Chrysoperla mohave (Banks) (Neuroptera: Chrysopidae): Two familiar species in an unexpected disguise.
Psyche 99:291-308, 1992.
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CHRYSOPERLA MOHAVE (BANKS) (NEUROPTERA:
CHRYSOPIDAE): TWO FAMILIAR SPECIES IN AN UNEXPECTED DISGUISE
Department of Ecology & Evolutionary Biology University of Connecticut
Storrs, Connecticut 06269
The vibrational courtship song of Chrysoperla mohave (Banks) from several widely separated sites in California is described and compared to C. downesi (Smith) and to a C. mohave-like popula- tion of the recently described species, C. johnsoni Henry, Wells, and Pupedis. Unexpectedly, C. mohave is shown to have a song very much like that of C. downesi, in contrast to the very different song of mohave-like C. johnsoni. Yet the C. downesi and C. john- soni versions of "C. mohave" are physically indistinguishable. Therefore, C. mohave is not a monophyletic taxon, but instead it is a color morph that has arisen independently at least twice in sepa- rate lineages of Chrysoperla. Both C. downesi and C. johnsoni are thus highly variable species, encompassing populations that range from solid dark green or bright green with no markings to light yellowish-green with tergal spotting and dark crossveins. It is argued that C. downesi should be taken from synonymy with C. carnea (Stephens) and recognized as a valid biological species or species complex, defined by a unique type of courtship song. Key Words: systematics, song, sibling species, courtship, reproductive isolation
My interest in green lacewings began in the fall of 1968. The preceding year, as a Junior in college, I had enrolled in an exciting undergraduate course on the biology of insects, taught by Professor Frank M. Carpenter. Carpenter had been approachable and encour- aging, so I asked him to support an undergraduate honors thesis Manuscript received 21 August 7992
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project in biology. He agreed to serve as my advisor, and sug- gested that I talk to his graduate student, Lee Miller, for some additional ideas. Miller was studying the structure and physiology of the unique ultrasound detector in the forewing of the common green lacewing, known then as Chrysopa carnea Stephens (Miller 1970). He proposed a trade: if I took over the care of his lacewing colonies, he would let me use his lacewing stocks and some of his laboratory space and equipment for my project. Before long, I was deeply involved in a study of courtship and mating behavior in this insect. By the end of the academic year, my undergraduate project was completed. It included the first description of the vibrational courtship songs that are now known to be typical of the lacewing genus Chrysoperla. Although years would pass before I returned to acoustical communication in insects, this study set the stage for all of my later research on songs, systematics and speciation. In those days, the taxonomy of the common North American chrysopids seemed relatively straightforward. Chrysoperla (for- merly Chrysopa) carnea was considered to be a widespread, hol- arctic species: Tjeder had recently synonymized nearctic C. plorabunda (Fitch) with palearctic C. carnea, unable to find con- sistent anatomical differences between the two (Tjeder 1960). Thereafter, it was assumed that the results of studies on American populations would apply equally to European or Asian populations -and vice versa. Thus, findings within local populations of C. carnea sensu lato were broadly generalized to the entire species in investigations of photoperiod and diapause (Honek and Hodek 1973, Sheldon and MacLeod 1974; Tauber and Tauber 1969, 1970), dispersal flight (Duelli 1980, 1981), defensive responses to bat sonar (Miller 1975), and resistance to common insecticides (Bartlett 1964, Plapp and Bull 1978). In addition, lacewings identi- fied as C. carnea were shipped freely all over the world in com- mercial and government-sponsored programs of biological control (Jones and Ridgway 1976, Ridgway and Jones 1969, Tulisalo and Korpela 1973, Tulisalo and Tuovinen 1975, Zeleny 1965). How- ever, those most familiar with the species were acutely aware that this unified view of C. carnea was a reflection more of ignorance than of cogent empirical data (Adams 1983, Bickley and MacLeod 1956, Bram and Bickley 1963; Adams, pers. comm.). Recognition of taxonomic diversity within C. carnea of North America (=C. plorabunda s. lat.) actually began years earlier, with
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the description of several species from local geographical areas that were later synonymized with or included as varieties of C. plorabunda. These have included C. robertsonii (Fitch), C. califor- nica (Coquillet), C. vegata (Navhs), C. downesi (Smith), and C. mohave (Banks), among others (Bickley and MacLeod 1956). Each was thought to be distinguishable from "true C. plorabunda" (or C. carnea) by different shades of green or by unique markings on the body and wings. Of these taxa, only C. downesi and C. mohave are commonly recognized and discussed today, although neither has official species status anymore (see below). Unfortunately, colors fade badly in lacewings no matter how they are preserved, so museum holotypes and paratypes have been of little use in resolv- ing taxonomic questions that concern the closely related taxa of the Chrysoperla carnea/plorabunda/downesi complex. Even in liv- ing specimens, ground color and markings, setation, body size, wing shape, and venation have been shown to vary markedly within single presumed species across relatively small geographi- cal areas (Tauber and Tauber 1986a; Tauber and Tauber 1975, 1981).
Increasing awareness of songs produced by Chrysoperla green lacewings has completely changed how we perceive species boundaries within the genus. These songs are vibrational tremula- tion signals, produced by rapid vertical oscillations of the insect's abdomen, and are transmitted between individuals through compli- ant substrates such as leaves, grass blades, or conifer needles (Henry 1979, 1980b, 1983a). No drumming is involved. Both sexes sing, and copulation depends upon a male and a female success- fully establishing a duet in which each partner alternately produces the same song phrase. Because the songs of each partner must exactly match for this to happen, populations which differ acousti- cally from one another will be unable to interbreed and should be considered separate biological species. By this criterion, C. carnea is not holarctic and monolithic, but instead consists of distinctive complexes of several species each, in both Europe and North America (Henry 1983a). The C. carnea complex of Europe remains to be analyzed (Henry 1985b), but extensive song analysis and behavioral tests of North America's equivalent C. plorabunda complex have supported the recognition of three sibling, cryptic species within it: C. plorabunda, C. adamsi Henry, Wells, and Pupedis, and C. johnsoni Henry, Wells, and Pupedis (Henry 1993,
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Henry, Wells, and Pupedis 1993, Wells and Henry 1992). These newly defined species are not clearly comparable to any of the species, subspecies, races or varieties of nearctic Chrysoperla pre- viously described in the literature. A very different type of song characterizes C. downesi, strongly supporting its taxonomic valid- ity and arguing against Garland's decision to synonymize it with C. carnea/plorabundu (Garland 1985). In fact, variation on the C. downesi song theme in different parts of North America suggests that this taxon may itself turn out to be a complex of cryptic bio- logical species (Henry l985a).
C. mohave is a special case. It appears to be closely allied to the three described species of the C. plorabunda complex, but it is uniquely characterized by numerous darkly pigmented crossveins and gradate veins in the wings (Banks 1938, Tauber and Tauber 1973). Also, the body is usually light yellowish-green, with more or less numerous brownish or reddish-brown spots on the thoracic and abdominal terga (Henry 1993). This suite of features is unknown in the C. plorabunda or C. downesi complex outside of the American southwest. Other traits that have been associated with some populations of C. mohave include semi-predaceous adult food habits and prey-mediated control of reproductive dia- pause (Tauber and Tauber 1981). Although it was finally reduced to the rank of a variety or ecotype of C. plorabunda (Tauber and Tauber 1973): it has enough distinctive traits to suggest that it might constitute a cohesive genetic unit. Certainly C. mohave is a candidate for careful analysis of courtship songs across its known geographical range.
The present study examines the songs of C. mohave collected from widely separated parts of California and identified as that species (or ecotype) by Phillip Adam, California State University, Fullerton. Results are compared to song data collected earlier on a special population of mohave-like insects from the San Francisco Bay area (Henry 1993), and to the songs of C. downesi, C. plorabunda, C. adamsi and C. johnsoni. The systematic status of C. mohave is then discussed and assessed, based on these comparisons.
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MATERIALS AND METHODS
Collection and Rearing: Living adults of C. mohave were co1- lected 20-28 September, 1987, from three relatively hot, dry sites in California, covering a north-south range of nearly 1000 km (Fig. 1). Those referred to as "Garberville" were found on the evening of 20 September in mixed stands of young Douglasfir and scrub live oak along a side street of Garberviile, California, elevation '280 m, about 22 km southeast of the Humboldt Redwoods. "Bartlett" specimens were obtained 2 1 September near the transi- tion from desert to forest, elevation =I000 m, in an open area of Springs
Figure 1. Collecting sites in California of the "C. mohave" yellow-green color variant of Chrysoperia johoni and C. downesi. Claremont, marked with a triangle, is the type locale of C. mohave (Banks).
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mixed Douglasfir and pine, along a dirt road from Route 20 to Bartlett Springs, California, ten km northeast of Clear Lake. "For- est Home" insects were taken 26-28 September in an open, diverse forest at the Forest Home Campground, California, elevation ~1650 m, in the San Bernardino Mountains. Collecting data for other mohave-like lacewings, obtained in Strawberry Canyon, Berkeley, California and assigned to C. johnsoni, can be found in another paper (Henry 1993).
Adults of C. downesi were procured in September and October, 1977-1983, from a second-growth forest of red spruce and from a young, open stand of red pine at the Huyck Nature Preserve, Rens- selaerville, New York, elevation ~650 m, about 32 km southwest of Albany. Other specimens identified as C. downesi were col- lected in 1987 at various locations in western North America, including the Bartlett and Forest Home sites described above. All insects were returned to Storrs, Connecticut for mainte- nance, rearing and song analysis. Sexes were kept apart and sup- plied with water and a WheastTM-based diet. In the laboratory, long day photoperiods (17:7 hr LID) terminated reproductive diapause in field-collected individuals and brought on sexual receptivity and spontaneous singing after 1-6 weeks. Progeny of selected mated pairs were raised under short day conditions (10114 hr LID) using established methods (Henry 1979, 1983b, 199 1). Upon eclosion, all adults were maintained under a long day photoperiod regime. This rearing protocol was designed to satisfy any obligatory dia- pause requirements of the insects (Nechols, Tauber, and Tauber 1987, Tauber and Tauber 1973b) and to facilitate rapid acquisition of sexual receptivity.
Analysis of Songs: At least five complete courtship songs (short- est repeated units or SRUs) of each presumed member of C. mohave from each locality were recorded on cassette tape and then digitized and analyzed with MS-DOS-based computer hardware and software, using methods described in previous papers (Henry 1979, 1980b, 1990; Henry and Johnson 1989, Henry and Wells 1990). Males and females were induced to sing by playing back previously recorded or artificially synthesized songs through a loudspeaker (Henry 1989). A similar protocol was applied to at least five SRUs of each individual of C. downesi. Comparisons to other species and populations used the results of analyses per- formed previously and tabulated in earlier papers.
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The songs of Chrysoperla green lacewings consist of frequency- modulated volleys of abdominal vibration repeated at regular inter- vals. Some taxa, such as C. plorabunda and C. adamsi, are characterized by relatively simple songs, composed of single-vol- ley SRUs repeated many times (Henry, Wells, and Pupedis 1993). Other species, such as C. downesi and C. johnsoni, produce more complex songs that consist of much longer, multisyllabic (multi- volley) SRUs and perhaps even two or more distinctly different types of volleys (Henry 1980a, Henry, Wells, and Pupedis 1993). The populations of C. mohave analyzed here have complex songs, very similar to those of C. downesi; I defined and measured ten song features, chosen for maximum compatibility with the song measurements published for other species (Table 1, Fig. 2). The following measurements were taken for each of the two types of volleys, long and short, found in these songs: (1) duration of each volley, (2) interval between the start of one volley and the start of the next, (3) frequency (pitch) of each volley, and (4) number of volleys per SRU. In addition, it was necessary to measure fre- quency (3, above) separately for beginning versus terminal short volleys in each SRU. Total length of the SRU (5) was also tabulated.
In total, comprehensive analyses were performed on the songs of 18 C. mohave individuals from California (1 3 from Garberville, 3 from Bartlett, and 2 from Forest Home). The sex ratio (male: female) of the total sample was 0.44. For C. downesi from New York State, the songs of 19 individuals were analyzed (sex ratio = 0.47). Comparisons were made to 3 1 additional mohave-like indi- viduals of C. johnsoni from Strawberry Canyon, described in another paper (Henry 1993).
Temperature strongly influences song characteristics, and data must be treated in some way to compensate for this if they are col- lected at different temperatures. Fortunately, a11 measurements of C. mohave were taken within half a degree of 25OC. However, data for C, downesi were obtained over several years, at temperatures ranging from 19-3 1 OC. Therefore, for that species, all individual means at different temperatures were transformed (normalized) to a standard temperature (25OC). This was done by regressing tem- perature against each song feature. When the temperature effect was significant (P<0.05), as it was for most features, the slopes of the resulting regression equations were used to modify the original
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Table 1. Means and standard errors of song features of Chrysoperla downesi (eastern U.S.A.) and mohave-like C. downesi (California). Unless otherwise noted, time is in milliseconds and frequency is in Hertz. Also shown are the results of a T- test to determine significant differences between the populations. -
Duration, long volleys
Interval, long volleys
Duration, short volleys
Interval, short volleys
Frequency, long volleys
Frequency, 1st short volleys
Frequency, last short volleys
Number of long volleys
Number of short volleys
Song Duration (total, in seconds)
values; otherwise, data were left unchanged. Calculations of basic statistics and Student's T-tests were then performed on the new data set of temperature-compensated and raw values. When appro- priate, tabulation of the residuals from the linear regression analy- sis was used to predict the mean and standard error at 25OC for each song feature (Table 1).
I used the PC software package CSS: Statistica 3.1 (Statsoft Inc., Tulsa, OK) for statistical analyses. Acquisition, display, tem-
C. downesi (east)
r---l-- I I I I I I I I I I I
0 1 2 3 4 5 6 7 8 9 1 0 1 1 1 2
Figure 2. Digitized oscillographs of the shortest repeated unit (SRU) of the vibra- tional song of mohuve-like C. johnsoni from Strawberry Canyon, California, dark green C. downesi from New York State, and mohuve-like C. downesi from Gar- berville, California. All were recorded at 25OC. poral and spectral analysis, and artificial synthesis of songs were executed using Waterfall 3.18 and Spike2 4.0 (Cambridge Elec- tronic Design, Cambridge, U.K.) and DADiSP 2.00B (DSP Devel- opment Corp., Cambridge, MA). The graphs and other figures were produced in SigmaPlot 5.0 (Jandel Scientific, Corte Madera, CA) and CorelDRA W 3-0 (Core1 Systems Corp., Ottawa, Canada). All programs ran under MS-DOS on an 80286 computer. Analysis of Morphology: All living, field-collected individuals of C. mohave were examined under a dissecting microscope, to iden- tify external morphological features that might vary among geo- graphical populations or between morphs. The genitalia of two preserved C. mohave males from Garberville and two more from
300 Psyche [Val. 99
Forest Home were prepared for closer study by clearing the last few segments of the abdomen in hot 10% KOH for 15-30 min, as described by Bram and Bickley (1963). Sclerotized regions were enhanced by staining for two minutes in 5% Chlorazol Black E aqueous solution. The genitalic structures were then everted using a small pipette and placed in a drop of glycerin for examination under a compound microscope. These preparations were compared to those of eastern C. downesi and mohave-like C. johnsoni geni- talia made earlier (Henry, Wells, and Pupedis 1993). Voucher specimens, pinned or in 70% ethanol, have been deposited in the personal collection of Charles S. Henry or in the collection of the Connecticut State Museum of Natural History, the University of Connecticut, Storrs.
Oscillographs of the vibrational songs (SRUs) of a mohave-like C. johnsoni from Strawberry Canyon, a C. downesi from New York State, and a C. mohave from Garberville, California are shown in Fig. 2. Each exhibits the volley duration, interval, and amplitude structure typical of its population at 25OC. The songs of C. downesi and Garberville C. mohave are compared further in Fig. 3, which shows the frequency (pitch) structure of the songs as computer-generated sonographs. The figures establish that the song of C. mohave from sites outside of Strawberry Canyon is very similar to that of classic C. downesi, and bears no resemblance to the song of its closest look-alike, C. johnsoni from Strawberry Canyon. When the temperature-corrected means of each song fea- ture were compared between C. mohave and C. downesi, the strik- ing similarity of the two populations was confirmed. Even though the comparison was between populations on opposite sides of the continent, T-tests revealed only minor differences (Table 1). Basi- cally, C. mohave has a lengthier song than C. downesi, distin- guished by more and longer volleys of both kinds, and the interval between its short volleys is less. But without seeing the striking color differences that separate them, it would be easy to consider C. mohave and C. downesi a single, homogeneous species. In a parallel manner, mohave-like C. johnsoni from the Berkeley area is acoustically indistinguishable from other, more typically pig- mented C. johnsoni from the Pacific Northwest, central and south- ern California, and southwestern Arizona (Henry 1993). Its song is
C. downesi, eastern U.S.A.
"C. mohave, " Garberville, California
Figure 3. Computer-generated sonographs of the SRU of typical dark green C. downesi from New York State and mohave-like C. downesi from Garberville, Cali- fornia, at 25OC. The sonograph shows frequency (tonal or pitch) changes with time, for the duration of each song.
302 Psyche [vo~. 99
so different from that of C. mohave/downesi that it is not clear how to begin any comparison. Two other sibling species, C. plorabunda (sensu stricto) and C. adamsi, were not considered further in this study, because neither exhibits mohave-type morphology. Also, they are even less similar to C. mohave/downesi in the structure of their songs than is C. johnsoni (Henry 1993). Externally, all C. mohave featured some degree of yellowish ground color, tergal spotting, and darkening of crossveins. So also did all individuals of mohave-like C. johnsoni from Strawberry Canyon, and in fact the latter could not be distinguished from the former using external morphology. More detailed studies of the male genitalia of several specimens from each taxon failed to reveal any uniquely different character states that could be of sys- tematic use.
The results clearly show that C. mohave, collected over a wide geographical range in California, shares its song with C. downesi and is almost certainly a member of that species. However, earlier results just as emphatically placed similarly defined "C. mohave" in the new species C. johnsoni, again based on song structure (Henry 1993). Yet there is little resemblance between C. downesi and C. johnsoni in any other way: not only are their songs com- pletely dissimilar, but the former is typically a much deeper green color than the latter. Two conclusions emerge from this. Neither conclusion is new or original at first glance, but each demands an important revision in the way we should approach the systematics, ecology, population genetics, and general biology of Chrysoperlu in the future.
First, C. mohave is not a valid clade, and therefore should not be recognized, even as a variety or ecotype. It is polyphyletic, hav- ing arisen in two independent (though very closely related) lin- eages. Of course, C. mohave even now has no official validity, having been synonymized with C. carnea (=C. plorabunda s. lat.) some years ago (Tauber and Tauber 1973). However, it continues to figure in detailed models of nutritional and photoperiodic con- trol of seasonal diapause, evolution of seasonal adaptations and life history traits, geographic polymorphism in ecophysiological responses, and sympatric speciation (Tauber and Tauber 1982,
19921 Henry 303
1987, 1989; Tauber and Tauber 1973a). Without sure knowledge of the species affiliation of the particular "mohave" being investi- gated, even the most careful, elegant experiments will generate misleading or meaningless results. Thus, much of the Taubers' work on Strawberry Canyon C. mohave probably applies to C. johnsoni, in the C. plorabunda species complex, but is not at all applicable to other California populations of C. mohave belonging to the C. downesi complex. Nor is it certain that C. mohave col- lected at any given site is the same entity from year to year or even from individual to individual: Chrysoperla spp. are renowned for their dispersal capabilities (Duelli 1980), and several different species are often sympatric or syntopic at western North American sites (Henry 199 1). Every field-collected individual must be placed in its correct species, based on courtship song, before any other work can be done.
The second conclusion is that acoustically defined species such as C. johnsoni and C. downesi are not necessarily homogeneous in their external appearance or biology. Again, the polymorphic nature of several species within Chrysoperla has already been rec- ognized and described, but that was when many different forms were still included within a monolithic, holarctic C. carnea (Tauber and Tauber 1986b) and C. downesi was defined by color alone (Tauber and Tauber 1981). It is now known that C. johnsoni, formerly considered part of C. plorabunda s. lat., encompasses populations whose colors vary from light yellowish-green to bright green, some of which remain green in winter diapause and others of which turn brown while hibernating or aestivating (Henry 1993). More surprisingly, the present study shows that C. downesi is also extremely variable in color. It is no longer acceptable to assign all dark green, nearctic Chrysoperla with carnea-type male genitalia to C. downesi. In fact, some are among the yellowest pop- ulations yet encountered in the genus.
Throughout this paper, I have assumed that C. downesi is a valid species, even though it is presently in synonymy with C. carnea-and therefore, presumably, with some unspecifiable mem- ber of the C. plorabunda species complex. Support for its validity comes from the unique structure of its courtship song (Henry 1980a), which is so different from the songs of the three species in the C. plorabunda complex. The C. downesi song varies region- ally, but is always recognizable in populations across the entire
304 Psyche [VOI. 99
width and breadth of the North American continent. Based on what we know of the songs of hybrids produced between eastern C. downesi and C. plorabunda in the laboratory (Henry 1985b), C. downesi seems not to hybridize with other species in nature: indi- viduals with hybrid songs have not been found in the field, in spite of extensive collecting. Thus, all evidence indicates that C. downesi is a monophyletic clade, and that it should have its species status reinstated. But as in C. johnsoni, distinctive color forms like "C. mohave" probably do not respect species boundaries within the C. downesi species complex. Instead, single biological species may show a wide range of color patterns and life-history traits in differ- ent regions, perhaps through adaptation to local conditions. The reasons for the parallel evolution of mohave-like morphol- ogy in at least two lineages of lacewings are unknown. One can speculate that these morphs are restricted to dry areas with highly seasonal precipitation patterns, and that the yellow-green ground color and dark crossveins camouflage the insects against desic- cated vegetation. Yet one of the driest regions collected, the Kofa Mountains of southwestern Arizona, supports a bright green popu- lation of C. johnsoni that remains green even during the winter (Henry 1993). Also, mohave-type individuals of C. downesi at the dry Bartlett Spring site coexist with typical dark green C. downesi, which seems contrary to the camouflage hypotheses (C.S.H., unpublished data). Clearly, much hard work remains to be done on the systematics and ecology of the C. downesi complex. Recogniz- ing the true, biologically-defined species boundaries within this and the other sibling species complexes of Chrysoperla will greatly facilitate our understanding of all aspects of their biology and prevent potentially costly scientific mistakes. This study was supported in part by National Science Founda- tion Award BSR-8508080 to Charles S. Henry and by the Research Foundation of the University of Connecticut. I thank the following for help in collecting and maintaining living lacewings from North America: Marta Martinez Wells and Julie J. Henry (University of Connecticut, Storrs); J. B. Johnson (University of Idaho, Moscow); Phillip A. Adams (California State University, Fullerton); Ray- mond Pupedis (Yale University); and Norman D. Penny
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(California Academy of Sciences, San Francisco). I dedicate this paper to my mentor and friend, Professor Frank M. Carpenter, who has managed so often to recognize and encourage hidden strengths in his students and associates, thereby coaxing from them their very best work.
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