was at night with a decline at sunrise, generally sing all night. Females may requiremore the time of most mating activity. The 24 h observa- time to evaluate males in species characterizedby

This content downloaded from 142.66.3.42 on Tue, 23 Jul 2013 15:10:33 PM All use subject to JSTOR Terms and Conditions 162 long bouts of calling (Walker 1983b). Increased Cade WH (1979b) Field cricket dispersal flights measured by calling at dawn is a variation on the all-night call- crickets landing at lights. Tex J Sci 31:125-130 and result from a combination Cade WH (1979c) Effect of male-deprivationon female phono- ing pattern may taxis in field crickets (:; Gryllus).Can of female choice and commencement of calling by Ent 111:741-744 previously silent males. Calling song at dawn is Cade WH (1980) Alternativemale reproductivebehaviors. Fla produced at lower sound intensities than earlier Ent 63:30-45 in the in G. Lower intensities Cade WH (1981) Alternativemale strategies:genetic differences night integer. song in crickets. Science 212:563-564 females to mate rather than may stimulate nearby Cade WH (1984) Effects of parasitoids on nightly calling attracting females from a distance (Cade 1979a). duration in field crickets. Can J Zool 62:226-228 Our data do not directly test the possibility of Cade WH, Wyatt DR (1984) Factors affecting calling behav- female choice or other selective factors influencing iour in field crickets, Teleogryllusand Gryllus(age, weight, the distribution of cricket One density, and parasites). Behaviour88:61-75 temporal activity. ForrestTG (1983) Calling songs and mate choice in mole crick- important criterion to a female choice model, how- ets. In: Gwynne DT, Morris GK (eds) Orthopteranmating ever, is that male variation in calling schedules is systems. Westview Press, Boulder, pp 97-119 heritable (Loher 1979b). Honegger (1981) demon- French BW (1986) Male reproductivecompetition in the field strated that individual male G. campestris call at crickets and G. pennsylvanicus.Msc thesis, certain times of the and and Cade Brock University, St. Catharines,Ontario day night, (1981) Honegger HW (1981) Three differentdiel rhythmsof the calling showed that nightly calling duration has heritable song in the cricket, Gryllus campestris,and their control variation in G. integer. Female mate choice should mechanisms.Physiol Entomol 6:289-296 also result in increased mating frequency with in- Loher W (1972) Circadiancontrol of stridulationin the cricket creased levels of male behavior Teleogrylluscommodus Walker. J Comp Physiol 79:173-190 calling (Alexander Loher W (1979a) Circadianrhythmicity of locomotor behavior 1975; Cade 1979a). Very few data are available and oviposition in female Teleogrylluscommodus. Behav to test this prediction, but selection for calling du- Ecol Sociobiol 5:253-262 ration occurs in some populations of field crickets Loher W (1979b) The effect of male calling on female locomo- More information is needed on tor activity of Teleogrylluscommodus. Behav Ecol Sociobiol (French 1986). 5:383-390 male-female interactions and ecological parame- Loher W (1981) The effect of mating on female sexual behavior ters to understand the factors influencing the tem- of Teleogrylluscommodus Walker. Behav Ecol Sociobiol poral distribution of behavior in field crickets 9:219-225 (Loher and Orsak 1985). Loher W, Orsak LJ (1985) Circadian patterns of premating behaviorin Teleogryllusoceanicus Le Guillou under labora- and field conditions. Behav Ecol Sociobiol 16:223- on veletis and G. tory Acknowledgements.Research G. pennsylvani- 231 fulfillmentof the for cus was completed in partial requirements Loher Rence B The behavior of in Sciences and was funded W, (1978) mating Teleogryllus the M.Sc. degree Biological (BWF) commodus and its central and control. Research Council of (Walker) peripheral by a Natural Sciences and Engineering Z 46:225-259 RD Tierpsychol Canada grant (A6174, to WHC). We thank Alexander, Otte D Communicationin In: Sebeok TA RW W RD S and JJ Flint (1977) Orthoptera. Knapton, Loher, Morris, Sakaluk, How communicate. Indiana Press, VL Back- (ed) University for comments on an earlierversion of the manuscript. 334-361 collection. JW Char- Bloomington, pp us and EJ McGowan helped with the data Sakaluk SK behaviour of the decorated dine with statistical (1987) Reproductive helped analyses. cricket,Gryllodes supplicans (Orthoptera: Gryllidae): calling schedules, spatial distribution, and mating. Behaviour References 100:202-225 Walker TJ (1980) Reproductive behavior and mating success Alexander RD (1961) Aggressiveness,territoriality, and sexual of male shorttailedcrickets: differenceswithin and between behavior in field crickets (Orthoptera: Gryllidae). Behav- demes. Evol Biol 13:219-260 iour 17:130-223 WalkerTJ (1983a) Diel patternsof calling in nocturnalOrthop- Alexander RD (1968) Life cycle origins, speciation, and related tera. In: Gwynne DT, Morris GK (eds) Orthopteranmating phenomena in crickets. Quart Rev Biol 43:1-41 systems. Westview Press, Boulder,pp 45-72 Alexander RD (1975) Natural selection and specializedchorus- Walker TJ (1983b) Mating modes and female choice in short- ing behavior in acoustical . In: Pimentel D (ed) In- tailed crickets (Anurogryllusarboreus). In: Gwynne DT, sects, science, and society. Academic Press, New York, Morris GK (eds) Orthopteran mating systems. Westview pp 35-77 Press, Boulder, pp 240-267 Alexander RD, Meral GH (1967) Seasonal and daily chirping Walker TJ, Whitesell JJ (1982) Singing schedules and sites for cycles in the northern spring and fall field crickets, Gryllus a tropical burrowingcricket (Anurogrvllusmuticus). Biotro- veletis and G. pennsylvanicus.Ohio J Sci 67:200-209 pica 14:220-227 Cade WH (1975) Acoustically orientingparasitoids: fly phono- Walker TJ, WineriterSA (1981) Marking techniquesfor recog- taxis to cricket song. Science 190:1312-1313 nizing individualinsects. Fla Ent 64:18-29 Cade WH (1979a) The evolution of alternativemale reproduc- Zuk M (1986) Sexual selection, mate choice and gregarinepara- tive strategies in field crickets. In: Blum MS, Blum NA site levels in the field crickets Gryllusveletis and G. pennsyl- (eds) Sexual selection and reproductivecompetition in in- vanicus.PhD dissertation,University of Michigan, Ann Ar- sects. Academic Press, New York, pp 343-378 bor

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