James B. Johnson

Discovering the True Chrysoperla carnea (Insecta: Neuroptera: Chrysopidae) Using Song Analysis, Morphology, and Ecology

Abstract What was once considered a single Holarctic species of green lacewing, Chrysoperla carnea (Stephens), has recently been shown to be a complex of many cryptic, sibling species, the carnea species group, whose members are reproductively isolated by their substrate-borne vibrational songs. Because species in the complex are diagnosed by their song phenotypes and not by morphology, the current systematic status of the type species has become a problem. Here, we attempt to determine which song species corresponds to Stephens’ 1835 concept of C. carnea, originally based on a small series of specimens collected in or near London and currently housed in The Natural History Museum. With six European members of the complex from which to choose, we narrow the field to just three that have been collected in England: C. lucasina (Lacroix), Cc2 ‘slow-motorboat’, and Cc4 ‘motorboat’. Ecophysiology eliminates C. lucasina, because that species remains green during adult winter diapause, while Cc2 and Cc4 share with Stephens’ type a change to brownish or reddish color in winter. We then describe the songs, ecology, adult morphology, and larval morphology of Cc2 and Cc4, making statistical comparisons between the two species. Results strongly reinforce the conclusion that Cc2 and Cc4 deserve separate species status. In particular, adult morphology displays several subtle but useful differences between the species, including the shape of the basal dilation of the metatarsal claw and the genital ‘lip’ and ‘chin’ of the male abdomen, color and coarseness of the sternal setae at the tip of the abdomen and on the genital lip, and pigment distribution on the stipes of the maxilla. Furthermore, behavioral choice experiments involving playback of conspecific versus heterospecific songs to individuals of Cc2 and Cc4 demonstrate strong reproductive isolation between the two species. Comparison of the adult morphology of song-determined specimens to that of preserved specimens in the original type series and in other collections in The Natural History Museum, London, indicate that the ‘true’ Chrysoperla carnea (Stephens) is Cc4. Cc2 cannot be confidently associated with any previously described species and is therefore assigned a new name, Chrysoperla pallida sp. nov., and formally described.

Chrysoperla lucasina (Lacroix): a distinct species of green lacewing, confirmed by acoustical analysis (Neuroptera: Chrysopidae)

The existence of cryptic, sibling species, distinguished principally by vibrational courtship songs, has been confirmed for the carnea‐group of Chrysoperla green lacewings in Europe and western Asia. One member of this species‐group, C.lucasina (Lacroix), is characterized by several morphological traits as well, but its taxonomic validity has been considered uncertain due to the subtle and variable nature of those traits. Here, we describe the calling and courtship songs of C.lucasina, which uniquely distinguish that taxon from all other members of the carnea‐group in Europe. The male of C.lucasina produces two slightly but consistently different types of songs, one while calling and the other while dueting with a female. The female produces just one type of song, identical to the male’s calling song, which is used for both calling and dueting. Measured features of the songs of C.lucasina are nearly invariant over a broad geographical area, from the Canary Islands to Cyprus and from northern Africa to the U.K. Similarly, at least one morphological feature, the presence of a dark stripe on the pleuron of the second abdominal segment, characterizes all adult individuals identified acoustically as C.lucasina. Furthermore, larval head markings vary little among different populations of the song species. We conclude that C.lucasina is a valid biological species, which can also be recognized in museum collections by a suite of morphological attributes. We also briefly compare the songs and adult morphology of C.lucasina with five other currently unnamed song species of the carnea‐group whose geographic ranges overlap extensively with it.

Obligatory duetting behaviour in the Chrysoperla carnea-group of cryptic species (Neuroptera: Chrysopidae): its role in shaping evolutionary history

An unusual system of communication has evolved in green lacewings of the Chrysoperla carnea‐group, triggering rapid proliferation of numerous cryptic species across all of the Northern Hemisphere and large portions of Africa. The system is based on sexually monomorphic, substrate‐borne vibrational signals, produced by abdominal oscillation. These low‐frequency signals are exchanged between courting individuals in a precise duetting format. The song of each of the more than 20 described species exhibits a unique acoustical phenotype that reproductively isolates the taxon from all other species with which it might come into contact. Here, we review what is known about duetting behaviour in the carnea‐group, emphasizing the dominant role that duetting has played in the evolution, ecology, and speciation of the complex. Included are descriptions and discussions of song diversity and its impact on reproductive isolation among species, the genetic basis of interspecific song differences, partitioning of acoustic space among sympatric species, parallel song evolution in allopatric species pairs, and modes of speciation within the complex. We also emphasize the importance of correctly identifying by song all species of the carnea‐group that are to be used either in experimental studies or programs of biological control, while acknowledging the continuing relevance of morphology to carnea‐group systematics.

Revised concept of Chrysoperla mediterranea (Holzel), a green lacewing associated with conifers: courtship songs across 2800 kilometres of Europe (Neuroptera: Chrysopidae)

The Holarctic carnea‐group of Chrysoperla green lacewings consists of numerous cryptic, sibling species, distinguished principally by vibrational courtship songs. A European member of this species‐group, C. mediterranea (Hölzel), was originally diagnosed by its dark green coloration, red band across the front of the head, narrow wings, minute basal dilation of the pretarsus and ecological association with pines. Here we describe its courtship and mating song, which uniquely distinguishes the species from all other members of the carnea‐group in Europe. Males and females both produce a single type of song, characterized by a long train of short, closely spaced volleys and nearly constant carrier frequency. Measured song features are nearly invariant across a large geographical range that extends well outside that previously known for C. mediterranea. Principal components analysis confirms the uniqueness of the mediterranea song in comparison with five other sympatric song species of the carnea‐group. Populations which show the mediterranea song phenotype do not necessarily retain all of the traditional morphological features of the species, particularly in eastern parts of the range. Specifically, the green coloration may be less intense, the wings broader and the pretarsal basal dilation larger, resulting in significant morphological overlap with other song species. Larval morphology and ecophysiology also fail to distinguish C. mediterranea from other song species. Based on unique song phenotype, however, we conclude that C. mediterranea is a valid biological species, which can also be recognized in museum collections when a suite of physical attributes is used.

A lacewing with the wanderlust: the European song species ‘Maltese’, Chrysoperla agilis, sp.n., of the carnea group of Chrysoperla (Neuroptera: Chrysopidae)

Abstract. A fifth European member of the Holarctic carnea sibling species group, Chrysoperla agilis, sp.n. is described. This species was initially recognized because of its unique song phenotype. Both sexes produce one type of song, characterized by a single very long volley averaging 4.5 s in duration and repeated every 9.5 s. The unit of exchange during heterosexual duets (the shortest repeated unit) is the single volley. The carrier frequency is upwardly, then downwardly, modulated during each volley. The maximum frequency is higher (around 110 Hz) than in other members of the carnea group. Each volley ends with an audible, percussive ‘rattle’. Song features vary only slightly over a large geographical range that extends from northern Iran westward to the Azores and northward to southern Switzerland. Discriminant function analysis confirms the uniqueness of the C. agilis song in comparison with nine other song species. Morphologically, the adult of C. agilis is very similar to C. carnea and C. pallida and is generally intermediate between them with respect to the size of the pretarsal basal dilation, the shape of the genital lip and chin, the colour and type of setae on the abdomen, and colour markings on the head and mouthparts. No single feature will distinguish C. agilis from either C. carnea or C. pallida, but a suite of physical attributes can be used with reasonable success. Larval morphology fails to distinguish clearly C. agilis from other song species. Ecologically, C. agilis shares an affinity for low vegetation with C. lucasina and C. carnea, and a preference for milder, Mediterranean climates with C. mediterranea. Adults undergo a colour change to pale yellowish brown during winter diapause, and eggs are laid singly rather than in groups. Based on its ecological characteristics, C. agilis may prove to be an effective agent of biological control in the agricultural fields of warmer, drier parts of southern Europe and the Middle East, where other members of the carnea group are less common or absent.

Courtship song of the South African lacewing Chrysoperla zastrowi (Esben-Petersen) (Neuroptera: Chrysopidae): evidence for a trans-equatorial geographic range?

The taxonomic status of green lacewings of the Chrysoperla carnea group from Africa and the Arabian Peninsula is investigated using comparative analyses of substrate‐borne vibrational songs, adult morphology, larval morphology and ecology. For the first time, the courtship song of C. zastrowi (Esben‐Petersen) is described and compared to the songs of other Eurasian taxa. This South African species is the only known representative of the carnea group from the Southern Hemisphere, yet both acoustically and morphologically it shows a striking resemblance to a previously undescribed song morph, Cc5, from the Arabian Peninsula. In fact, Cc5 and C. zastrowi are so much alike that they are here considered to be a single species, characterized by single‐volley songs of relatively long duration and carrier frequencies that lack complex harmonics and that sweep downward during the course of each volley. The two taxa also share several other traits, including nomadic habits, light green colour, identically shaped external genitalia in the male, small basal claw dilation, similar markings on the genae, clypeus and frons of the adult head, and similar larval head markings. However, the taxa are sufficiently different in song, morphology and geographic distribution that they are best considered distinct subspecies. Cc5 is, therefore, formally described as C. zastrowi arabica n. subsp., leaving the nominate species as C. zastrowi zastrowi. We surmise that C. zastrowi likely originated from Cc5 or a Cc5‐like ancestor in the Northern Hemisphere, where all other members of the carnea group of cryptic species are presently found.

Association of the wheat stem sawfly with basin wildrye.

The association of the wheat stem sawfly (Ccplus cinctur Nor-t., Hymenoptera:Cephidae) and basin wildrye (Efymus cincrcus Scribn. & Merr) was investigated ln 2 wildrye stands in southern Idaho during the summers of 1982 and 1983. From 62 to 88% of wiidrye plants were infested with the sawfly at the Idaho National Engineering Laboratory and Craters of the Moon National Monument. Plant phenoiogy was a good predictor of sawfly emergence. Larvae that developed within cuims consumed vascuiar tissues and may have impaired transport of water and carbohydrates. Seed weight and the number of caryopses developing within wiidrye florets were signlflcantly reduced in cuhns containing sawfiy larvae (p<O.O06 and KO.018, respectively). Germination rates of seeds from infested and non-infested culms were not significantly different (p>O.OS).

A new cryptic species of the Chrysoperla carnea group (Neuroptera: Chrysopidae) from western Asia: parallel speciation without ecological adaptation

Parallel (or convergent) evolution of vibrational mating songs between species confined to different continents has been found several times in the Chrysoperla carnea species‐group of cryptic (morphologically indistinguishable) green lacewings. Repeated parallel speciation resulting in taxa that differ in duetting songs but not in appearance or ecology suggests an atypical mode of speciation, one that need not involve ecological adaptation. Here we describe an additional example of convergent song phenotypes reflecting parallel nonadaptive speciation, between the common North American species Chrysoperla plorabunda (Fitch) and a newly discovered species that appears to be widespread in western Asia. To support the hypothesis of parallel evolution, we describe the song of the new species in detail, comparing it to that of C. plorabunda and demonstrate their acoustical similarity. Results of song playback trials are then presented, showing that the songs are also functionally (behaviourally) indistinguishable between individuals of both species and could not prevent hybridisation if the two species were sympatric. We demonstrate that the new species is very similar in morphology and ecology not only to C. plorabunda, but also to at least four other species in the carnea‐group that co‐occur with it in western Asia. To reject the alternative hypothesis that C. plorabunda and the new species are alike simply due to common ancestry, we show that they occupy relatively distant positions in a phylogenetic analysis of 4630 base pairs of protein‐coding mitochondrial DNA. We then formally describe the new species as Chrysoperla heidarii sp.n., including with this description observations of its behaviour, ecology and life history.

The most important lacewing species in Indian agricultural crops, Chrysoperla sillemi (Esben-Petersen), is a subspecies of Chrysoperla zastrowi (Esben-Petersen) (Neuroptera: Chrysopidae)

Across the Indian subcontinent, the agriculturally important Chrysoperla carnea species-group of Chrysopidae is represented by a single common species, Chrysoperla sillemi (Esben-Petersen, 1935). However, the cryptic species within the carnea group can be reliably distinguished from one another only by their substrate-borne vibrational duetting songs. Therefore we analyse mating signals recorded from C. sillemi collected at several Indian sites between latitudes 11°N and 31°N. Feature by feature comparison of courtship songs indicates that all the C. sillemi tested conform acoustically to the subspecies C. zastrowi arabica Henry et al. 2006 from the Middle Eastern region. Adult and larval morphology confirm that diagnosis. Here, we revise the nomenclature of the carnea group of Chrysoperla Steinmann 1964 to reflect our findings, and erect Chrysoperla zastrowi sillemi stat. rev. to include both the Indian and Middle Eastern populations. Chrysoperla zastrowi arabica Henry et al. 2006 becomes a junior synonym of the new subspecies.

Arthropod Diversity and Abundance on Feral and Cultivated Humulus lupulus (Urticales: Cannabaceae) in Idaho

Abstract The diversity and abundance of arthropods in feral and cultivated hop, Humulus lupulus L., in the major hop producing area of Canyon Co. in southern Idaho was measured during 2000 and 2001 from leaf and vacuum samples. A total of 133 arthropod species was collected from cultivated and feral hop during the 2-yr study. More species were collected using vacuum than leaf samples, but both methods indicated that feral sites were more diverse than cultivated sites. For leaf samples, the higher diversity of feral sites resulted from greater species evenness in feral than in cultivated sites. For vacuum samples, species evenness was similar, and species richness higher, in feral compared with cultivated sites. Cultivated hop had 5–10 times as many Tetranychus urticae Koch/leaf than feral hop; however, no statistically significant differences in the number of T. urticae/leaf on cultivated and feral hop were detected in either year. Hop plants in feral sites were infested with a greater number of Phorodon humuli (Schrank) in 2000 but not in 2001. The diversity and abundance of phytoseiid predators of T. urticae, did not differ between feral and cultivated hop.