Charles S. Henry and Christine Busher.
Patterns of mating and fecundity in several common green lacewings (Neuroptera: Chrysopidae) of eastern North America.
Psyche 94:219-244, 1987.

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PATTERNS OF MATING AND FECUNDITY
IN SEVERAL COMMON GREEN LACEWINGS
(NEUROPTERA: CHR YSOPIDAE)
OF EASTERN NORTH AMERICA*
Box U-43, Dept. of Ecology and Evolutionary Biology The University of Connecticut, 75 North Eagleville Road Storrs, Connecticut 06268 (U.S.A.)
Recently, much interest and innovative research have focussed on the mating systems of animals (Thornhill and Alcock, 1983; Willson and Burley, 1983). Our interpretation and understanding of repro- ductive behavior, for example, has undergone a metamorphosis in the last few years. In the recent past, such common reproductive activities as courtship were viewed as steps to overcome some sort of physiological threshold in the female of the species (Marler and Hamilton, 1966, chapter 3), or, alternatively, as mechanisms to pre- vent the interbreeding (hybridization) of different species (Mayr, 1963). However, principally since the publication in the mid 1970's of works by Alexander (1975, 1977) and Wilson (1975), evolution- ary biologists have adopted a rather different view of courtship and other reproductive behavior. This perspective is a more inclusive one, stressing the evolutionary or selective benefits to individuals of behaving the way they do during sexual activity. Courtship is more properly viewed as a series of test questions posed by the courting individual to its potential partner. The answers to these questions help the individual decide where the other individual is located; what species and sex that individual is, to avoid costly mistakes in mating; and how good a mate that individual will make, in terms of its vigor, strength, and success at intrasexual competition or at se- curing resources for its partner. In fact, the ultimate goal of repro- ductive behavior is success in transmitting an individual's genes to the next generation, through the production of viable, fit offspring. Individual reproductive success can be achieved in a variety of ways. Females can have very high fecundity, or they may provide more care or resources for fewer offspring. Additional strategies are *Manuscript received by the editor September 25, 1987 219
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220 Psyche [Vol. 94
open to males, which need only produce energetically "cheap" sperm rather than expensive eggs. On the one hand, a male can copulate with as many females as time and conditions allow; alter- natively, he may be more careful to ensure, through attention and guarding, that the sperm transferred are actually used by the female to produce offspring (Waage, 1983). The stage is set in many ani- mats for sexual inequality: males may embark on highly polygynous reproductive lives, while females choose fewer times and more care- fully among the scrabbling suitors. With such inequities comes unfairness, especially among males: if one male can inseminate many females, but each female accepts only a few males, then many other males must never get the opportunity to mate. High variance in reproductive success among males is the basis for strong sexual selection on males (Darwin, 1859, 187 I), which in turn is thought to sculpt the obvious morphological and behavioral dimorphism between the sexes that exists in the majority of animal species. It is often assumed, but rarely documented, that individual males of sexually dimorphic species inseminate many females, and can produce many more progeny than can individual females. Converse- ly, it follows that species displaying little sexual dimorphism should be reasonably equivalent in the reproductive potential of the two sexes. Insects are well suited for testing predictions of sexual selec- tion theory, because they exhibit inexhaustible diversity of life- history strategy (Dingle and Hegmann, 1982) and are often easy to observe and manipulate in the field and laboratory. For example, green chrysopid lacewings show a convenient range of sexual di- morphism, from extreme in Mdeoma Fitch spp. (Bickley and MacLeod, 19561, through moderate in the common Chrysopa ow- ta~a Say (Smith, 1922), to negligible in the carnea-group within the genus Chrysoperla Steinmami (Henry, 1983). Fortunately, most lacewing species adapt well to laboratory culturing, so simple stud- ies measuring individual reproductive success are both feasible and reasonably representative of conditions in nature. Here, we concen- trate on the reproductive biology of two well known, closely related species of the cornea-group, but we include some preliminary data on several other species characterized by greater sexual dimorpliism. The principal protagonists are the syrnpatric, closely related North American species C. plorabunda (Fitch) and C. downesi (Smith). C. plorabunda is a common meadow-dwelling form with multiple generations per year, while C. downesi is a darker green



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conifer-associated species that produces but one annual generation (Tauber and Tauber, 1976; Henry, 1980a). Each species, but espe- cially C. plorabunda, has been well studied because of its impor- tance in biological control (New, 1975; Hassan, 1978). Also, both species have figured prominently in investigations of sympatric spe- ciation through disruptive selection (Tauber and Tauber, 1977a, b; 1982) and song divergence (Henry, 1980a, 1983,1985a, b). Extensive fecundity data, relating egg production to diet or age, have been published for these and several other important green lacewings (Rousset, 1983). However, the extent of polygyny and polyandry, or the effect of multiple matings on fertility and fecundity, have not been determined for any chrysopid. Yet such basic information about mating habits and consequences is prerequisite to understand- ing several broader issues-particularly, the consequences of differ- ent life-history patterns and reproductive strategies, the dynamics of rapid speciation through acquisition of assortative mating patterns (West-Eberhard, 1983; Henry, 1986), and mass rearing and release in programs of biocontrol.
Data for this paper were generated over several years, as part of a larger project investigating courtship singing behavior, reproductive isolation, and speciation in sibling species of the genus Chrysoperla (Henry, 1983, 1985a, b, 1986). Adult green lacewings of C. plora- bunda, C. downesi, and several additional species were collected from the field during the warmer months and maintained through- out the year in small, outbred colonies of 25 to 50 individuals. Most species were available locally, within 15 miles of Storrs, Connecti- cut; however, C. downesi and most of the Meleoma emuncta (Fitch) came from coniferous forests on the E. N. Huyck Preserve in Rens- selaerville, New York. Additional C. downesi in 1982 and 1983 were from populations in central Vermont (Echo Lake), southern New Hampshire (Mount Monadnock), and northwestern Massachusetts (north of Quabbin Reservoir). And late in 1986, we included several individuals of C. plorabunda from near Moscow, Idaho, in the study. Laboratory colonies of all species were maintained as de- scribed earlier (Henry, 1979, 1980a, b) and kept at 261k2OC. An artificial diet consisting of equal proportions (by weight) of honey, yeast hydrolyzate (DifcoTM), water, and WheastTM was available in excess to all adults. Chrysopa oculata, the only species studied



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conifer-associated species that produces but one annual generation (Tauber and Tauber, 1976; Henry, 1980a). Each species, but espe- cially C. plorabunda, has been well studied because of its impor- tance in biological control (New, 1975; Hassan, 1978). Also, both species have figured prominently in investigations of sympatric spe- ciation through disruptive selection (Tauber and Tauber, 1977a, b; 1982) and song divergence (Henry, 1 98Oa, 1983, l985a, b). Extensive fecundity data, relating egg production to diet or age, have been published for these and several other important green lacewings (Rousset, 1983). However, the extent of polygyny and polyandry, or the effect of multiple matings on fertility and fecundity, have not been determined for any chrysopid. Yet such basic information about mating habits and consequences is prerequisite to understand- ing several broader issues-particularly, the consequences of differ- ent life-history patterns and reproductive strategies, the dynamics of rapid speciation through acquisition of assortative mating patterns (West-Eberhard, 1983; Henry, 1986), and mass rearing and release in programs of biocontrol.
Data for this paper were generated over several years, as part of a larger project investigating courtship singing behavior, reproductive isolation, and speciation in sibling species of the genus Chrysoperla (Henry, 1983, 1985a, b, 1986). Adult green lacewings of C. plora- bunda, C. downesi, and several additional species were collected from the field during the warmer months and maintained through- out the year in small, outbred colonies of 25 to 50 individuals. Most species were available locally, within 15 miles of Storrs, Connecti- cut; however, C. downesi and most of the Meleoma emuncta (Fitch) came from coniferous forests on the E. N. Huyck Preserve in Rens- selaerville, New York. Additional C. downesi in 1982 and 1983 were from populations in central Vermont (Echo Lake), southern New Hampshire (Mount Monadnock), and northwestern Massachusetts (north of Quabbin Reservoir). And late in 1986, we included several individuals of C. plorabunda from near Moscow, Idaho, in the study. Laboratory colonies of all species were maintained as de- scribed earlier (Henry, 1979, 1980a, b) and kept at 26+2OC. An artificial diet consisting of equal proportions (by weight) of honey, yeast hydrolyzate (DifcoTM), water, and WheastTM was available in excess to all adults. Chrysopa oculata, the only species studied



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requiring adult prey for proper egg maturation (Tauber and Tauber, 1973), was given Aphis fabae Scopoli raised on greenhouse-grown Nasturtium sp. Meleoma emuncta adults were fed a mixture of assorted pollens and honey (J. Johnson, Univ. of Idaho, pers. corn.). All larvae were fed ether-killed Drosophila spp. every 2-3 days. Photoperiod was manipulated for C. downesi to break adult repro- ductive diapause (Tauber and Tauber, 1976); for other species, con- stant long-day (17L:7D) light regimes were maintained. We took three simple experimental approaches: (1) Field- captured, gravid females were allowed to oviposit freely without re-mating. From this, we could assess the extent of egg productivity possible from sperm in reserve under natural conditions. (2) Young (two-week-old), laboratory-reared virgin females were mated as often as they would accept previously unmated males, while others of the same cohort were mated just once; whenever possible, copula- tion duration was noted. Egg production and sexual receptivity were monitored for each female throughout the experiment. This approach was designed to determine the extent of polyandry, the number of eggs produced per copulation, and the relationships among sexual receptivity, re-mating, copulation duration, and egg- laying. Sexual receptivity, which is lost in female lacewings after copulation, was assessed by playing back species-appropriate songs to the insects and waiting for "answers" (abdominal dueting behav- ior [see Henry, 1985a, b]). To minimize the effects of aging on fecundity, insects that had been sexually mature for more than two weeks were excluded from these studies. Maturity, in turn, was judged by the onset of sexual receptivity. (3) Finally, individual two-week-old males were re-mated to unmated, receptive females at 1-3 day intervals, until they could no longer copulate. This provided estimates of sperm transferred and accepted per copulation, degree of polygyny, and minimum total lifetime reproductive potential for each male. Females were selected from cohorts of the same age as the males. Since a single male could easily mate with many females, we were forced in one case (male H of Table 6) to recruit two-week- old virgin females after the 18th copulation. All three approaches above shared one simple but important pro- tocol: count every egg and determine whether or not it had been fertilized. Counting was facilitated by the egg stalk so typical of the green lacewings: each egg could be clipped cleanly from its substrate and placed on the filter paper floor of a 10 cm plastic petri dish for



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19871
Henry & Busher- Green lacewings
storage. Fertility was indicated by darkening of the initially green egg within two days of oviposition at about 26OC. Unstalked eggs, glued directly to the substrate or dropped to the ground, were also monitored for darkening and included in any counts if fertile. Eggs were clipped, counted, and monitored three times per week, unless otherwise specified. Clipped eggs from one session were saved until the next7 so that their fertility or sterility could be guaranteed. Since just 5 to 10 percent (at most) of any individual female's eggs were ever inviable, the results tabulate only fertile, developing eggs. Sample sizes varied considerably from one experiment to another, due to the opportunistic nature of the studies. For exam- ple> egg counts were performed on 8 field-captured, gravid females of Chrysopa oculata and 6 of Chrysoperla harrisii (Fitch), but only three of such females of C. rufilabris (Burmeister) and one of c. downesi were available, and C. plorabunda was neglected alto- gether. Similarly, multiple-mating experiments on females were completed only with C. plorabunda (21 females) and C. downesi (1 7 females). Individuals that produced fewer than 400 eggs were excluded, since our interest was in maximal fecundities. Male multiple-mating studies were limited to C. plorabunda (8 males), C. downesi (21, and C. oculata (2). Finally, a few data correlating fertility with copulation duration were taken, but only for C. plora- bunda (27 matings) and C. downesi (15 matings). Means and standard deviations were calculated from the data using a computer spreadsheet (LOTUS 1, 2, 31M). Samples were tested for normality by a Kolmogorov-Smirnov routine, and deemed significantly different by two-tailed t-tests and confidence limits of 99%, using the statistical functions of the computer program ASY STANT-kTW.
Voucher specimens have been deposited in the insect collection of the Department of Ecology and Evolutionary Biology, University of Connecticut, Storrs.
Egg Counts: Field-capt ured, Gravid Females. Egg productivity by wild females of C. oculata, C. harrisii, C. rufilabris, C. downesi, and M. emuncta are shown in Tables 1 and 2 (no field-collected C. plorabunda were tested). For all species except M. emuncta, totals per female averaged between 700 and 1000 eggs: insignificantly different from one another. Such totals also reflect



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Table 1. Average fecundity of females of six chrysopid species, from field and laboratory data. Data are means and standard deviations; sample sizes are entered parenthetically. Oviposition lifespan, in days, is the period during which a female continuously produced fertile eggs.
Chrysoperla C. downesi Chrysoperla Chrysoperla Chrysoperla Meleoma plorabunda harrisii rufilabris oculata emuncta (Laboratory) (Lab.) (Field) (Field) (Field) (Lab.) (Field) (Field) Total Eggs 780 k 769 k 991 (1) 744 k 905 (k) 683 * 761 2 132 k 240 (21) 233 (17) 146 (6) 1 17 (3) I 19 (6) 299 (9) 41 (8) Eggs: 1st Cop. 502 k 527 k -- -- -- -- -- -- 310 (21) 276 (17)
Eggs: 2nd Cop. 243 k 311k -- -- -- -- -- -- 195 (17) 221 (I I)
Ovip. Lifespan 64 * 53 * 48 (1) 32 k 36 k 54 k 36 & -- 21 (18) 19 (17) 1.4 (6) 1.4 (3) 6.2 (4) 11.5 (8)



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19871 Henry & Busher-Green lacewings 225 single-mating reproductive potentials of individuals of those species, because other experiments described elsewhere in this paper indicate that female lacewings do not store appreciable quantities of sperm from one mating to another. Certain field-caught individuals within each species were remarkably fecund, especially considering that none was re-mated after capture. For example, some females of C. oculata and C. rufilabris oviposited more than 1000 fertilized eggs, while one female each of C. harrisii and C. downesi nearly matched that level (Figs. 1, 3, Table 2). Except for slightly higher early rates of egg-laying by C. oculata, the overall patterns shown are quite similar in all of the above species, and in fact are much the same as that seen in monogamous C. plorabunda raised in the laboratory (Fig. 2). The egg production by all once-mated females of all species, whether laboratory-reared or field-captured, is summarized in Table 2.
Egg Counts: Continuously Re-mated Females. The C. plorabunda and C. downesi females mated 1-6 times, the former species averaging a total of 780 eggs and the latter 769 (Tables 1, 3, and 4). Both species averaged two matings over an individual's lifespan. Oviposition spanned a mean of 64 days in C. plorabunda and 53 days in C. downesi, but the high variance indicates no significant interspecific difference. Lifetime patterns of egg-laying, sexual receptivity, and mating varied considerably among individuals of both species. Some females produced consistently high numbers of eggs for prolonged periods from their first fertilization, without ever recovering sexual receptivity or re-mating. Examples of this pattern can be seen in both C. plorabunda (86-4, Fig. 2) and C. downesi (FLDl, Fig. 3). More commonly, a female became sexually receptive and re-mated after a shorter time, just as her egg productivity began to dip (Figs. 2, 3, Table 5). If immediately re-fertilized, such individuals ovipos- ited large numbers of eggs again and receptivity disappeared, but without re-mating egg production soon ceased, suggesting sperm depletion. A third, rare subset of individuals recovered sexual recep- tivity many days before their egg productivity declined, as seen in females E (C. plorabunda) and B and E (C. downesi) in Table 5. Actually, receptivity in such insects waxed and waned rather errati- cally, and none succeeded in re-mating until egg production truly diminished.




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19871 Henry & Busher- Green lacewings 227 In general, females that mated more than once produced the majority of their eggs from the first copulation (Tables 3 and 4). However, a subsequent pairing could yield large numbers of eggs if earlier copulations had little issue (e.g., 1, Table 3, and B, Table 4). At their peak of egg productivity, females of either species could oviposit nearly 40 eggs per day. Despite varying rates of egg-laying and radically different lifetime patterns of re-mating, the most fecund individuals consistently laid about 1200 eggs altogether. Field-captured Meleoma emuncta females had the lowest fecun- dity of any of the lacewings studied (avg. 132 eggslfemale, Table 2). This low fecundity may be due in part to unknown dietary or envi- ronmental requirements for optimal growth and reproduction (Tauber 1969); the species is notably difficult rear (J. Johnson, pers. corn.).
Male Reproductive Potential: Continuously Re-mated Males. Males of C. plorabunda, C. downesi, and C. oculata could mate several times (Table 6). One C. downesi mated with I0 different females at 24-hour intervals, and C. plorabunda males inseminated maxima of 22 and 30 females. The highest value was posted by an individual of C. plorabunda that was re-mated at 2-day rather than 24-hour intervals; in fact, this male remained reproductively compe- tent for much of his long lifespan (210 days). Generally, the data from egg counts described a decline in male fertility with time, suggesting irreversible sperm depletion. However, the active indi- vidual was conspicuously different, maintaining high fertility even after many copulations: for example, his 20th female oviposited 620 eggs, as many as produced by females paired with fresh, virgin males. The reproductive potential of males consistently exceeded that of females in all three species studied. Again, the exceptional C. plorabunda male fathered many more offspring than any other individual: over 9600, vs. 2253 for the runner-up. The performance of this extraordinary individual, compared with the next-most- fertile male, is graphed in Fig. 4.
Egg Production vs. Copulation Time.
Chrysoperlaplorabunda had consistently shorter matings than its sibling, C. downesi (Table 7). Highest individual fecundity in the former species was associated with copulation durations of 8-10 minutes, whereas in C. downesi, longer copulations (19-65 minutes)



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228 Psyche
[Vol. 94
C. oculata
--
= 0613
A = 061
DAY 4 DAY 16 DAY 28 DAY 40 DAY 52
PERIOD of EGG - LAYING
Figure 1.
Fertile egg production as a function of time in two females of Chrysopa oculata, collected from the field. Eggs were clipped every 3 days. were optimal. C. downesi varied considerably more than C. plora- bunda in the time spent in copulo, although high variance typified both species.
Female Fecundity.
Fecundity data on many lacewing species are well summarized in Rousset (1983). Our results differ strikingly from those of other workers, in the sheer numbers of eggs produced by individual lace- wings under a variety of mating protocols. For example, even single- mated females of C. plorabunda, C. downesi, C. harrisii, C. rufilabris, and C. oculata produced 1000 or more fertile eggs (Table 2), which is significantly more than previously reported for any lacewing. Multiply-mated females increased this figure further, to 1207 in C. plorabunda and 1286 in C. downesi (Tables 3 and 4). (The champion was actually a single-mated C. oculata that depos- ited 1289 eggs in 55 days.) The literature reports individual maxima of only 617 for C. oculata (Smith, 1922), 850 for C. plorabunda (= C. carnea [Stephens]; Hagen and Tassan, 1966), and 189 for C.



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Henry & Busher- Green lacewings
\
5. plorabunda
ere-mated \/ \
PERIOD of EGG - LAYING , DAYS
Figure 2.
Fertile egg production as a function of time by two females of Chryso- perfaplorabunda, mated in the laboratory on Day 1. Eggs were clipped on a 2,2, and 3 day timetable each week.
rufilabris (Hydorn and Whitcomb, 1979; Ru et al., 1976), all reared on diets very similar to those we used. We are unable to explain these discrepancies, except to note that great variability character- izes the reproductive potential of lacewings of all species. Occasion- ally, for example, we found ourselves rearing a stock of insects with consistently low fecundity and high larval mortality, despite contin- uing efforts to avoid inbreeding. Whether such episodes were the results of genetic factors or disease was never resolved, but analo- gous problems could have unnaturally curbed egg productivity in the studies of others.
An important and perhaps unexpected result of this work was the observed uniformity of maximal individual egg production from species to species. On the one hand, it may not be too surprising to find similar maximal fecundities in very closely related, sibling spe- cies like C. plorabunda and C. downesi; but more distantly related taxa like C. rufilabris and C. harrisii and even representatives of distinct genera like Chrysopa oculata also had similar individual lifetime egg totals. Actually, even the life-history patterns of the



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230 Psyche
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PERIOD of EGG - LAYING, DAYS
Figure 3.
Fertile egg production as a function of time for two females of Chryso- perla downesi, mated on day 1 (83-3) or collected from field (FLD1). Eggs were clipped on a 2, 2, and 3 day timetable each week. siblings C. plorabunda and C. downesi differ so much that their similar fecundities seem anomalous: the former species is multivol- tine, whereas the latter is univoltine. In any case, it seems clear that individual females of either C. plorabunda or C. downesi can fertil- ize about 80 percent of their lifetime supply of viable eggs with the sperm of a single male, although this may not happen very often in nature, for reasons to be discussed shortly. Principi (1 949) obtained similar results for C. formosa Brauer, suggesting that a fertilization pattern like this may be widespread in Chrysopidae. Females in some other insect orders have also been shown to fertilize most of their eggs with the sperm of their first mate: Drosophila melano- gaster Meigen is a good example (Pyle and Gromko, 1978). The relatively low fecundity of Meleoma emuncta (Table 2) may not be typical of the species or genus, for Tauber (1969) counted 347 fertile eggs from one female fed an artificial diet fortified with levu- lose and choline chloride. In that study, a specimen of M. dolichar- tha (Navas) produced 313 eggs from the same diet. As mentioned



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Table 3.
Fecundity of individual females of Chrysoperla plorabunda that were re-mated to satiation. Ovip. Days = oviposition lifespan, as in Table 1. Only fertile eggs were tabulated. Individuals