Charles S. Henry.
Eggs and Rapagula of Ululodes and Ascaloptynx (Neuroptera: Ascalaphidae) : A Comparative Study.
Psyche 79:1-22, 1972.

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PSYCHE
vol. 79 March- June, I 972 No. 1-2
EGGS AND RAPAGULA OF ULULODES AND
ASCALOPTYNX (NEUROPTERA: ASCALAPHIDAE) : A COMPARATIVE STUDY*
BY CHARLES S. HENRY
Biological Laboratories
Harvard University, Cambridge, Mass.
02 I 38
I. INTRODUCTION
Ascalaphidae is a fairly large family of planipennian Neuroptcra, encompassing perhaps 300 species in 65 genera, yet relatively little is known of the biology of its various representatives. Although several systematic monographs concerned exclusively with the family have been published ( Lefebvre, I 842 ; Rambur, I 842 ; McLachlan, 1871 ; Van der Weele, 1908 ; Navis, 1913), attempts to discern the true phylogenetic relationships among the various genera and other taxa must necessarily await studies of life-history and behavior. In fact, definite larva-adult associations are lacking for a great majority of ascalaphid species. Larvae have been reliably identified only for the genera Ascalaphus Fabricius, Helicomitus McLachlan, Pseudo- ptynx Weele, Suhpalacsa Lefebvre, and Ululodes Currie, all be- longing to the "split-eyed" subfamily A~cala~hinae; of the "entire- eyed" subfamily Neuroptynginae, only Ascaloptynx Banks has been associated with a larval type (MacLeod, 1970: p. 155). I have succeeded in rearing an additional species of Ululodes from egg to adult: Ululodes mexicana ( McLachlan), common in northern Mexico and southern Arizona and New Mexico. I have also been able to compare the form and habits of the various life stages of this species with those of a sympatric neuroptyngine species, Ascalo- ptynx furciger (McLachlan). The identity of this last-named species is inferred, but based upon various types of evidence: (I) third- instar larvae, raised from field-collected eggs, were positively identi- fied by Dr. Ellis G. MacLeod (University of Illinois) as those of Ascaloptynx; (2) the only species of the genus Ascaloptynx- or, for that matter, of subfamily Neuro~tynginae - ever taken at the *Manuscript received by the editor August 1, 1972. Pu&e 79:)-22 11972). http //psychr enlclub.mB/P9/TO-OOl him)



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2 Psyche [March-Junt
collecting sites in question is furciger; (3) males and females of Ascaloptynx firciger were captured in fair abundance in the same areas and at the same time of year that eggs and young larvae were collected; (4) dissections of gravid A, furcigw females revealed eggs and egg-attendants (see text) that were in every respect identical to field-laid eggs that yielded Ascaloptynx larvae. The first student of ascalaphid lifehistory was the Reverend L. Guiiding, whose 1827 account of the various life stages of Ululodes marleayaw (Guilding)* from St. Vincent's Island in the West Indies remains one of the best such studies ever published. In de- scribing the eggs of this species, he noted the presence of curious rod-shaped structures encircling the twig beneath the egg-mass. He called these egg-attendants "repagula,"** meaning "barriers," be- cause he believed that they prevented ants and other predators from approaching and destroying the eggs and newly hatched larvae; con- versely, he felt that the repagula discouraged the larvae from leaving their twig "until they have acquired strength to resist . . . [their] enemies." Mtdendon (191) also noted repagula accompanying the eggs of Ululodes hyalina (Latreille) [believed by Machod ( 1964) to be Ululodes senex (Burrneister)] from Texas; he con- firmed Guilding's description of these structures and concluded from his dissections of gravid female ascalaphids (unfortunately unillus- (rated) that certain ovarioles ("tubercles") were specialized for the production of repagula. Thus it was shown that repagda were in fact abortive eggs. Seventy years later, New ( 1971 ), apparently overlooking the papers of Guilding and McClendon, re-introduced the concept of ovariolar dimorphism in his cursory study of the eggs and repagula of eight species of Ascalaphidae from central Brazil. New's paper is important, nonetheless, for two reasons: first, it proved that repagula-formation is not unique to the genus Uluhdes but is also found in the closely-allied genera Cohbopterus Rambur, Ascdorphnc Banks and Cordvlccerus Rambur. and in the neuro- ptvngine genera Byas Rambur and Episperches Gerstaecker ; secondly, it suggested that the repagula of neuroptyngine species are funda- mentally different in form from those of ascalaphine species- the former type more nearly resembling fertile eggs than the latter type. The functional significance of repawla has not been investigated. Most authors ( Imms, 1957, for example) have accepted GuiIding's "ant guard" view. New (1971) intimates that repagula and eggs *Guilding's name for this species was Ascalu$kw macleayanus. **singular = repagulum.




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19721 Henry - Ululodes and Ascaloptynx 3 alike of Ululodes were carried off by ants in Brazil, but admits that more controlled experimentation is needed to assess the effects of the repagula on egg or larval survival. Through my studies of the life-histories of Ululodes mexicana and Ascaloptynx furciger, I have been placed in a unique position to verify or disprove experi- mentally the ant-guard hypothesis, as it applies to these representa- tive species of two taxonomically distant genera. Especially important is the fact that Ululodes is an ascalaphine genus while Ascaloptynx is a neuroptyngine one, thus encouraging direct comparison of the functional significance of the morphologically disparate repagula char- acteristic of the members of these subfamilies. In the remainder of this paper, I intend (I) to describe the eggs and repagula of Ululodes mexicana and Ascaloptynx furciger, (2) to outline the procedures and results of several simple experiments undertaken to test the protective importance of the repagula of both species, and (3) to discuss the functional significance of the ascalaphine type of egg and repagula as compared to that of the neuroptyngine type. 11. ACKNOWLEDGEMENTS
Special thanks are extended to Professor Frank M. Carpenter, my advisor and friend for the past five years. All aspects of the work in this paper draw heavily from his awesome knowledge of insect behavior, morphology, evolution and taxonomy, especially of the order Neuro~tera. I am also in his debt for his help in guiding this study into publishable form.
My wife, Nancy FitzGerald, should also be cited as a primary source of inspiration for this project. Her shrewd suggestions and sharp observations in the field are apparent to me again and again as I review my notebooks and find her influence in their pages. In addition, warm thanks are extended to: Professor Ellis G. MacLeod ( University of Illinois), for his generous willingness to transmit his intimate knowledge of the habits of all sorts of neuropterous insects to a neophyte like myself, and for confirming the identity of Ascaloptynx larvae; Professor Edward 0. Wilson (Harvard Biological Laboratories), for enthusiastically supporting my research effort and for determining the genera and species of ants used in the ant-guard experiments; Mr. Vincent Roth of the South- western Research Station, for his assistance with my field work in Arizona ; Dr. Lauren Anderson (University of California at River- side), for his advice on securing newly-hatched ascalaphids; and Mr. Robert E. Silberglied (Harvard Biological Laboratories), for his photographic help and biological acumen.



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Figure 1. Typical sites for oviposition, Ululodes mexicana (1-a) and Ascaloptynx furciger ( 1-b) .
Year-round financial support for my studies was for three years provided by the National Science Foundation, in the form of a Pre-Doctoral Fellowship (September, 1968 to September, I 97 I ) . A final fourth year of research was completed with the aid of a Rich- mond Fellowship ( I 97 I-'72) offered through Harvard's Department of Biology. Unusual expenses associated with travel to the field and with publication of this paper were generously advanced by the Committee on Evolutionary Biology, Harvard University (NSF Grant GB 27911, Reed Rollins, Harvard University, Principal Investigator).
Eggs of both Ululodes mexicana and Ascaloptynx furciger were collected during August and September in the southeastern part of Arizona, within a 25-mile radius of the Southwestern Research Station of the American Museum of Natural History (SWRS).
All egg-masses, 25 of UZuZodes and 35 of Ascaloptynx, were taken on shrubs in the arroyos and canyons of the 'Chiricahua and Peloncillo Mountains, at elevations of 4700 to 5700 feet ( 1500-1800 meters). Several egg-masses were left in situ and visited twice daily; others



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19721 Henry - Ululodes and Ascaloptynx 5 were placed twigs and all in 2.5 cm X 9.0 cm glass screw-top vials and transported carefully to the research station laboratory. There, the egg-bearing twigs were taped in their "natural" positions, covered with large glass jars for observation and situated in a southwest window shielded by heavy curtains form the vicissitudes of indoor artificial light. Complete records from oviposition through hatching to descent of larvae were obtained for seven egg-masses of Ululades and eight of Ascaloptynx. Additional egg-clumps of both species of Ascalaphidae were exposed to several natural and exotic insect preda- tors (mostly ants) under various experimental conditions, to ascertain the effectiveness of the repagula. In each experiment, for each ascalaphid species, two normal egg-masses and one egg-mass stripped of its repagula were mounted (on their respective twigs) in the
vicinity of foraging ants, in such a manner that the bottom-most egg of each clump was positioned 16 cm above the ground. The behavioral details and success of each foray of an ant (or other insect) up an egg-bearing twig were carefully noted. Similar experiments were carried out using hatched egg-masses, prior to
descent of the larvae from their twigs.
Closer observation and dissection of eggs, repagula, and gravid female ascalaphids were undertaken beneath a Wild M5 stereoscopic dissecting 'scope outfitted with an integral camera lucida attachment; most of the illustrations included with this paper were rendered with the aid of this precision imaging device. Extremely small specimens and structures were treated with xylene and mounted in Damar on depression-slides and observed at higher magnification using a Bausch and Lomb stereoscopic compound microscope with one ocular fitted with a 10 X 10 micrometer grid to insure accurate drawings.
IV. DESCRIPTIONS OF EGGS AND REPAGULA
A. Ululodes mexicana ( McLachlan)
Adults of U. micana appear in large numbers in southeastern- Arizona at the beginning of August, and remain abundant until the time of first frost - mid or late October. Males apparently die off by early September, while females, which individually may live three months or more under laboratory conditions, begin laying eggs at the start of the dry season in September and continue ovipositing far into October. Females display great selectivity in their choice of sites for oviposition, but are quite unselective of the particular species of plant: eggs are laid probably at dawn on the thin periph- eral dead twigs of any two or four foot deciduous shrub growing



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19721 Henry - Ululodes and Ascaloptynx 7 on totally exposed, south-facing embankments of dry arroyos and canyons (figure I-a). The insects always seem to choose inclined rather than vertical twigs, and seek out the downhill sides of the bushes in preference to any other spots; this latter choice gives the hatched larvae an unobstructed fall of 50 to 85 cm (18-30 inches) to the crumbling rocky substrate below. U. mexicana eggs are laid on the undersides and towards the tips of their twigs, in two long interdigitating rows together totalling 30 to as many as 52 eggs (figure 2). Each freshly laid egg is light grey or cream-grey in color and oblong in shape, averaging 1.6 to 2.0 mm in length and 0.8 to I .O mm in diameter; all the eggs in a given egg-mass will be of roughly equivalent size, but different egg-masses will vary considerably in their egg dimensions. The eggs are laid on end, inclined slightly toward the tip of the twig. They are attached to the substrate by a shiny reddish-brown glue. Each egg possesses two identical, pale micropyles, about 0.1 mm in diameter, axially located one at each end; high power examination reveals the micropyle to be saucer-shaped, constructed of approximately twenty ribs or channels radiating from a central depression (figure 3-A). Except for the micropylar sculpturing and a very slight graininess to the balance of the egg surface, the Ululodes chorion displays no elaborate fine-stucture.
Figure 3. Micropyles of Ululodes mexicwa (A) and Ascaloptynx furciger (B) eggs.




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Three to four days after oviposition there appears a diffuse whitish line nearly girdling the egg a short distance from its distal pole (figure 4). This line circumscribes an arc of 270 degrees and marks the line of weakness along which the egg will split as the larva emerges; the extent of the weakened area and the positioning of each egg at the time of laying assures that the "cap" of each egg will remain attached to the main egg body by a "hinge" and will flip toward the midline of the egg-mass at the time of hatching. It can be seen (figure 4) that the developing embryo conforms to no strict rule of position within the egg except to have its head end toward the egg's distal pole. A few days prior to hatching, the whitish outline of the embryo disappears and the sides of the egg cave in slightly; the egg progressively darkens to a slate-grey color and hatches on the fifteenth or sixteenth day after oviposition. The repagula of UZuZodes mexicana do not resemble the eggs at all. They are rod- or club-shaped structures, reddish-brown and shiny in apperance, surrounding the twig bristle-like five to ten millimeters below the egg-mass (figure 2). Sometimes they are arranged in a series of neat rings but more usually are rather irregularly placed. Each repagulum is approximately two-thirds the length of a normal egg, measuring 1.2 to 1.4 mm in length and 0.25 to 0.30 mm at its widest point; it appears to lack any vestige of a micropyle, despite its ovariolar origin. It is characterized by a small, round, light-colored basal swelling and a larger, oblong, darker distal swelling, joined by a thin translucent stem (figure 5-B). The over-all reddish hue is apparently imparted by the shiny fluid coating each repagulum. This non-sticky fluid should not be confused with the hard brownish glue that secures both eggs and repagula to the stem: it neither hardens upon nor evaporates from the repagulum surface for at least three to four weeks after ovi- position. Long after the true eggs have hatched, these strange barriers gradually collapse, their surfaces choked with debris. Apparently the repagula are extruded from the female's body after she has deposited her eggs, since in laboratory situations repagula are often found glued randomly to the surfaces of the eggs. Thus it would seem that the Ululodes female oviposits progressively from the tip of the twig towards its base, with her head oriented down- ward; such a view agrees with what we know of the standard rest- posture of Ascalaphidae. Typically, four of the twelve ovarioles in each of the female's ovaries are modified for the production of repagula (figure 6). However, the insect is nevertheless capable



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Henry - Ululodes and Ascaloptynx
Figure 4. Detail of eggs of Ululodes mexicana, three to four days old. 'of depositing as many as or more repagula than eggs at any given time, since each modified ovariole can store many more "mature" repagula than a normal ovariole can eggs. Stored repagula show no trace of the reddish color characteristic of oviposited repagula, suggesting that the red fluid is secreted by some accessory gland at the time of deposition.
B. Ascaloptynx furciger ( McLachlan)
Adults of Ascaloptynx furciger are active earlier in the summer than U. mexicana, seemingly being most abundant in southeastern Arizona during the rainy season, from early June to early September. As in Ululodes, males become less common in the latter half of this time period. Eggs are in greatest evidence during August, with chalcidoid parasitism destroying 95 percent of the egg-masses de- posited after September I. Again like Ululodes, ovipositing Ascaloptynx females are extraordinarily habitat specific, yet display little preference for particular plant species: eggs are laid on the thin terminal dead twigs of any one to two foot perennial or grass clump growing in protected semi-shaded locales in the foothills of the mountains, where rainfall is relatively great and scrub oak (Quercus emoryi and Q. arizonicus)
and juniper ( Juniperus dep-
peana) abound. In contrast to Ululodes, vertically oriented twigs



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Figure 5. Comparison of the repagula (r) and eggs (e) of Ascaloptynx furciger (A) and Ululodes mexicana (B).
or grass-stems are always selected (figures I-b) ; the substrate be- neath the egg-clumps is nearly always densely strewn with dry oak litter.
Ascaloptynx furciger eggs are laid in dense clumps completely surrounding their twigs, near the tips of the stems, perhaps 22 to 55 cm (8 to 18 inches) from the ground. The structure of the egg- mass suggests that it might consist of several long, parallel, tightly- spiraling rows of eggs. These clumps typically include 35 to 45 ovoid eggs, each one glued by its mid-section to its twig with its longer dimension oriented nearly horizontally (figure 7). The freshly laid Ascaloptynx egg is bright yellow-ochre in color, aver- aging 2.1 to 2.4 mm in length and I .2 to I .3 mm in diameter; it is thus larger and proportionally less elongate than that of UZuZodes. It possesses two axially located micropyles, about 0.15 mm in diameter, identical to those of Ululodes in all respects except size (figure 3-B). The chorion of the egg displays no1 sculpturing. As in Ululodes, several days after oviposition a whitish girdling line appears at the "head" end of the egg, outlining the extent of the egg cap (figure 8). In Ascaloptynx, positioning of the eggs on the twig assures that every egg cap will flip downward on its hinge;



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19721 Henry - Ululodes and .Ascdo~~ynx I I in fact, the cephalic (cap) pole of each egg is slightly lower than its opposite pole and related to the cephalic poles of its neighbors in such a way that no larva interferes with another during hatching. It is of interest that in AscaZofitynx the whitish outline of the developing embryo always appears on the dorsal surface of the egg. As in UZulodes, this outline disappears as the egg gradually darkens to a muddy brownish-yellow color and acquires a semi-collapsed appearance several days before hatching; eclosion occurs a minimum of 14 days after oviposition.
The repagula of Ascdoptynx furciger appear to be miniaturized versions of fertile eggs: each is identical to a full-sized egg in color, proportion) micropylar structure, and orientatation (figure 5-A). Typically) a repagulum in this species measures 1.3 to 1.4 mm by 0.65 to 0.70 mm; it has no fluid of any kind on its surface. In all egg-masses examined, repagula occurred in a small group immediately below (and continuous with) the main egg clump, and in a larger group about 10 cm further down the twig; frequently, one or two additional, smaller masses of repagula would be present, spaced varying distances below the largest clump (figure 7, "R3"). Usually the masses of repagula surround the twig in the same manner as fertile eggs, but occasion ally, especially on large stems, the repagula are deposited in an obvious spiral pattern. Dissections of AscaZo$tynx females reveal an arrangement of specialized ovarioles similar to that in UZuZodes; however, pooer preservation prevented reliable con- clusions as to numbers of ovarioles present and modified. Field- collected egg-masses always exhibit slightly ,higher numbers of fertile eggs than of repagula.
Experimental exposure of the eggs and repagula of both ascalaphid species involved three situations :
( I ) natural predation by Dory-
myrmex ~yranzicu~~ Formica sp. and Pogonomyrmex sp. at the site of the Southwestern Research Station (5400 feet) ; (2) natural predation by Pheidole sp., Paratrechina sp., Crernat~~aster sp., D~orynzyrmex pyramicusJ and Formica sp. at a typical egg-collecting site near Crystal Cave in the Chiricahua Mountains (5700 feet) ; and (3) artificially-induced predation by Monom~orium sp. introh duced to the Harvard Biological Laboratories (Cambridge, Massa- chusetts) from Brazil.
A. UZuZodes mexicana
In all experimental situations, UZuZodes mexicana eggs protected



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Figure 6. Ventral dissection of gravid female Ululodes mexk-ana, show- ing normal ovarioles (Oe) and those specially modified for the production of repagula (Or).
by their repagula were unassaiIable by any species of ant, even large (2 5mm) Formica sp.
(see Table I ) ; on the other hand,
unprotected eggs were quickly discovered and carried off by all ant species tested. Ants ascending the twigs and touching the repagula with their antennae would immediately and violently withdraw, occasionally falling to the ground. An intense period of antenna- cleaning, lasting from 15 to 60 seconds, always followed such con- tact. Experiments under laboratory conditions using the exotic Brazilian ant A~onomorium sp. (2 mm long) indicated that con- tact with one repaguIum alone was sufficient to discourage an ant from ascending the twig. Artificial "repagula" made from short-.



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ANT SPECIES
TESTED
Oorymyrmex pyramicus
Formica sp.
Pogonomyrmex SF.
Pheidole sp-
Paratrechina sp.
Crematogaster sp.
Monomorium sp.
1 EXPERIMENT 1 11 EXPERIMENT 2 11 EXPERIMENT 3 SWRS grounds, Portal, Arizona
Natural Egg-habitat, 1/2 mi.
Laboratory: Cambridge, MA.
11 from SWRS
I
IEs
1 ufufOde' mexicana 11 A s c a ~ ~ $ ~ ~ r 11 U. mexicana 11 A. furciger 11 U. mexicana 11 A. f~rciger ULT egg-mass: egg- mass: egg- mass: egg-mass: egg-mass: egg-mass: Table 1. Tabulation of the susceptibility of UZuto dex mexicana and Ascaloptynx furciger eggmasses to attack by various species of ants. Succ. = successful attack, defined by ant ascending 16 cm o,f twig to bottom- most true egg. Fail = uns~uccessful attack: ant does not reach bottom-most egg. a and b = field-collected egg-masses, complete with protective repagula. contr. = control, field-collected egg-masses stripped of their repagula,




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threads coated with mineral oil were partially effective as guards against filonomoriu?n, but induced in the ant simple avoidance rather than active withdrawal; a single artificial ('repagulum" proved totally inadequate for protecting an egg-clump. Our field data is most complete and convincing for the ground- and low-bush-foraging species Dorymyrmex pyramicus (3 to 4 mm long). This is fortunate in the sense that pyramicus appears to be quite abundant in areas normally chosen by UZulodes for ovi- position ; however, Formica sp.) Crematogaster sp., and several other undetermined species of bush-foraging ants are also potentially important egg predators and should be more extensively tested. The ant-fences of UluZodes are equally effective against ant predators after hatching has occurred and the larvae are sitting in a group on their eggshells; in fact) repagula remain full and fluid- covered even three weeks after eclosion) while the larvae apparently rest on the twigs for no more than ten days. Insect predators or other disturbances introduced artificially elicit no defensive reactions from the larvae during their gregarious phase. Instead) upset Iarvae simply drop to the ground) suspended at first on silken threads two to three centimeters long.
B. AsclaZoptynx furciger
The repagula of AscaJoptynx furciger seemingly serve no dis-