K. W. Cooper.
Sexual Biology, Chromosomes, Development, Life Histories and Para sites of Boreus, Especially of B. notoperates. A Southern California Boreus. II. (Mecoptera: Boreidae).
Psyche 81:84-120, 1974.

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SEXUAL BIOLOGY, CHROMOSOMES, DEVELOPMENT, LIFE HISTORIES AND PARASITES OF BOREUS,
ESPECIALLY OF B. NOTOPERATES.
A SOUTHERN CALIFORNIA BOREUS.
11. (MECOPTERA : BOREIDAE) *
BY KENNETH W. COOPER
University of California, Riverside
California 92502
This, the second of three accounts devoted primarily to Boreus notoperates Cooper, deals with aspects of its life history. The sub- jects include, among others, sex ratio, mating, developmental stages, a brief comparative aCCQUnt of its cytology, its host mosses and pecul- iar adaptation to a life in their thin sods on diorite boulders in a region annually subject to long periods of drought and considerable heat. All of this is placed in a framework of what is now known for the other species of Boreus on these topics. Though some fifty or so articles are referred to or discussed that are devoted to, or comment upon, Boreus, there are an additional sixty to seventy more papers and accounts which, though all have been consulted, either do not bear directly on the topics treated, or seem wholly derivative. My choice of references is based upon their substantial treatment of a subject, their content of new observations or ideas, or the need to correct a standing error. To these sources, I have added my own unpublished observations on B. brumalis Fitch and B. niworiundus Fitch where relevant. The overall aim, then, is to draw together, to compare, and, where possible, to generalize what is known of the species of Boreus on the topics presented and on which I have information derived from B. noboperates. Among the matters given emphasis are: the likelihood that species of Boreus have a sex ratio approaching equality (a debated topic) ; the fact that B. notoperates is the only species (of eight for which information is known) that deviates in its mating; the curious re- ciprocal intromission at mating by male and female alike, and the anatomical relations of their parts; the conservative nature of the chromosomal cytology of Boreus and other scorpion flies as compared with Panorpa; the prevalence of a larval epistomal suture, which *Manuscript received by the editor February 10, 1974. 84




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19741 Cooper - Bonus 85
bears upon the tenability of the order Neomecoptera that specially sets Boreus apart from other scorpion flies; the likelihood that Boreus, like other Mecoptera, has four larval instars; the occurrence of both pupal and adult pharate stages in development; that whatever limits the distribution of a species of Boreus, it is not its host mosses ; and finally, that Boreus species, despite their peculiar life cycle, may have an obligate hymenopterous parasite, a matter which puzzled Withy- combe. The third and final article will deal with the range of habi- tats species of Boreus have entered, the mosses with which Boreus species are associated, interpretation of Boreus as a winter insect, and a reconsideration of its distribution in relation to drift and glaci- ation.
Boreus notoperates has so far been collected at two localities only, both being NW faces of steep canyons, at 121gm altitude (Cold- water Canyon) and at 1645111 (Black Canyon), on Mt. San Jacinto, Riverside Co., California. The first is a yellow pine - chaparral ecotone (Pinus ponderosa Dougl. - Adenostoma fasciculatum Hook. and Arn.) that is Upper Sonoran, or Upper Austral in Merriam's ( 1898) original sense, the mean temperature for the six hottest weeks (July through mid-August) being -q0C. The second is a mixed woods of yellow pine, incense cedar, white fir and canyon oak (Pinus ponderosa, Libocedrus decurrens Torr., Abies concolor Gord. & Glend., and Quercus chrysolepis Liebm.), fringed and penetrated by chaparral elements; it is Transitional, the corresponding high mean temperature being about 21 OC. Over the period 1955 - 7 I the mean annual precipitation (close by at the Idyllwild Fire Station, alt. 1645m) was 59.6 cm (23 in.), with 74% falling in the months of November through March during which adult B. notoperates have been collected. The adults have so far been found only on mosses growing on boulders and large jointed blocks of diorite, or on snow about them, in both fairly open (chiefly Coldwater Canyon) and shaded (chiefly Black Canyon) situations. Even during the period of winter precipitation the mosses are only periodically dampened and luxuriant, for precipitation is widely scattered, and melts rapidly when snow. The activity of Boreus at all its stages coincides with those periods, frequently brief and generally spaced out, when rhe mosses and their roots are damp. At other times the relative humidity is low, the mosses are dry to the touch, even friable, and their sods



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86 Psyche [March
crumbly or powdery. In periods of desiccation Boreus are found, if at all, with difficulty, unless a special method is used. The earliest that adult Boreus notoperates have been taken was mid-November, several days following the second snowfall of an inch or more, although it is likely that a snow or a soaking rain in Octo- ber would bring them forth to judge from laboratory emergences of pupae collected in mid-August. Thereafter adults have been found during the damp periods in all months until mid-March, when they become rare. Air and surface temperatures have been mild when adults have been collected, ranging from a low of 6.iå¡ to 18.3'C, though in the November through March interval below freezing temperatures are not uncommon, mean low temperatures for these months ranging from -4.2OC to 3.zå¡C with absolute lows to - 12.2OC.
The sex ratio among adult B. notoperates from field collections, though slightly skewed toward an excess of males early in the season, of females late in the season, does not depart from equality; thus: I3 I c-3 d", 150 $ $? (of which 32 of each sex were collected as mated pairs) ; chi-squared gives 0.3 > P > 0.2. Nor is there a departure from equality among immature stages collected in mid-August and early September. For 47 such larvae and pupae we have: 29 late instar larvae and p'harate pupae of which: I 9 sexed by dissection of gonads, giving : I 2 ~3' , 7 Q Q ;
10 pupated, giving: 68 8, 4 $? 9 ;
18 pupae when found, of which : 7 c? d , I I Q ;
which gives a sex ratio of 25 d 6 : 22 9 9 , for which 0.7 > P > 0.5. Now Strubing (1950) has shown from extensive field and lab- oratory observations that males of Boreus hyemalis (L.) do not tend to emerge earlier than females in the autumn. They do, however, tend to die off somewhat earlier than females, and this has been claimed or inferred by others both from field and laboratory observa- tions (e.g., Withycombe 1922, Syrns I 934, Cotton 197 I ; and for B. westwoodi Hagen, Brauer 1855; for an undescribed species?, Kolenati 1847) l. My own observations on B. notoperates are in lstrubing (1950) gives strong reason to believe that Brauer's species is almost certainly B. we'stwoodi, and not B. hyemalis as he and others have thought. Furthermore, Pliginsky (1930) states that Kolenati's specimens, from the glacier of Aar (Kazbek, Kaukas), no longer can be found, and are very likely an undescribed species. From Kolenati's comments, they fall among the species with a reduced antenna1 joint number (4).



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19741 Cooper - Boreus 87
agreement. But it has also been claimed, as early as Hardy's (1848) and MacLachlan's (1868) notes, that the sex ratio of Boreus is spanandrous, but only loosely in Marchal's ( I 9 I I ) sense, namely
that males regularly make up a minority of the population. Not surprisingly, small collections of Boreus may show a predominance of one sex. In gener,al, however, collections of two dozen or more specimens at a locality, but not made at the season's close when females do tend to predominate, give sex ratios which approximate equality, as do those for B. notoperates. There are, however, excep- tions. But for none of the following records is there a significant departure (namely, P < 0.05) from equality of the sexes: I. B. brumalis Fitch 27 c? d' 26 ? $ (Hanover, N. H., Cooper, unpubl.)
2. B. coloradensis Byers
21 20 (BY~~s 1955)
3. B. unicolor Hine
64 57 (Chapman 1954)
4. B. hyemails (L.)
39 41 (sifting, Druet & Le-
gros, ex Lestage I 94 I )
33 45 (table I, to Dec. 20,
Strubing 1950)
103 I 10 (table 4, not text p. 84,
Strubing I 950)
I9 I I (Schui-mann, ex Strub-
ing 1950)
3 8 45 (pitfall traps, Cotton
1971
j. B.westwoodi Hagen 60 64 (Martynova1954) 24 25 (Martynova1954)
12 14 (Martynova 1954)
6. B. bey-bienkoi Tarb. 56 49 (Tarbinsky1960) As exceptions, with probabilities < 0.02 to < 0.001 as random departures from equality of the sexes, we have: 7. B. nivoriundus Fitch 42 8 23 $9 (Hanover, N. H. Cooper, unpubl.)
8. B. hyemalls (L.) 398 123 (Steiner 1937) 9. B. westwoodi Hagen 97 67 (3 collections, data homogeneous, Fj ellberg
& Greve I 968)
Judging by records
1-6, and from the proportions among im-
mature stages which have been sexed, the records 7-9, all of which show a significant preponderance of males, may reflect a tendency for



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88 Psyche [March
males to wander widely at times in search of females, 01- true pecu- liarities of the particular populations, or perhaps of the mode or circumstances of collecting. Strubing's ( I 950) laboratory rearings of B. hyemulis gave 408 d, 36 $9, and Fraser's (1943) account implies that his collection (in September) of pupae of B. hyemalis consisted of 29 d d' , 21 $9 (for which 0.3 > P > 0.2). My own collection of larvae, pharate pupae, and pupae of B. nivoriundus in August, at the same site in Hanover, N. H., at which the adults scored in 7 above were later collected (December to mid-April), gave 30d d, 33 $? . Pupae of B. brumalis collected (from October to mid-November) at Princeton, N. J., likewise do not depart from an equality of sexes : 40d 8, 46 $? Q . As Striibing ( 1950) concluded, the sex ratio in Boreus appears to be close to unity for both immature stages and adults, as is the case for B. notloperates. The answer to Lestage's (1941 ) question "is there spanandry in Boreus?" must be: "not so far as known, and perhaps not at all," as Lestage suspected. Indeed, the only significant departures so far recorded are in fact spangynous, not spanandrous.
Mated pairs of B. notoperates are found chiefly on patches of damp moss, free of snow, from early in November to near the middle of March. Although Fraser (1943) claimed B. hyemalis to be cre- puscular, there seems to be no special time of day that is favored for mating by B. notoperates if the temperature is mild; nor is light a requirement, for B. notoperates mates readily in the dark (in an incubator, at gå¡C) In but one case (of 33) has a mated pair been found on the snow, and that mated pair had most likely fallen a foot or so out onto the snow from a steep, moss-covered rock-face. Cer- tainly the suggestion that Boreus occurs on snow because it is easier to find mates there is implausible; the rule seems to be that mating generally occurs on or in moss, where they congregate when it is available to the insects.
Nine complete matings of B. notoperates have been observed, namely from the first attempts of the male to gain a partner to the completion of intromission, as well as a good many partial sequences from all stages in the routine. B. notoperates is without a courtship, just as in the three species for which the course of events of mating have been described, namely B. westwoodi (Brauer 1855, 1863,



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Sauer I 966) perhaps Svensson I 96b2) ) B. hyeiizalis ( Withycombe 1926, syms 1934) steiner 193'7)) and B. brumalis (cooper 1940) Crampton 1940). From its very onset the affair is between a "coy)' female acting as though bent on escape, and an aggressive) though not necessarily persistent) male. An ardent male) when within some millimeters range) springs at the female) ensnaring her with his tong- like wings while seizing whatever he can of her extremities with one or both of his genital claspers (or gonostyles). If he fails to gain a hold) as he occasionally does) the female leaps away and is not directly pursued. Thereafter the male either takes a waiting stance on a sprig of moss) or courses about the moss) in both cases twitching his wings and opening and flexing his gonostyles from time to time.3 When chance again presents another or the same female) the male attempts once again to gain a firm hold of the female. When a mating spring has been successful^ the male may have seized a female by a posterior femur (5 cases)) a mid-tibia (2 cases)) a pro- tarsus (I case)) or the antennae ( I case). In some other instances, in which only a part of the mating routine was followed) males had gained holds simultaneous1y of both a mid- and fore-tarsus) or a fore- tarsus and antenna) or a mid- and hind-tibia) and so on. The initial hold thus seems fortuitous and not limited to a particular appendage or to but one appendage at a time. Depending upon the particular grip of the gonostyles, and the appendage(s) seized) a male may either face opposite to the captured female (7 cases)) and may even be chiefly behind her) or face in the same direction as his partner. When a female's femur or tibia has been grasped) a male) without loosening or losing his hold) can generally draw his own body about to a position at right angles to that of the female by forcibly rotating her appendage, but he cannot wholly reverse the direction in which he faced without obtaining an entirely new hold) as he must when initially facing I go0 away from hi? partner. Once seized) the female's response is immediate and energetic, as though designed to free her from the clinging, intermittently passive, male. She drags the male on his back) his side) or even vertically on his hypopygium) over and through obstacles presented by the moss and debris. Occasionally the male acts to resist) splaying his legs outward as though a drag-anchor) or clutching at the moss) offering *? Also Svensson (19661, whose account must refer to B. westwoodi, to B. hyemalis, or to both.
'Terminology referring to the external male "genitalia" follows Michener (1944).




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90 Psyche
[March
such resistance to the female as he can. From time to time the female rests, and may even pause to feed at rosettes of young moss leaves. At such times the male becomes enlivened, rights himself, turns the length of his body at right angles to the female's while still holding his original grip with his gonostyles, and swiftly (and repeatedly) arches backward over the female in an endeavor to gain firm grasp of her body with his wings. If he fails and rests) the rebellion of the female returns unabated and continues, as just described, until the male succeeds in subduing her, or she finally rids herself of himm4 Should the male succeed in gaining a firm hold with his stiff, spined and hooked wings, he deftly changes grip with his gonostyles so that he now faces in the same direction as the female. Once a position has been attained from which he can rear backward and to the side of the female, and grasp her between her head and mesono- tum with his wings, holding her body parallel to his own) he again quickly moves his gonostylar grip forward. Once a sufficiently for- ward grip with the gonostyles has been gained, the head of the female now being behind the male's forebody, he rears strongly backward a number of times and rakes and manipulates the female's rostrum and antennae with his spined wings as he falls forward again. Should he gain hold of the female's pronotum with his wings, he may move his gonostylar grip from the female's legs to clutch one or both antennae, and then briefly but smartly, drag her about by the anten- nae. Mauling of the antennae is quickly followed by a wholly passive state on the part of the female who thereafter stands as though mes- merized. Surprisingly, on the initial assault in one case, the male seized the female's antennae with his gonostyles; that female there- upon became submissive without a struggle. When the standing female has become passive, the male (still anterior to the fe~nale and gripping an appendage with his gonostyles) again bows backward repeatedly until his groping wings gain a secure hold behind her head, to each side of the pro- or mesonotum, with the female's head pressed sharply and to the side by his flank. The gonostylas grip is then moved as far posteriorly as the male can manage) and the wing grip released. Once the male has the female again firmly gripped with his wings, and the gonostyles reach suffi- ciently far backwards, he tries to seize the ovipositor with his gono- styles; ordinarily several attempts are required, and after each failure 4Markchal (1939) misremembers Lestage's (1920) account when he states '(c'est la
9
qui saute sur le 8, celui-ci cherchant i fuir et a den dkbaras- ser!", and goes on to tell still more of female sexual aggressiveness.



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Fig. 1. Mating of Boreus notoperates.
A) mated pair preserved in female
perpendicular position; the medial tooth of $the gonostylus has disengaged (at death) from the lateral basal notch of the gonapophysis. B, full union of male and female; medial tooth of gonostylus seated into the lateral basal notch of the gonapophysis; C, semi diagrammatic representation of mated specimens cleared in clove oil; as in A, the gonapophysis is partially with- drawn from the endandrium, and the lateral basal notch of !the gonapophysis (at arrow) is clearly visible; dorsal proctigeral plate (closely, transversely lined) lies within epandrial notch; gonapophyses stippled ; aedeagus (widely, transversely lined) partially inser~ted in common oviduct - note flap at anterior margin of female gonopore and paired ejaculatory ducts entering base of aedeagus; the sclerotized lamina that forms floor of endandrium is cross-hatche,d (see text). D, male terminalia with everted aedeagus) apical nipple of which bears the gonopore; upper left-inner face of right gono- style to show median tooth and stylocavernula. All from camera lucida sketches; scale: for A and B equals I mm, for C and D equals 0.5 mm.



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92 Psyche [March
the gonostyles are returned to a grip on the posterior legs) near the coxae) and the male rests. When at last the ovipositor has been grasped) the gonapophyses are pried down and slightly apart, the female holding them) as though plastic, in whatever position they were released by the gonostyles. The gonapophysis of each side is then engaged between the inner tooth and the tip of the corresponding gonostyle which, on adduction, directs and thrusts the tip of the gona- pophysis into a pocket ventral to the epandrium (see below). Ratchet- like, the two gonapophyses together are worked down and in by the gonostyles. Finally each gonostyle becomes securely seated on the cor- responding gonapophysis) for its inner tooth (figs. ID; 2A, B) engages the lateral notch of the gonapophysis near its base (fig. IB, compare with IA and C, arrow).
The female is then released from the clasp of the male's wings. Thereupon she rocks backward go0 or more, with rostrum and an- tennae folded between the forelegs) femora drawn up to the sides) tibiae adducted, tarsi drooping - the "death-feigning)' posture that concludes the leap of a startled Boreus. Surprisingly) the female thereafter remains vertically in that posture) though her legs relax) and the male folds his wings to their usual rest position over the back, fig. IA). In side view it can be seen that the tip of the aedeagus has been fully inserted into the common oviduct (fig. IC). Despite the unbalanced appearance of a male and female united thus at a right angle) without any noticeable difficulty the male may run) climb, feed, and hop) landing without loss of balance. If startled, the male may leap several centimeters or more, landing in (or assuming) the death-feigning posture, motionless and resting on his flank; the female too death-feigns as before; after a few moments) the male returns to his feet.
In all, ten cases have been timed from the first assault of the male to intron~ission; these took from 6 minutes to 18, with a mean of 13 minutes (all at I 7O-20å¡C) The total duration of intromission has not been timed) but I have observed cases in which it was less than an hour) others of more than several hours. Both sexes mate repeatedly, with the same or different partners. 5Esben-Petersen (1921) was unable to see this median tooth in specimens before him of B. brumalis and B. nivoriundu~; Lestage (1940) took the supposed absence of a median gonostylar tooth as presenting a cardinal character for Euboreus, a genus he erected for ,all American species. For discussion of Euboreus, see Cooper (1972).



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19741 Cooper - Boreus 9 3
The events just described are different in a number of significant features from those in the matings of B. hyemalis, B. westwoodi and B. brumalis, which are alike. Once a female of those species has been seized by a male, it ordinarily becomes passive (but nlot always, see Synls 1934) Aubrook I 939, Sauer I 966, Crampton 1940). The rested male then grips the female across the midbody with his wings (as does B. notoperates)) and with them and his gonostyles works her body over his dorsum so that it is axially symmetrical and paral- lel to his own. The gonapophyses are then pried down and inserted into the subepandrial pocket, the wing-hold is released and the female rocks back until perpendicular to the male. Intromission very likely
occurs at this point, as it does in B. notofierates. The relative station of the two sexes just prior to intromission, or the ((pose)) (Lamb 1922)~ in all four species is truly a "female vertical poseJJ with (pre- sumably) an-inverse correlation of the genital conduits of the two sexesS6
Now Lamb (1922) used '(vertical" as a contrasting term to ('linear)' (or tail to tail) to denote arrangements of partners in which one partner is above the other. In the overwhelming majority of such cases, the body of the upper insect lies more or less ~arallel to that of its partner. Consequently I shall call the pose common to the four Boreus a "female perpendicular pose)y to distinguish it. The final copulatory attitude of B. notoperates does not depart from the pose; accordingly it is a "female perpendicular positiony' (fig, IA). In contrast, B. hyemalis, B. westwoodiJ B. brumalis, B. californicus ( = var. fuscus Carpenter?) (Cockle 1908, 1914)~ B. nivoriz~ndus Fitch (Carpenter I 936 ; Cooper, unpubl.) B. unicolor Hine ( Byers 1954) and B. vlasovi Martynova (Vlasov 1g50), namely in all other species for which the copulatory position has been recorded, the final attitude differs from the pose) being a female vertical po~ition.~ intromission) the apparent dorsal wall of the aedeagus of Boreus lies in contact with the ventral wall of the common oviduct, hence in ('inverse correlationJ') which is ,unusual (fig. 1C). In most insects correlation is '(direct)', or symmetricaly for contact is dorsal-dorsal and ventral-ventral; in many insects having a vertical position, direct correlation is brought about by rotation of the male genital ttract (see Lamb 1922). 'For original drawings) or photographs (reference in boldface), of copu- lating pairs in their final fem'ale vertical position, see: for B. hyemal'i~, fig. 3, pl. 8, Withycombe r1922), fig. 1, Steiner (1937), fig. 7) Striibing (1958) ; for B. westwoodi, fig. 5) p1. 3) Brauer (1855)) fig. 2) Sauer (1966) ; for B. brumalis, fig. 9) Cooper (1940)) fig. 1) Crampton (1940).



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94 Psyche [March
On the basis of its morphology, B. notoperates (along with the similar B. brevicaudus Byers) has been adjudged the least primitive of all known species of Boreus (Cooper 1972). Interestingly, its mating stands apart from that described for the other three studied species: at its onset (the enduring resistance by the female), at its midpoint (submission by the f male only after antenna1 "abuse") , and at its very end (a female perpendicular position derived without change from a similar pose). In that last attribute, it differs from all seven other species of Boreus for which the position has been re- corded and, notably, that position is alike in all seven. The long period of female coyness and the need for manipulation of the fe- male's antennae go hand in hand, but I cannot decide whether these are primitive aspects or not. But the female perpendicular position is almost certainly a specialization, the marked change from pose to position that occurs in other species of Boreus most likely being primi- tive. I suspect that the presumed loss of change is related to the unusually shortened ovipositor of B. notloperates and the relative depth to which the gonapophyses are inserted into the male; if that is so, B. brevicaudus may be expected to have a female perpendicular position, and possibly also the remote B. chadzhi-gireji Plikinsky as well.
Because most Boreus follow closely similar mating patterns, as do B. humah and B. nivoriundus, with poses and final positions that are alike, the question quite naturally arises as to whether cross- matings occur or are even attempted. My own trials on this score were with smallish B. nivoriundus males and B. brumalis females, two species quite frequently found within common areas in New Hampshire. They showed no mutual interest whatsoever. This was not to be attributed to lack of potential competence or sexual aggres- siveness on the part of the males for, when female B. nivoriundus were added, the males soon paired, or attempted to do so, with the females of their own species. Perhaps the scent or secretion claimed for female Boreus (Hardy 1848, Withycomb 1922, Mar&hal 1939) has a role as a species specific mating pheromone. The female vertical position is widespread among insects, yet not common. It has been recorded for Orthoptera (where it, or its equivalent, the "false male vertical position" of Richards, is the usual mode), Plecoptera, Mallophaga, Anoplura, Mecoptera, Siphonaptera,