z K
> ''
/
' \y > ' S Xgv os**X >
IfllliSNI NVINOSHillAJS^Sa I dVHe II L! BRAR I ES^SMITHSONIAN INSTITUTIC
-rp ~X CO „ ^ ~y CO —jr
v ... -'£*75^ z uj j=
o\ —
iR ARIES SMITHSONIAN INSTITUTION NOlifUliSNI NVINOSH1IWS S3IUVHa z r- — z r- , z
^V^OA/TX O O ■ . O ><T)c,Va?'
szvzt
iinuiSNi NvmosHims^sB i ava a n li brar i es^smithsonian institutk
2 to 2 .y. CO 2
X CO
o z
co Z co ^ Z — S
3 R ARIES SMITHSONIAN INSTITUTION NOlifUliSNI NVIN0SH1IWS S3IBVU8
CO “ ^ CO ^ . CO
uj fx Ixi ^<r.cvir>v
.4 </>
O ><!v D V^ Q
IlfUliSNI- NVINOSHilfllS^SS I HVH 8 II^LI B RAR I ES^SMITHSONIAN”lNSTITUTI(
r; «> z r~ 2 r~
r« ^ 5 /5a^\ O
00 33 >
07 ^
iyAs^y m '' \,x§y ^ m
3RAR I ES SMITHSONIAN~INSTITUTIONC/5NOIiniliSNl”NVINOSHillMS S3 I HV8 8
CO 2
CO
2
O
CO
X
X CO
O \*1
z
> X4JA|*^ *5 ' ■ \XV > ' *5 X^OSHVX >
Z CO ■ ^ Z CO 2
lifUliSNI^NVINOSHlIINS S3 I H V8 9 I T L I BRAR! ES SMITHSONIAN JNSTITUTIC
a#S% 3 V* ? 1 " A 5
jKf
sc
0 ••' o 2 ,s
2 -1 Z j z
3RARIES SMITHSONIAN INSTITUTION NOlifUliSNI NVINOSHillAIS S3I8V89
1 v V y5 | 5 ° ^
33 /f/gp 5 fo'&'rfbg\ 30
> teg jp 2 fe£ 31) >
5 ft
•— \°
o\~nc y co
2 ~e%?" i*i ^ ~s^mxy>
HinillSNrNVIN0SHlllAISCOS3 I 9 V*3 9 ll“L I B R AR I ES^SMITHSONIAN INSTITUTI
< zS5^5x s .< Ac E /z5iwTx < jgSv.
,/// I/a g s! 5 isr*>-
vx
nillSNI NVINQSHJLIWS S3ldVdail LIBRARIES SMITHSONIAN INSTITUTION — > tn — tn zz (
. _ z
(n
GO
o W* — ^222^ O
Z ~J Z
[ARIES SMITHSONIAN INSTITUTION NOIJ.nilJ.SNI NVIN0SH1IWS S3IHVaan
fn&\ P y- y x u' 8 tn
^3l) B * r & jt B (l^^l >
nillSNI- NVIN0SH1I INS S3 I a Vb a n~L I B R AR I ES^SMITHSONIAN^I TITUTION z , ^ w 5 £ z
< S ,. < c E /^asvTT'x S
/ A* z A' -I M&m&Zk z
VARIES SMITHSONIAN INSTITUTION NOlinillSNI NVINOSHilWS S3iavaan tn ^ <n — cn
o^oc .y “ '^r o XOndc^ " 5 X "
niliSNI^NVINOSHUINS^SH I BVH 8 ll^LI B RAR I ES^SMITHSONIAN^INSTITUTION
jvAsv^x m '' w ^ m
CO ± CO ™~ i: c/>
? AR I ES SMITHSONIAN INSTITUTION NOlinillSNI NVIN0SH1IWS S3iavaan
w z , w z
^ i v*#* <
Z K^v A JKsk Z
X tn
,y |
nmsNi NviNOSHiiws^sa i ava a n\i brar i es smithson ianjnstitution
RARIES SMITHSONIAN INSTITUTION NOlinillSNI NVIN0SH1IWS S3iavaaiT
m
inmsNi nvinoshiiws S3 1 ava a n“u b rar i es'/>smithsonian_institution
Z w z Mr ¥L Z
ISSN 0033-2615
50- Hbi (r°OH
^ PSYCHE
A JOURNAL OF ENTOMOLOGY
founded in 1874 by the Cambridge Entomological Club
Vol. 89 1982 No. 1-2
i JMH .1 i 'in. , J
/ IfiDADlP^
• **■* o ft A r\ 5
CONTENTS
Dedication: Joseph C. Bequaert. Frank M. Carpenter 1
Communication, Raiding Behavior, and Prey Storage in Cerapachys
(Hymenoptera: Formicidae). Bert Hdlldobler 3
Designation of a Type-species for Cvclogaster Macquart, 1834, and the Result- ing Synonymy (Diptera: Stratiomyidae). Norman E. Woodley 25
Orb Plus Cone-webs in Uloboridae (Araneae), with a Description of a New Genus and Four New Species. Y. D. Lubin, B.D. Opell, W. G. Eberhard, and H.W. Levi 29
Population Structure and Social Organization in the Primitive Ant, Amblyo- pone pallipes (Hymenoptera: Formicidae). James F.A. Traniello 65
The Biology of Nine Termite Species (Isoptera: Termitidae) from the Cerrado of Central Brazil. Helen R. Coles de Negret and Kent H. Redford 81
The Life History of the Japanese Carrion Beetle, Ptomascopus morio and the Origins of Parental Care in Nicrophorus (Coleoptera, Silphidae, Nicrophini).
Stew art B. Peck 107
Tergal and Sternal Glands in Male Ants (Hymenoptera: Formicidae). Bert Hdlldobler and Hiltrude Engel-Siegel 113
Termite-Termite Interactions: Workers as an Agonistic Caste. Barbara L. Thorne 133
Type Designations and Synonymies for North American Silphidae (Coleoptera). Stewart B. Peck and Scott E. Miller 151
Chemical Mimicry as an Integrating Mechanism for Three Termitophiles Asso- ciated with Reticulitermes virginicus (Banks). Ralph W. Howard, C.A. McDaniel, and Gary J. Blomquist 157
Parataruma, a New Genus of Neotropical Crabronini (Hymenoptera, Spheci- dae). Lynn S. Kimsey 169
Supplementary studies on ant larvae: Formicinae (Hymenoptera: Formicidae) George C. Wheeler and Jeanette Wheeler 175
Morphological comparisons between the obligate social parasite, Vespula aus- traica (Panzer) and its host, Vespula acadica (Sladen). Hal C. Reed and Roger D. Akre 183
CAMBRIDGE ENTOMOLOGICAL CLUB Officers for 1981-1982
President Barbara L. Thorne
Vice-President Frances Chew
Secretary Heather Hermann
Treasurer Frank M. Carpenter
Executive Committee John Shetterly
Mary Hathaway
EDITORIAL BOARD OF PSYCHE
F. M. CARPENTER (Editor), Fisher Professor of Natural History, Emeritus, Harvard University
W. L. Brown, Jr., Professor of Entomology, Cornell University and Associate in Entomology, Museum of Comparative Zoology P. J. DARLINGTON, Jr., Professor of Zoology, Emeritus, Harvard University
B. K. HOLLDOBLER, Professor of Biology, Harvard University H. W. LEVI, Alexander Agassiz Professor of Zoology, Harvard University R. J. McGlNLEY, Assistant Professor of Biology, Harvard University Alfred F. NEWTON, Jr., Curatorial Associate in Entomology, Harvard University
R. E. SlLBERGLIED, Smithsonian Tropical Research Institute, Panama E. O. WILSON, Baird Professor of Science, Harvard University
PSYCHE is published quarterly by the Cambridge Entomological Club, the issues appearing in March, June, September and December. Subscription price, per year, payable in advance: $11.00, domestic and foreign. Single copies, $3.50.
Checks and remittances should be addressed to Treasurer, Cambridge Entomological Club, 16 Divinity Avenue, Cambridge, Mass. 02138.
Orders for missing numbers, notices of change of address, etc., should be sent to the Editorial Office of Psyche, 16 Divinity Avenue, Cambridge, Mass. 02138. For previous volumes, see notice on inside back cover.
IMPORTANT NOTICE TO CONTRIBUTORS Manuscripts intended for publication should be addressed to Professor F. M. Carpenter, Biological Laboratories, Harvard University, Cambridge, Mass. 02138.
Authors are expected to bear part of the printing costs, at the rate of $27.50 per printed page. The actual cost of preparing cuts for all illustrations must be borne by contributors: the cost for full page plates from line drawings is ordinarily $10.00 each, and for full page half-tones, $12.00 each; smaller sizes in proportion.
Psyche, vol. 88, no. 3-4, for 1981, was mailed May 28, 1982
The Lexington Press, Inc., Lexington, Massachusetts
Joseph Charles Bequaert
This issue of Psyche is dedicated to the memory of Joseph C. Bequaert, who died in his 96th year in Amherst, Massachusetts, on January 12, 1982.
Dr. Bequaert was born in Belgium in 1886 and was educated there, receiving his Dr. Phil, degree in botany in 1908 from the State University in Ghent. The next seven years he spent in the Belgian Congo (now Zaire), at first as Entomologist on the Belgian Sleeping Sickness Commission and later as head of botanical explorations in the Congo for the Belgian Colonial Government. During those years his main interest shifted from botany to entomology, in which he subsequently did the greater part of his research and teaching. In 1917 he was appointed Research Associate in Congo Zoology at the American Museum of Natural History. Six years later, after becom- ing a naturalized citizen of the United States, he joined the faculties of the Harvard School of Public Health and the Harvard Medical School, as an assistant professor in medical entomology, and remained there until 1945. He then accepted the position of Curator of Recent Insects in the Museum of Comparative Zoology, succeed- ing Nathan Banks. In 1951 he was appointed Alexander Agassiz Professor of Zoology, a chair that he held until his retirement in 1956. Most of the remaining 26 years of his life were spent in Tuc- son, Arizona, where he was associated with the departments of entomology and zoology at the University of Arizona.
He was internationally known for his publications, totalling more than 250, on medical entomology, mollusks, botany, and systemat- ics of several families of insects.
Joe joined the Cambridge Entomological Club in 1923, as soon as he reached the Boston area, and he was very active in the society for the next 33 years. He was president in 1928, 1935-36, and 1942-43; vice-president in 1937, 1941, and 1946; secretary in 1925 and 1926; and treasurer in 1943. He also served on the editorial board of Psyche from 1947-1956. He gave many of the scheduled talks at our regular meetings and was chosen as the speaker for the 500th meet- ing of the Club on December 15, 1931. In recognition of his services and contributions to the activities of the society, he was elected an Honorary Member in 1961.
1
Joseph Charles Bequaert
Photograph taken in Belgian Congo, 1934
I first met Joe at the September meeting of the Club in 1923, at which he was nominated for membership. His exuberance and his extraordinary enthusiasm for nearly every aspect of natural history were the most obvious traits of his personality. In 1956 he wrote the following statement of his scientific interests: ecology of flowers; taxonomy and ecology of Bryophyta; geography and ecology of African plants; relations of Arthropoda to disease; taxonomy and ethology of Diptera and Hymenoptera, particularly Vespidae; mala- cology; medical entomology. He was certainly one of the most dis- tinguished and respected entomologists of his generation.
Frank M. Carpenter, editor
PSYCHE
Vol. 89
1982
No. 1 -2
COMMUNICATION, RAIDING BEHAVIOR AND PREY STORAGE IN CERA PA CHYS (HYMENOPTERA; FORMICIDAE)*
By Bert Holldobler
Department of Organismic and Evolutionary Biology,
MCZ - Laboratories
Harvard University, Cambridge, Mass. 02138 U.S.A.
Introduction
The former subfamily Cerapachyinae was recently recognized by Brown (1975) as a tribe (Cerapachyini) within the subfamily Poneri- nae. All of the cerapachyine ant species investigated feed entirely on ants (see review in Wilson 1958; Brown 1975). During foraging cerapachyine workers engage in mass expeditions during which they raid the nests of the prey species, capturing preferably larvae and pupae, but also occasionally adults and returning them to the raid- ers’ nest.
Although the detailed field observations on cerapachyine forag- ing raids reported by Wilson (1958) strongly suggest that the raiding expeditions follow chemical trails, this has not yet been experimen- tally investigated. In fact, almost nothing was hitherto known about the behavioral organization of the raiding expeditions and the under- lying communication mechanism. This paper presents the first ex- perimental analysis of the raiding behavior of a cerapachyine ant species.
Materials and Methods
Three colonies of Cerapachys (?) turneri (turneri group) (acces- sion #163a, b, c; voucher specimens in Australian National Insect
* Manuscript received by the editor January 22, 1982.
3
4
Psyche
[Vol. 89
Collection, ANIC, Canberra) were collected from nests in the soil in a sclerophyl scrub pasture near Eungella, North Queensland (Aus- tralia). One colony had a single ergatoid queen; the other colonies had two ergatoid queens apiece. Each colony was housed in separate glass tube nests (8cm X 0.6cm c />), with water trapped at the bottoms behind cotton plugs. Each nest tube was placed into arenas of varying sizes, depending on the experimental design. Histological studies were conducted according to the procedures described in Holldobler and Engel 1978. Additional methodological details will be given with the description of the individual experiment, as pre- sented below.
Results
Raiding behavior and paralysis of prey larvae
Species of the genus Cerapachvs seem to preferably prey on ant species of the myrmicine genus Pheidole (Wilson 1958; Brown 1975). When 1 provided Cerapachvs with colonies or fragments of colonies of a variety of species of the genera Iridomyrmex, Meranop- lus, Monomorium, Crematogaster, Pheidole, Stigmacros, Polvrha- chis, Camponotus (placed in a 65 X 120cm arena) they preyed freely only on Pheidole. They also accepted Monomorium larvae as prey, but only when these insects were directly inserted into the Cera- pachys nest. When the Cerapachvs workers encountered workers of the other species, or came close to their nest tubes, they usually showed avoidance behavior. The reaction was very different, how- ever, when individual scouts of Cerapachvs discovered the nest tube of Pheidole (accession #209, voucher specimens in ANIC). The Cera- pachys worker vigorously vibrated its short antennae and moved slowly into the nest tube, which contained approximately 200 Phei- dole workers and soldiers and about 150 larvae and pupae. It did not venture very far into the foreign nest but left after a short while and ran, in a somewhat meandering route, back to its own nest, located 70cm away from the Pheidole nest. During honyng it appeared frequently to touch the ground with its abdominal tip, as if it were laying a chemical trail or depositing scent spots. Seconds after it had entered the nest of its own colony, its n^stmates became very excited. Many grouped around the scout ant, which repeatedly raised its gaster upwards. Within one minute the scout left the nest
1982]
Holldobler — Cerapachys
5
again and moved in direction toward the Pheidole nest tube. It was closely followed by 17 nestmates. The leading scout ant continued to move with its abdominal tip close to the ground, but intermittently it paused or moved much slower while raising its gaster slightly upwards (Fig. 1). When the Cerapachys column arrived at the Phei- dole nest tube they invaded it and attacked the Pheidole workers and soldiers. Pheidole fought back but without any effect. The heav- ily sclerotized and specially protected Cerapachys (Fig. 2) were not at all affected by the mandibular grip of the Pheidole soldiers, even when they were attacked simultaneously by 3-5 Pheidole (Fig. 3). Although Pheidole outnumbered the Cerapachys invaders more than 10 times, they were rapidly disabled by the obviously very
Figure 1. Recruiting Cerapachys worker, (a) Worker walking with its abdomi- nal tip close to the ground, (b) Worker raising the gaster upwards; arrow indicates the position of the opening of the pygidial gland.
6
Psyche
[Vol. 89
Figure 2. Longitudinal section through the head and part of the thorax (a) and through part of the petiolus and gaster (b) of a Cerapachvs worker. Arrows indicate cuticle projections over intersegmental membranes (IM).
1982]
Holldobler — Cerapachys
7
Figure 3. Cerapachys raiding group invading a Pheidole nest.
effective stinging attack of the Cerapachys, during which the raiders grasped the Pheidole with their short mandibles, simultaneously bending their gasters forward, so that in each case the tip, where the sting extrudes, touched the opponent’s body. Each sequence usually lasted less than 1 second. Almost immediately after such an attack the Pheidole appeared to be immobilized. Only a few Pheidole workers escaped from the nest tube into the arena, some of them carrying brood. After approximately 15 minutes almost all Pheidole adults in the nest tube were disabled or killed but not a single Cerapachys worker was dead or visibly injured. Next the Cera- pachys began transporting the dead and immobilized Pheidole adults to their own nest. After the first workers of the raiding expe- dition had returned and unloaded the booty they returned to the Pheidole nest. Some of them raised the gaster repeatedly upwards, upon which several additional Cerapachys workers followed them to the Pheidole nest, where they participated in the retrieval of the prey. Only after most of the Pheidole adults had been retrieved did the Cerapachys begin to transport the Pheidole brood. Each larva and pupa was briefly stung before it was picked up and carried to the Cerapachys colony. Interestingly, after approximately half the brood had been retrieved, Cerapachys nest workers began discard- ing all the dead and disabled Pheidole adults, and the next day only
8
Psyche
[Vol. 89
Pheidole brood was stored in the Cerapachvs nest. Apparently the booty of this raiding expedition was so abundant that Cerapachvs preferred to keep only the more valuable and better preservable brood of the prey species, and they discarded the less valuable cadavers of the adult Pheidole. In other instances, however, where Cerapachvs had only, adults of prey species available, I observed Cerapachvs feeding on the gasters of dead Pheidole workers and soldiers.
This experiment was conducted on the 25th and 26th of October
1980. At this time there was no Cerapachvs brood in the colony. On November 10, 1980, I noticed the first large clutch of eggs in the Cerapachvs nest tube. On December 1 1, 1980, the colony had many large (presumably last instar) larvae, and another large cluster of eggs (Fig. 4). The colony still contained a very good supply of Pheidole larvae (Fig. 4), which did not grow or develop further but which were obviously alive. Under the microscope one could see that the prey larvae slightly moved their mouthparts. Workers, queens and larvae of Cerapachvs all fed on the Pheidole larvae. On December 26, 1980, there were still some prey larvae left. Many of the large Cerapachvs larvae had pupated; in addition the nest con- tained many medium sized larvae and another large clutch of eggs. On January 3, 1981, a Cerapachvs worker was observed leaving the nest tube and venturing out into the arena, for the first time since October 27, 1981. At this time I provided another fragment of a Pheidole colony with larval brood in the arena; and on January 5,
1981, Cerapachvs conducted another raid, very similar in details to that just described. The fact that the captured Pheidole larvae were kept alive inside the Cerapachvs nest chamber for a period of more than two months (but did not pupate or visibly increase in size) strongly suggested that they were sustained in a state of metabolic stasis. Recently Maschwitz et al (1979) provided experimental evi- dence that the ponerine species Harpegnathus saltator and Lepto- genys chinensis paralize prey objects by stinging and thereby are able to store prey a limited time. In one case the preserving paralysis effect was observed to last for two weeks, and in no instance did the stung prey object ever recover from the paralysis. Similar observa- tions have been made independently by Traniello (unpublished data) with the ponerine species Aniblvopone pal/ipes.
1982]
Holldobler — Cerapachys
9
Figure 4. Fractions of a Cerapachys colony, with paralyzed prey larvae. Q: erga- toid queens; E: eggs; C: Cerapachys larvae; P: Pheidole prey larvae.
10
Psyche
[Vol. 89
As just noted, Cerapachys workers apparently sting each Phei- dole larva and pupa during the raid, before they transport the vic- tims to their nest. This appears to be a very stereotyped behavior. For example when 1 shook a Cerapachys colony which contained Pheidole larvae out of the nest tube into the arena, so that they had to move back into the nest, Cerapachys workers picking up a Phei- dole larva almost invariably went through the typical stinging motion pattern. They did not do this, however, when they picked up their own larvae. Although stinging behavior did not frequently occur inside the nest, occasionally I observed a Cerapachys stinging several larvae while reshuffling a pile.
The Pheidole larvae are small and tender and the powerful Cera- pachys sting (Fig. 5) could easily pierce the larva and thereby kill it. Thus the injections of a paralyzing secretion through the sting has to be very subtle in order not to kill, but to preserve the larva. Brown (1975) describes the differentiated pygidium (Fig. 6) with its denticu- late margins, being present in all workers and queens of cera- pachyine ants. Brown states that “the function of the denticle- bordered pygidial plate is not known from direct observations, but it is assumed to have something to do with helping the insects to force their way through passages and cracks in soil or rotten wood, perhaps in connection with their entry into nests of termites or ant prey species”.
Our morphological and histological investigations have revealed that these denticuliform and spinuliform setae on the pygidium of Cerapachys turneri and Sphinctomyrmex steinhei/i are sensory setae and comprise probably mechanoreceptors (Fig. 7). It is most likely that during the stinging process these mechanoreceptors sig- nal the gaster tip’s touch of the prey larva and the extent of the stings’ protrusion is thereby regulated. Many of the nonsocial acu- leate Hymenoptera, which paralyze prey by stinging, are equipped with mechanoreceptors on the tip of the sting sheath (Oeser 1961, Rathmayer 1962, 1978). We did not detect similar structures on the tip of the sting sheaths of Cerapachys or Sphinctomyrmex. In addi- tional experiments I further confirmed the suggestion that the prey larvae, captured by Cerapachys, are preserved alive. Approximately 30 Pheidole larvae collected from a Pheidole colony were put with- out workers in a small test tube, which was kept moist by a wet cotton plug. A second similar test tube contained 30 Pheidole larvae which were taken from the Cerapachys nest. In two replications the
1982]
Holldobler — Cerapachys
11
Figure 5. (a) SEM picture of the abdominal tip of a Cerapachys worker. The
picture shows the partly extruded sting, surrounded by the sensory setae at the pygidium, and last exposed sternite. (b) Close-up of the two kinds of setae at the pygidium.
12
Psyche
[Vol. 89
Figure 6. SEM picture of frontal view of pygidium of a Cerapachvs worker (a), and a worker of Sphinctomvrmex steinheili (b). Note the arrangement of the two kinds of setae on the truncated pygidial plate of both species.
1982]
Holldobler — Cerapachys
13
Figure 7. Longitudinal section through pygidial plate (a) and last exposed ster- nite (b) of a Cerapachys worker. The structure and innervation of the setae suggest that they function as mechano receptors.
14
Psyche
[Vol. 89
larvae taken directly from the Pheidole colony were all dead after two weeks. On the other hand all of the larvae from the Cerapachys colony were obviously still alive after two weeks, many of them moving their mouthparts slightly. These findings clearly demon- strate that Cerapachys can store living prey larvae for a considerable period of time. This food storage system appears to enable Cera- pachys to stay inside their nest for longer intervals. They evidently do not conduct raids as long as a good food supply is present. The following experiments were designed to test this hypothesis.
One day after the Cerapachys colony B had conducted a raid on Pheidole all prey larvae were removed. As a control I manipulated colony A in the same way, but the prey larvae were immediately returned to colony A. A few days later I observed scouts of colony B in the arena, where I had provided a nest tube with a fraction of a Pheidole colony, and within a period of 4 (test 1) and 7 days (test 2) colony B had conducted another raid. In the control colony A I noticed a worker briefly leaving the nest tube only once and then without venturing far into the arena. Although a tube containing Pheidole workers and brood was also provided in the arena of colony A, this colony did not conduct another raid until its supply of prey had declined considerably.
Emigration behavior
Although it is still an open question whether the Cerapachyini are nomadic, Wilson (1958, 1971) and Brown (1975) suggested that nomadism in the ant-preying cerapachyine species could well be adaptive to avoid depleting the food supply in a given neighbor- hood, just as it is in the army ants. This assumption of a nomadic life style is further supported by Brown’s observations that the nests of many cerapachyine species appear to be impermanent, and that the “brood show a strong tendency to be synchronized, like those of army ants and nomadic Ponerinae”. Brown (1975) also pointed out that the larvae of the Cerapachyini have a slender and cylindrical shape (G. C. Wheeler and J. Wheeler 1964), which makes them easy to transport longitudinally under the bodies of workers in the manner of other predatory and nomadic ants, such as Eciton, Aenic- tus, Dorylus, Leptogenys and Onychomyrmex. Although I was unable to demonstrate periodic nomadic behavior of Cerapachys in
1982]
Holldobler — Cerapachys
15
the laboratory, I could easily initiate nest emigrations by removing the waterplug and thereby causing the nest tube to quickly dry out. Individual workers soon ventured into the arena and eventually discovered a new moist nest tube located approximately 20-30 cm away from the old nest. After exploring the new nest site the scout moved back to the colony. When entering the nest tube it exhibited the same behavior as when recruiting to a raid, including a repetitive lifting of the gaster. When the scout left the nest again to return to the newly discovered nest site, it was usually followed by several ants. Most of these first recruits also showed the gaster raising behavior on their return to the colony, and soon the whole colony began to leave the old nest tube and move to the new one. The larvae and pupae were carried in the manner Brown (1975) pre- dicted, slung longitudinally under the bodies of the workers (Fig. 8). Adult transport was never observed; the ergatoid queens and even relatively freshly eclosed workers moved on their own to the nest site. The colonies did not contain males. After the workers had moved most of their own brood, they transported the prey larvae ( Pheidole ).
Figure 8. Cerapachys worker carrying a larva during nest emigration.
16
Psyche
[Vol. 89
From the ants’ orientation behavior it appeared that they were following chemical trails during the nest emigration. In fact, the recruitment behavior during nest emigrations and raiding appeared to be identical. The following experiments were designed to analyze further the communication mechanisms involved in both events.
Communication during emigration and raiding
Two distinct behavioral patterns were observed in Cerapachys ants during recruitment. (1) They seem to lay a chemical trail when returning from the target area (prey colony or new nest site) by frequently touching the abdominal tip to the ground; and (2) when close to or just entering the nest, they repeatedly raised their gaster upwards into a “calling position” and continued to do so when they moved back to the target area, usually being closely followed by a group of recruited nestmates. Since it was easier to initiate emigra- tions rather than raids, most of the experiments were conducted during colony emigration. Several new exocrine glandular struc- tures have recently been discovered in ponerine ants (Holldobler and Haskins 1977; Holldobler and Engel 1978; Holldobler et al. 1982; Maschwitz and Schonegge 1977; Jessen et al. 1979). The Cerapachyini were not included in these studies. We therefore con- ducted first a histological survey for possible exocrine glands that might be involved in the communication behavior of Cerapachys. Besides the known glands associated with the sting, we found a pygidial gland, which consists of a paired group of a few glandular cells under the 6th abdominal tergite. Each cell sends a duct through the intersegmental membrane between the 6th and 7th tergite (Fig. 9). The intersegmental membrane is laterally slightly invaginated, so that at each side it forms a small glandular reservoir. No particular cuticular structure on the pygidium is associated with the pygidial gland.
In a first set of pilot experiments I dissected out of freshly killed Cerapachys workers poison glands, Dufour’s glands, hindguts, pygidial glands (6th and 7th tergites) and the last 3 sternites. For each test one organ of a kind was crushed on the tip of hardwood applicator sticks. These were then immediately inserted into the nest tube until the tip of the applicator was 2-3cm away from the colony,
1982]
Holldobler — Cerapachys
17
Figure 9. (a) Longitudinal section through the gaster of a Cerapachys worker
showing the location of the pygidial gland (PG). (b) Longitudinal section through
the pygidial gland; GC: glandular cells; CH: glandular channels through inter- iegmental membrane.
18
Psyche
[Vol. 89
which usually had gathered near the cotton plug. In the following 30 seconds I observed the reaction of the ants, and between each test I waited at least 10 minutes before another sample was inserted into the nest tube. These pilot tests (3 repetitions with each organ) clearly indicated that only crushed poison glands and pygidial glands eli- cited increased locomotory activity and attraction in Cerapachvs workers. The ants did not exhibit any particular behavioral reaction when sternites, hindgut or crushed Dufour’s glands were intro- duced.* For the next series of experiments I first initiated colony emigrations either by following the procedure described above, or by shaking the colony out of the nest tube onto the arena floor. Before each experiment the arena was provided with a new paper floor. A new nest tube was offered 15-20cm away from the old nest tube or the displaced colony.
Once the colony emigration to the new nest tube had commenced, I covered the floor area between the colony and the new nest site with a cardboard, onto which I had drawn two artificial trails, one with a crushed glandular organ to be tested, and a second one with a drop of water (control). The trails were made to originate either from the entrance of the nest tube or from the periphery of the clustered colony. Each trail (test and control) diverged through an angle of 45° to either side from a possible natural trail (which was of course covered by a piece of cardboard). In addition the whole paper floor was rotated for 90°, in order to control for possible visual orientation (Fig. 10). During the following 2 minutes I counted the ants following the trails (10cm long) to the end. Only trails drawn with crushed poison glands elicited a precise trail fol- lowing behavior in Cerapachvs workers. There was some initial following response to trails drawn with crushed pygidial glands, but the ants followed only through the first 1-3 cm, then usually turned or meandered off the trail. Only once was it possible to conduct a similar test during raiding behavior of Cerapachvs. In this instance the ants followed only an artificial trail drawn with a crushed poison gland.
Although pygidial gland secretions did not release trail following behavior in Cerapachvs, it clearly elicited increased locomotory
*Cerapachvs has also a very well developed sting sheath gland. It was not possible to test whether or not secretions of the gland play a role in communication.
1982]
Holldobler — Cerapachys
19
Figure 10. Schematical illustration of the experimental arrangement during trail tests. The colony was emigrating from nest NI to nest Nil along a natural trail a. During the trail tests, the whole arrangement was turned 90° (arrow). The natural trail a was covered by a cardboard, on which the test trail (T) and a control trail (C) were offered, each deviating from a in an angle of 45°.
activity and attraction in the ants. I hypothesized therefore that the recruiting ant might discharge pygidial gland secretions when it exhibited the gaster raising behavior. The pygidial gland pheromone might function as an additional recruitment signal by which the recruiting ant keeps the raiding party stimulated when leading it to the prey colony. In order to test this hypothesis, I tried on four different occasions to close the opening of the pygidial gland by applying collophonium wax between the 6th and 7th tergites. Unfor- tunately these experiments failed; apparently the ants were too dis- turbed by the procedure. During two raiding expeditions of
20
Psyche
[Vol. 89
Cerapachys we succeeded, however, in diverting individual ants from the raiding column over a distance of at least several centi- meters by presenting two applicators in front of them, one contami- nated with pygidial gland secretions and the other with water. Both applicators were slowly moved away from the columns in opposing directions. Of a total of 10 ants tested, 4 responded by following for a few centimeters behind the applicator with the pygidial gland secretions; no ant followed the control applicator. Although these results can be considered only preliminary, they do suggest that pygidial gland secretions might be involved in the recruitment pro- cess of Cerapachys. This suggestion was further supported by the results of a series of experiments in which I offered artificial trails drawn with crushed poison glands. I compared the trail following response of Cerapachys (within the first two minutes) successively either to trails drawn with poison gland secretions only or to poison gland trails offered simultaneously with pygidial gland secretions. For each kind a total of 6 experiments was carried out. Between each test at least one day had elapsed. The following response appeared to be stronger to poison gland trails when offered together with pygidial gland secretions (5.5 ± 2.9) than to those offered with- out pygidial gland secretions (3.0 ± 1.4) (0.1 > p > 0.05; Students t-test). Because of lack of material this series could not be extended, and thus the results remain only suggestive.
The two final experiments demonstrated that a trail (10cm long) drawn with one crushed poison gland, was still effective as an orientation cue several hours after it had been drawn. Using the same experimental arrangement described above (Fig. 10), I was able to show that emigrating Cerapachys would follow poison gland trails, 2 and 6 hours old, when they were offered after the natural trail had been covered. On the other hand, crushed poison glands introduced into the nest tube after 2 and 6 hours, or poison gland trails offered 2 and 6 hours after they had been drawn, did not elicit excitement or spontaneous trail following behavior. From these results it appears that the poison gland material might contain a short lasting stimulating component as well as a longer lasting orienting component.
1982]
Holldobler — Cerapachys
21
Discussion
Raiding expeditions in Cerapachys turneri are organized by indi- vidual scout ants, that return to the colony after having discovered a nest of the prey species. The scout lays a chemical trail with secre- tions from the poison gland, which serve as recruitment and orienta- tion signals for the nestmates. Circumstantial evidence suggests that in addition the scout releases a stimulating chemical recruitment signal from the pygidial gland. This occurs probably when the scouts move with their gaster held slightly upwards in a calling position.
Wilson (1958) reports the field notes made by H. Potter on the cerapachyine species Phvracaces potteri, which contain the only available description of the early stages of a complete raid observed in the field. Before the raid started Potter noted a few workers moving rapidly about, “each with its abdomen raised upwards”. These observations match closely my findings in the laboratory and lend further support to the hypothesis that in addition to the trails laid with poison gland secretions, another stimulating signal is dis- charged, presumably from the pygidial gland of the recruiting ants.
Wilson (1958) observed groups of Phvracaces moving along a raiding trail laid down by a raiding party on the previous day. In this case no individual leadership was involved and the foragers seemed to emerge from the nest randomly without a special recruit- ment stimulation by scout ants. Obviously these ants were following an established foraging trail, leading to a previously raided Phcidole nest which appeared to be vacated this time. Small exploratory parties conducted brief excursions to the side, but in most cases they turned back to the main trail. No nest suitable for raiding was found during these explorations.
These observations strongly suggest that chemical trails laid dur- ing raiding expeditions might still function as orientation cues one day later and that foraging parties can follow these established trails without the leadership of a recruiting scout ant. Indeed, my labora- tory experiments with Cerapachys have demonstrated that artificial trails drawn with poison gland material are effective as orientation cues at least for several hours.
22
Psyche
[Vol. 89
Although the raiding cerapachyine ants are usually enormously outnumbered by the worker force of the prey species, not one Cera- pachys worker was lost during all the raiding experiments in the laboratory. As can be seen from Fig. 2, Cerapachys and Sphinc- tomyrmex are excellently protected by a heavily sclerotized cuticle. The intersegmental joints, that is, the joints between head and thorax, and between thorax, petiole and gaster, are covered by cuticular projections so that no intersegmental membrane is ex- posed, even if the ant is twisted and bent to an extreme degree.
In addition, Cerapachys and probably all the other cerapachyine ants have a most powerful sting that immobilizes the opponents within seconds. Not only the adults of the raided colony, but also the captured larvae and pupae are stung by the raiders before they are retrieved to the Cerapachys nest. Observations and experiments demonstrated that the prey larvae are kept in a stage of metabolic stasis and can thereby be stored for a period of more than two months. This food storage system enables Cerapachys to adjust the raiding activities to food requirement and supply. From the labor- atory experiments we can conclude that Cerapachys does not con- duct daily or periodic raiding expeditions. The frequency of raiding expeditions depends on the food supply stored inside the Cera- pachys nest.
I was unable to demonstrate periodic nomadic behavior in Cera- pachys in the laboratory. I assume that nest emigrations might occur relatively frequently in this species, but that they do not fol- low a periodic pattern. Instead, environmental factors such as food supply or physical conditions of the nest site are likely to play the important role in inducing a Cerapachys colony to emigrate.
Acknowledgements
Many thanks to H. Engel-Siegel for technical assistance, to E. Seling for the SEM work, and to W. L. Brown and R. W. Taylor for identifying the ants. I am most grateful to R. W. Taylor and the Division of Entomology, CSIRO, Canberra (Australia) for their generous hospitality. This work was supported by a grant from the National Science Foundation BNS 80-021613, the National Geo- graphic Society and a fellowship from the John Simon Guggenheim Foundation.
1982]
Holldobler — Cerapachys
23
References
Brown, W. L., Jr.
1975. Contributions toward a reclassification of the Formicidae. V. Ponerinae, Tribes Platythyreini, Cerapachyini, Cylindromyrmecini, Acanthostichi- ni, and Aenictogitini. Search‘5, 1-115.
Holldobler, B. and C. P. Haskins
1977. Sexual calling behavior in primitive ants. Science 195, 793-794. Holldobler, B. and H. Engel
1978. Tergal and sternal glands in ants. Psyche (Cambridge) 85, 285-330. Holldobler, B., H. Engel and R. W. Taylor
1982. A new sternal gland in ants and its function in chemical communication. Naturwissenschaften in press.
Jessen, K., U. Maschwitz and M. Hahn
1979. Neue Abdominaldriisen bei Ameisen. 1. Ponerini (Formicidae: Poneri- nae). Zoomorphologie 94, 49-66.
Maschwitz, U. and P. Schonegge
1977. Recruitment gland of Leptogenvs chinensis: a new type of pheromone gland in ants. Naturwissenschaften 64, 589.
Maschwitz, U., M. Hahn and P. Schonegge
1979. Paralysis of prey in ponerine ants. Naturwissenschaften 66, 213.
Oeser, R.
1961. Vergleichend-morphologische Untersuchungen liber den Ovipositor der Hymenopteren. Mitt. Zool. Mus. Berlin 37, 1-1 19.
Rathmayer, W.
1962. Das Paralysierungsproblem beim Bienenwolf, Philanthus triangulum F. (Hym. Sphec.) Z. Vergl. Physiol. 45, 413-462.
Rathmayer, W.
1978. Venoms of Sphecidae, Pompilidae, Mutilidae, and Bethylidae. Hand- book of Experimental Pharmacology vol. 48, Arthropod Venoms (S. Bettini, ed.) pp. 661-690. Springer-Verlag, Heidelberg-New York, 1978.
Wheeler, G. C.
1950. Ant larvae of the subfamily Cerapachyinae. Psyche 57, 102-1 13. Wheeler, G. C. and J. Wheeler
1964. The ant larvae of the subfamily Cerapachinae. Suppl. Proc. Entomol. Soc. Washington 66, 65-71.
Wilson, E. O.
1958. Observations on the behavior of the cerapachyine ants. Insectes Sociaux 5, 129 140.
Wilson, E. O.
1971. The Insect Societies. Belknap Press of Harvard University Press, Cam- bridge (Mass.).
DESIGNATION OF A TYPE-SPECIES FOR CYCLOGASTER MACQUART, 1834, AND THE RESULTING SYNONYMY (DIPTERA: STRATIOMYIDAE)*
By Norman E. Woodley Museum of Comparative Zoology Harvard University Cambridge, Massachusetts 02138
The generic name Cyclogaster Macquart (1834) has been used in combination with specific names for taxa of Stratiomyidae from diverse regions of the world. It has remained more or less in synony- my with Lasiopa Brulle (1832) since the time of Brauer (1882), although Pleske (1901: 336) described Cyclogaster caucasica (Palae- arctic) and Hutton (1901: 10) described C. peregrinus from New Zealand after Brauer’s work appeared. Kertesz (1908) also consid- ered the two names synonymous, and placed 15 species in Lasiopa. These species are placed in at least five genera at the present time.
The purpose of this paper is to designate a type-species for Cyclo- gaster, which to my knowledge has never been done, in order to stabilize the generic synonymy as it is presently used by workers in the Stratiomyidae. A brief review of the history of the name Cyclo- gaster and generic names associated with it is necessary to under- stand the situation fully.
Macquart (1834: 256) first proposed the name Cyclogaster in the Diptera, and included in that taxon two species, Nemotelus villosus Fabricius (1794: 270; Palaearctic) and Stratiomys at rata Fabricius (1805: 83; Neotropical). No single type-species was designated.
The generic name Inermyia Bigot (1856: 82, 63) was proposed for the South African species Stratiomys edentula Wiedemann (1824: 29). Gerstaecker (1857: 322) and Loew (1860: 7) both considered Stratiomys edentula a member of Cyclogaster Macquart and Ker- tesz (1908: 30) listed Inermyia as a synonym with a query. Lindner (1972: 32) considered the species to be congeneric with the true, Palaearctic Lasiopa, and it is listed as such by James (1980: 260).
Kirkaldy (1910: 8) noted that the name Cyclogaster was preoccu- pied in zoology by Cyclogaster Gronovius, in the fishes (this name will be discussed in more detail below). He proposed a replacement name for the name in the Diptera, Neotropicalias. No reference was made to any specific names, although one might infer he was think-
25
26
Psyche
[Vol. 89
ing of the Neotropical species that Macquart had originally included in Cyclogaster.
Enderlein (1914: 579, 615), without any reference to Kirkaldy (1910), but evidently realizing that the two species originally in- cluded in Cyclogaster were not congeneric, proposed the name Labocerina for Stratiomys at rat a Fabricius. In his paper, the new name was spelled Labocerina twice (pp. 579, 615), and “ Labacerino ” once (p. 615), and has subsequently been spelled “ Labocerino ” by James (1940: 124). These latter two spellings were regarded as errors by James (1973: 26.29). In the same paper, Enderlein considered Cyclogaster a synonym of Lasiopa.
The name Cyclogaster Gronovius (1756: 9; 1760: 265; 1763: 55) was in dispute, as were all of his generic names, because many authors felt his work was not truly binomial. His Cyclogaster was first published in 1756, but this is pre-Linnean. The 1760 work is clearly not binomial, although this is the date of the name usually found in zoological nomenclators, being the first post-Linnean publi- cation of it. In 1954, the International Commission on Zoological Nomenclature formally ruled that Gronovius’ 1763 work, as well as an index of it subsequently published by Meuschen, be placed on the Official Index of Rejected and Invalid Works in Zoological Nomenclature. Thus Macquart’s Cyclogaster became the earliest valid use of the name in zoology.
Lindner (1958: 432), while discussing “Cyclogaster” peregrinus Hutton from New Zealand, recounted most of the above briefly, and noted that no type-species had been designated for Cyclogaster Macquart, but was apparently not aware of the I. C. Z. N. ruling. He also mentioned that Nemotelus villosus Fabricius was the type- species of Lasiopa (as had Enderlein, 1914: 613, and several other authors), which is erroneous, as the only species name associated with Lasiopa in Brulle’s original description was Lasiopa peleteria, which was described concurrently and is still regarded as a valid species.
As I interpret the situation, a type-species designation is necessary for Cyclogaster Macquart in order to stabilize generic synonymy, and as far as I am aware, this has never been done. In order to preserve the presently accepted generic synonymies, I hereby desig- nate Nemotelus villosus Fabricius, originally included in Cyclogas- ter by Macquart, as type-species for that genus. The following
1982]
Woodley — Cyelogaster
27
synonymy for Lasiopa, the senior generic name, results:
Lasiopa Brulle, 1832: 307. Type-species: L. peleteria Brulle, 1832: 308 (by monotypy). Cyelogaster Macquart, 1834: 256. Type-species: Nemotelus villosus Fabricius, 1794: 270 (by present designation).
Inermvia Bigot, 1856: 82. Type-species: Stratiomys edentu/a Wiedemann, 1824: 29 (by original designation, op. cit. :63).
Neotropiealias Kirkaldy, 1910: 8; replacement name for Cyelogaster Macquart, 1834, nee Gronovius, 1763. Type-species: Nemotelus villosus Fabricius, 1794: 270 (by autotypy).
The above type-species designation thus stabilizes the long-used synonymy of Cyelogaster with Lasiopa, while retaining the name Laboeerina Enderlein for the Neotropical Stratiomys atrata Fabri- cius. The name Neotropicalias Kirkaldy became an unnecessary, and therefore invalid, replacement name when Cyelogaster Grono- vius was rejected by the I. C. Z. N. ruling.
Acknowledgments
I wish to thank Curtis W. Sabrosky and Margaret K. Thayer for critically reading the manuscript.
Literature Cited
Bigot, J. M. F. 1856. Essai d’une classification generale et synoptique de l’ordre des Insectes Dipteres. (4e Memoire.) Ann. Soc. Ent. Fr. (3)4: 51-91.
Brauer, F. 1882. Zweifltigler des Kaiserlichen Museums zu Wien. II. Denk- schr. Akad. Wiss. Wien 44(1): 59-1 10.
Brulle, G. A. 1832. IVe Classe. Insectes. Pp. 64-395, in Bory de Saint- Vincent (ed. ), Expedition scientifique de Moree. Section des sciences physiques 3(1) (Zool. 2), Paris. 400 pp.
Enderlein, G. 1914. Dipterologische Studien. IX. Zur Kenntnis der Stratio- myiiden mit 3astiger Media und ihre Griippierung. A. Formen, bei denen der I. Cubitalast mit der Discoidalzelle durch Querader verbunden ist oder sie nur in einem Punkte beriihrt (Subfamilien: Geosarginae, Analcocerinae, Stratiomyii- nae). Zool. Anz. 43: 577-615.
Fabricius, J. C. 1794. Entomologia systematica emendata et aucta. Secundum classes, ordines, genera, species adjectis synonimis, locis, observationibus, de- scriptionibus. Vol. 4. Hafniae. 472 pp.
1805. Systema antliatorum secundum ordines, genera, species adiectis
synonymis, locus, observationibus, descriptionibus. Brunsvigae. 372+ 30 pp.
Gerstaecker, A. 1857. Beitrag zur Kenntniss exotischer Stratiomyiden. Linn. Ent. 11: 261-350.
28
Psyche
[Vol. 89
Gronovius, L. T. 1756. Musei Ichthyologici tomus secundus sistens Piscium indigenorum & nonnullorum exoticorum, quorum maxima pars in Museo Lau- rentii Theodori Gronovii, J. U. D. adservatur, nec non quorumdam in aliis Museis observatorum descriptiones. Accedunt nonnullorum exoticorum Pis- cium icones aeri incisae, et Amphibiorum Animalium Historia Zoologica. Lug- duni Batavorum. [i-viii] + 1-88 pp.
1760. Animalium in Belgio Habitantium centuria prima. Acta Helvet- ica 4: 243-270.
1763. Zoophylacii Gronoviani Fasciculus primus exhibens Animalia
Quadrupeda, Amphibia atque Pisces, quae in Museo suo adservat, rite exami- navit, systematice, disposuit, descripsit, atque iconibus illustravit. Lugduni Batavorum. [i-iv] + 1 136 pp.
Hutton, F. W. 1901. Synopsis of the Diptera brachycera of New Zealand. Trans. Proc. New Zealand Inst. 33: 1 95.
International Commission on Zoological Nomenclature. 1954. Opinion 261. Rejection for nomenclatural purposes of the Index to the Zoophylacium Gronovianum of Gronovius prepared by Meuschen (F. C.) and published in 1781. Opin. Decl. Int. Comm. Zool. Nom. 5: 281-296.
James, M. T. 1940. Studies in Neotropical Stratiomyidae (Diptera). IV. The genera related to Cvphomyia Wiedemann. Revista Ent. 11: 119 149.
1973. Family Stratiomyidae, No. 26, in A catalog of the Diptera of the
Americas south of the United States. Sao Paulo. 95 pp.
1980. 20. Family Stratiomyidae, pp. 253-274, in Crosskey, R. W.,
ed. Catalogue of the Diptera of the Afrotropical Region. London. 1437 pp.
Kertesz, K. 1908. Catalogus Dipterorum. Volumen 111. Stratiomyiidae, Erin- nidae, Coenomyiidae, Tabanidae, Pantophthalmidae, Rhagionidae. Buda- pestini. 366 pp.
Kirkaldy, G. W. 1910. On some preoccupied generic names in insects. Canad. Ent. 42: 8.
Lindner, E. 1958. Uber einige neuseelandische Stratiomyiiden Osten-Sackens im Deutschen Entomologischen Institut in Berlin. Beitr. Ent. 8: 431-437.
1972. Uber einige Stratiomyidae des Transvaal Museums (Diptera: Bra- chycera). Ann. Transvaal Mus. 28: 27 34.
Loew, H. 1860. Die Dipteren-Fauna Siidafrika’s. Erste Abtheilung. Abh. Naturw. Ver. Sachsen u. Thiiringen in Halle 2: 57-402.
Macquart, J. 1834. Histoire naturelle des Insectes. Dipteres. Vol. 1. Paris. 578 pp.
Pleske, T. 1901. Studien fiber palaearktische Stratiomyiden. I. Die Gattung Cyclogaster Macqu. Sitzungsber. Naturf. Ges. Univ. Jurjeff (Dorpat) 12: 335-340.
Wiedemann, C. R. W. 1824. Munus rectoris in Academia Christiana Albertina aditurus Analecta entomologica ex Museo Regio Havniensi maxime congesta profert iconibusque illustrat. Kiliae. 60 pp.
ORB PLUS CONE-WEBS IN ULOBORIDAE (ARANEAE), WITH A DESCRIPTION OF A NEW GENUS AND FOUR NEW SPECIES
By Y. D. Lubin,1, B. D. Opell,2, W. G. Eberhard,3 and H. W. Levi4
Introduction
Spiders of the genus Uloborus (Uloboridae) characteristically spin horizontal orb-webs with a sticky spiral of cribellar silk. We describe here the webs of U. conus, U. albolineatus, U. bispiralis, U. #2072, U. trilineatus, and Conifaber parvus which are modifications of this basic uloborid orb-web form and include cones composed of regular arrays of threads beneath the orbs’ lower faces. The web building and prey capture behaviors of U. conus (observations of YDL) are also described, and descriptions of Conifaber parvus new genus, new species and the new species U. conus, U. albolineatus, and U. bispiralis are provided (by BDO).
Study Sites and Methods
Uloborus conus was found at three localities in Papua New Guinea: 1) in lowland wet forest, Gogol Forest Reserve near Madang, Madang Province, 2) in a Pandanus swamp (freshwater) and a mangrove swamp (brackish) at Buso, Morobe Province, and 3) in the understory of klinki pine (Araucaria hunsteinii ) plantations at 1200 m elevation in McAdam Memorial Park near Wau, Morobe Province. Webs were built about 0.5 to 2.0 m above the ground in gaps formed by the uppermost, generally vertical branches of small shrubs and saplings. They were always found in humid, shaded
1. Smithsonian Tropical Research Institute, Apartado 2072, Balboa, Panama and Department of Zoology, University of Florida, Gainesville, Florida, 32611.
2. Department of Biology, Virginia Polytechnic Institute and State University, Blacksburg, Virginia 24061.
3. Smithsonian Tropical Research Institute and Escuela de Biologia, Universidad de Costa Rica, Ciudad Universitaria “Rodrigo Facio”, Costa Rica.
4. Museum of Comparative Zoology, Harvard University, Cambridge, Massachu- setts 02138.
* Manuscript received by the editor September 25, 1981.
29
30
Psyche
[Vol. 89
locations. Several individuals were kept and observed in an insect- ary at the Wau Ecology Institute (WEI).
Uloborus albolineatus and U. bispiralis were found on the Gazelle Peninsula, East New Britain (ENB), Papua New Guinea. The webs of U. bispiralis were observed on the Lowlands Agricultural Experi- mental Station (LAES) at Kerevat, ca. 100m elevation, in cocoa plantations and in secondary growth lowland forest and near Malasat (ENB) at ca. 600m elevation. One web of U. albolineatus was observed at LAES in secondary-growth forest along a river.
A single mature female of Uloborus #2072 (numbers refer to specimen numbers placed in vials) was found (by WGE) near Dan- deli, Karnataka, India, in the foliage of a bush growing in a teak forest. Uloborus trilineatus is common in undergrowth of gallery forest in eastern Colombia where WGE worked extensively. The webs described here were found at Finca Chenevo, about 20 km SW of El Porvenir, Meta, and Finca Mozambique, about 15 km SW of Puerto Lopez, Meta. Conifaber parvus was also found at Finca Mozambique (by WGE) where it occurred in periodically flooded forest but not in surrounding savanna.
Webs were first dusted with cornstarch or talcum powder using either the method described by Eberhard (1977a) or Carico’s (1977) modification of this method, and then measured and photographed. All specimens mentioned in this paper are deposited in the Museum of Comparative Zoology.
Observations Uloborus conus *
The Web
The web of U. conus has three parts: the inner orb, the rim, and the cone (Fig. 1). The inner orb and rim are in nearly the same plane and are more or less horizontal. The inner orb consists of a closed hub, radii and a few loops of non-sticky spiral, while the rim has several loops of sticky, cribellar spiral which end where the rim radii join those of the inner orb. Rim radii are continuous with those of the cone, and those of the inner orb are attached to them. Cone radii are attached in groups of two or three to a central guy thread which
♦This is a new species decribed below.
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
31
Figures 1-2. Web of Uloborus conus. 1. Side view showing the rim sticky spiral (RS), inner orb (I), cone (C) with jagged sticky spiral (CS) on a framework of radii and non-sticky spiral, and cone radii (CR) converging toward a central guy thread. Note that 2-3 cone radii are attached together to form one thread which attaches to the cone guy thread, and that these attachments are dispersed along the guy thread so that there is no single apical point to which all cone radii attach. 2. Top view showing typical Uloborus- type hub and non-sticky spiral of the inner orb. The cone with its jagged sticky spiral (CS) is seen through the plane of the orb. Note the gap between the non-sticky spirals of the cone and inner orb on the one hand and the rim sticky spiral on the other. The cone sticky spiral can be seen as a continuation of the rim spiral (arrow points to beginning of cone sticky spiral).
32
Psyche
[Vol. 89
is in turn attached distally to a leaf or branch. The cone has a non- sticky spiral and a few irregularly-spaced, jagged turns of cribellar silk. This jagged sticky spiral is a continuation of the innermost sticky spiral loop in the rim (Figs. 2, 4).
The hub of the inner orb (Fig. 2) is similar to that of other uloborid orbs, e.g. U. diver sus (Eberhard, 1972), and its spiral continues outward to form the non-sticky spiral of the inner orb. There is always a large gap between the last turn of this spiral and the innermost loop of sticky rim spiral (Figs. 1, 2).
Sticky spiral loops in the rim are more tightly spaced than are either the non-sticky spiral loops of the inner orb and cone or the cone’s sticky spiral. The outermost loop of rim spiral often follows a zigzagging path, with some segments of the sticky silk found on the radii (Figs. 2, 3). This zigzagging was more pronounced in some webs than in others and was generally most evident on the side of the orb which was larger (the orbs were rarely perfectly symmetrical).
Variations on this basic pattern were seen. Webs of immatures frequently had only a narrow rim, sometimes with only a single loop of sticky spiral. Some webs had a few loops of sticky spiral on the inner orb, with the non-sticky spiral left intact (Fig. 4). Webs of two adult females and several immatures had thin linear stabilimenta at their inner hubs. Adult males were found sitting on webs similar to those of immatures, but it was not determined if these were of their own construction. Adult males did not build webs in captivity.
Web Building Behavior
Web building by two adult females was observed from start to finish and various stages of web construction were seen on four other occasions. Durations of different stages of construction were noted for one of the adult females. Web construction began late at night or in early pre-dawn hours. The inner orb and cone of the old web were probably removed early in the night, but this behavior was not observed. One WEI female was found sitting at the center of a rudimentary web consisting of a partly collapsed rim and a few radii, and had a ball of silk in her mouthparts which shrank visibly as it wasj(presumably) ingested. This spider removed the rest of the rim and added the material to the ball of silk in her chelicerae before building the new web. Reusing frame threads from the previous web, the spider began construction by laying new radii.
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
33
Figures 3-4. Web of Uloborus conus. 3. Detail of first (outermost) loop of rim sticky spiral showing zigzag path with sticky silk laid directly on the radii. 4. Top view of web with 1 x/i loops of sticky spiral (IS) in the inner orb (IS). Also visible is the cone sticky spiral (CS) continuing in from the rim spiral (RS) and the zigzag outer loop of rim sticky spiral.
34
Psyche
[Vol. 89
Radii and non-sticky spiral were laid as in U. diversus (Eberhard, 1972) and their construction lasted 5 and 1.5 minutes, respectively. Radii were laid by walking out from the hub on an existing radius with a dragline, attaching the dragline to a frame thread, and then doubling it by walking back to the hub with another dragline. At the hub the dragline was attached to a succession of adjacent radii (forming the closed hub spiral) before the next radius was laid. When most of the radii were completed, the spider continued the hub spiral outward to form the non-sticky spiral, laying occasional “tertiary radii” (Le Guelte, 1966) during the process. This non-sticky spiral did not reach the frame threads.
At the start of the sticky spiral even very faint light falling on the spider caused her to cease spinning and bounce up and down on the web. Consequently, observations of sticky spiral construction were made only sporadically, using indirect lighting. The first (outer- most) loop of non-sticky spiral was completed in 13 min. During sticky spiral construction the spider reversed directions five times in the larger part of the web. The sticky spiral was attached to each radius that it crossed, and the spider broke non-sticky spiral loops as she laid the sticky spiral. One immature female was observed laying a zigzag outer loop of sticky spiral. The sequence of attachments of the cribellar silk to produce the zigzag loop (Fig. 5a) was distinct from that involved in laying the normal sticky spiral loops (Fig. 5b).
After meticulous, slow sticky spiral construction, which in one case lasted 3 hrs. 6 min., the spider suddenly began spinning out cribellar silk in a rapid and seemingly reckless fashion while moving inward toward the hub at an angle of about 25° to the last turn of the regular sticky spiral (Figs. 2, 4). After completing half a loop, the spider reversed direction and continued spiralling toward the hub, laying a jagged and irregularly spaced sticky spiral. The jagged spiral was attached to only a few radii, crossing 3-7 radii and, in some cases, several non-sticky spiral loops between attachments. The non-sticky spiral was left intact. This entire phase was very rapid and in one case the four jagged loops were completed in just 6 min. This jagged spiral was to become the sticky spiral of the future cone.
After completing the cone sticky spiral, the spider moved to the hub and slowly turned in a circle, pulling on successive radii with the first legs. After 2 min. she went out to the end of a radius and
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
35
Figure 5. Construction of U. conus web. (a) Sequence of attachments of sticky silk to produce the outer zigzag loop of rim sticky spiral. The spider started at the junction of the radius (Rl) and frame thread (F), attaching the cribellar thread at point A, walked along Rl toward the hub and attached the cribellar thread at point B, about half way between the frame thread and outer loop of non-sticky spiral (NS). The spider then continued inward along Rl, combing out cribellar silk, reached the non-sticky spiral and ran rapidly across it and 2/3 of the way out on R2 without combing out additional silk. It then continued to walk out on R2, combing out cribellar silk and attached the thread at point C, the junction between R2 and the frame thread. The sequence was then repeated, walking in along R2, attaching cribellar thread at point D, etc. (b) Sequence of attachments of cribellar silk to produce the normal sticky spiral. The spider attached cribellar thread at point A on radius Rl, walked in on Rl, combing out cribellar silk, until it reached the temporary, non-sticky spiral loop (NS), then ran along the non-sticky spiral and out on radius R2 without combing out cribellar silk and attached the cribellar thread to R2 at point B.
dropped from it to a leaf below, attached her dragline to the leaf, and went back up the dragline and across the web to its hub on a radius, attaching the new dragline from the leaf to the hub. This formed the central guy thread of the cone. The spider then went down the guy thread, broke it, reattached it to a different point on the leaf, and then returned to the hub. By this time the hub was al- ready drawn down under tension, and the web formed a shallow cone. The cone was then elongated by cutting radii at their attachment to the hub, lowering their tension and then attaching them to the central guy thread by the sequence of behaviors shown in Fig. 6a, b.
36
Psyche
[Vol. 89
Figure 6. Construction of U. conus web. Sequence of thread attachments in forming the cone (web viewed from the side). Arrows indicate direction of movement of the spider. Dots are points where attachments were made or broken, (a) The spider went to point X on radius R1 at the edge of the hub, cut the radius, attached its dragline to the inner broken end and then let out additional dragline as it faced away from the hub. This was then attached to the outer broken end which had now moved to point Xi. Usually adjacent radii were also broken and attached to radius Ri at point Xi (see also Fig. 1). (b) The spider then walked back toward the hub to point
Y, attached a dragline, ran to the hub and down the central guy thread (G), attaching the dragline at point Z. Radius Rl was thus pulled down toward the apex of the cone to form the cone radius YZ while the thread HY formed a temporary inner orb radius, (c) To move the temporary inner orb radius up on the cone, the spider walked out on temporary radius HY and broke it at its attachment to the cone at point Y. The spider then attached a dragline to the broken end and walked out on radius Rl, reattaching it at point A at the inner edge of the rim sticky spiral.
(d) The completed cone radius is indicated by line AZ and the new inner orb radius by line HA. The section AY of the cone radius bears the cone sticky spiral. The upper portion of the guy thread (HZ) was absent in the completed web, but it is not known when it was removed.
After forming the cone, the spider cut most of the temporary inner orb radii, thus collapsing the hub and leaving only a bit of silk to which a few temporary radii were attached. The spider then began replacing these temporary inner orb radii and at the same time completing cone formation by incorporating into the cone the
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
37
section of the original orb containing the jagged sticky spiral (Fig. 6c, d). This stage followed initial cone formation without interrup- tion, and it was difficult to determine when cone building ended and replacement and construction of new inner orb radii began. The spider went out to the cone along a temporary radius, broke the attachment to the cone and attached her dragline to the inner end of the temporary radius, then carried the radius upward by walking along radii and non-sticky spiral loops on the inner surface of the cone, and finally reattached it at or just inside (below) the innermost loop of the rim sticky spiral. She then walked back to the hub on the new radius, thereby doubling the thread. Upon reaching the center, she made attachments to form a new hub. The upper portion of the guy line was absent in finished webs, but it was not determined how it was removed.
Additional new inner orb radii were constructed in much the same manner as “normal” orb radii. The spider went out on an existing radius (or temporary radius) with a dragline, reached the cone non-sticky spiral, walked across it to the next cone radius, attached the dragline to the cone radius just below (inside) the rim spiral, and return to the hub on the new radius (doubling it). Consecutive radii were always laid with angles of more than 90° between them, perhaps serving to reduce differences in tension on all sides of the orb (Eberhard, 1981).
The last stages of web building, beginning with attachment of the dragline and ending with completion of the inner web, lasted 23 min.
Resting Postures
The spider normally sat under the hub with legs I and II slightly flexed and holding separate radii. When disturbed, the spider adopted a cryptic posture with legs I and II held together and flexed and legs III and IV pressed close to the body (Figs. 2, 4). This posture was adopted either at the hub or under a short “dragline” thread beneath the hub, which was attached to the hub at one end and to a radius at the other. When disturbed repeatedly, or when sunlight struck the web and made it visible, the spider dropped from the hub onto the dragline thread and bounced up and down on it. Spiders also bounced while wrapping prey and sometimes while going out to attack an insect or upon returning to the hub. This
38
Psyche
[Vol. 89
bouncing may be an anti-predator behavior similar to the bouncing flight of craneflies and the rapid vibrating of opilionids and pholcids.
Prey Capture Behavior.
Successful captures of five fruitflies ( Drosophila-sizQ ), one 4 mm long dolichopodid fly, one unidentified 1 mm fly, three 3^t mm ants, and one 5 mm lepidopteran larva were observed (by YDL). Of these, seven were trapped in the rim and three in the cone. All but one sequence conformed to the description given below. Like other uloborids (Marples, 1962; Eberhard, 1969; Lubin et al., 1978) U. conus and U. bispiralis immobilize all insects by wrapping in silk. Spiders ran out to the cone on an inner orb radius to reach insects trapped in the rim sticky spiral, squeezed through the cone (often turning sideways to do so) and continued out onto the undersurface of the rim. If an insect was trapped on the cone sticky spiral, the spider went through the cone and ran down the outer surface of the cone. Upon reaching the insect, the spider often tapped it with legs I, turned 180° so that it faced the hub (or upward on the cone) and began to wrap. Initially the prey was wrapped from a distance by throwing sheets of silk backwards with legs IV. Later the spider moved into contact with the prey and held it with legs II and III while wrapping. The spider interrupted wrapping to cut sticky spiral attachments, then cut the inner radius attachment (toward the hub) and continued to wrap while holding the end of the radius with one leg I. Finally, the outer (distal) end of the radius was cut and the prey was held free of the web in legs II and III while the spider hung from the broken radius by legs I, bridging the gap with its body, and wrapped the prey with legs IV while rotating it occasionally with the palps or legs.
All prey were carried to the hub in the palps (with the aid of the chelicerae), held “overhead” in characteristic uloborid fashion. After transferring the prey package from the legs to the palps, the spider attached a dragline to the distal end of the broken radius and then to the proximal end, thus closing the gap. At the hub the spider again transferred the prey from the palps to legs II and III and wrapped it while hanging from the dragline thread beneath the hub. In most instances the dragline thread appeared to be broken and the spider spanned the gap with its body.
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
39
Prey Capture Sequences With Different Prey Types.
The only case not conforming to this description was that of a fruitfly caught on the inner orb; the spider wrapped it, secured it by reattaching it to the radius and fed on the prey in situ.
U. conus rejected or ignored a number of insects offered as prey. Five small orthopteran nymphs 3-4 mm long (probably newly emerged) where given to adult females and all were rejected. On two occasions, the spiders approached and tapped the insects with legs I and then returned to the hub. In other instances the spider pulled the radii in the direction of the orthopteran, shook the web and then ignored it. The same individuals readily attacked fruitflies offered as prey after the orthopterans. Fruitflies were not attacked on three occasions when they were offered while the spider was already wrapping a prey or feeding at the hub. Two ants ( Anopolepis longipes, 4mm long) were rejected under the same circumstances.
Sequences With Multiple Prey.
On six occasions spiders feeding at the hub attacked second or third prey thrown into their webs. These included two ants, two fruitflies, a dolichopodid fly and an unidentified small fly. On all but one occasion the spider carried the first prey in its palps as it ran out to attack the second. In one instance a spider that had been wrapping the first prey at the hub attached this insect to a dragline thread below the hub before going out to attack the second insect.
The second prey was immobilized in the same manner as the first, but rather than cut this insect out and carry it to the hub, the spider secured the second prey at the capture site and returned to the hub to resume feeding on the first prey. While performing immobili- zation wrapping, the spider usually broke the radius attached to the prey on the inner side (toward the hub), but not on the outer side. Before leaving it at the capture site, the spider reattached the prey to the broken end of the radius, thus securing it at both ends.
Eggsac and Eggsac Web.
The eggsac of U. conus is about 8mm long by 3mm wide, with angular projections along the edges (Fig. 7). It is suspended in an eggsac web on a strengthened radius of a former web, where the hub of the inner orb had been. The web is similar to those of U. diversus (Eberhard, 1969) and Miagrammopes sp. near unipus (Lubin et al. 1978) and consists of frame threads, a few radii and one or more
40
Psyche
[Vol. 89
zigzag loops of sticky silk, with some sticky silk laid directly on the radii. The radii are attached to the main eggsac radius or to the eggsac itself. One female had a three-dimensional eggsac web consisting of a rudimentary cone and inner orb radii (Fig. 7) with sticky silk in both the plane of the orb and the cone. Unlike the eggsac webs of Miagrammopes, these webs were retained both day and night. Insects that became entangled in the sticky threads were attacked in the usual manner.
Females guarded their eggsacs (one per female) until the young emerged (13 days for one eggsac). Newly emerged spiderlings remained on the eggsac web for one or two days, then moved away and constructed typical Uloborus-type “baby webs”, consisting of radial threads connected by a thin sheet of very fine, non-sticky silk (Szlep, 1961; Eberhard, 1977b) without any cone. One immature, however, had an orb plus cone-web with a filmy “baby web” sheet where the rim sticky spiral would normally be found and also some “baby web” sheet on the cone. Structural spirals were present in the rim and inner orb; there was no sticky spiral.
Uloborus bispiralis*
The cone web of U. bispiralis (Fig. 8) is similar to that of U. conus in that the cone sticky spiral is continuous with that of the rim, and the outer loop(s) of rim spiral follow a zigzag path, with some sticky silk laid on the radii. Unlike webs of U. conus , the inner orb non- sticky spiral extends right up to the innermost (last) loop of rim sticky spiral and all webs had a few loops of sticky spiral in the inner orb. Most webs also had a thin, linear stabilimentum of white silk across the inner orb, with a spider-size gap at the hub.
Webs of juvenile females were similar in all respects to those of adults. None of the webs observed showed signs of repairs. Like those of U. conus, they are probably renewed daily. On one occasion only, a juvenile female was seen hanging inside the cone while an adult male fed on prey at the hub. Another adult male was observed sitting at the edge of an adult female’s web and a third male was found sitting in a small cone-web (no sticky spiral was observed).
This is a new species, described below.
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
41
Figures 7-9. Uloborus. 7. Eggsac and three-dimensional eggsac web of Ulo- borus conus. The female spider can be seen sitting in a cryptic posture to the left of the eggsac. Sticky threads (heavy white lines) occur in the plane of the former orb and on the rudimentary cone. 8. Web of Uloborus bispiralis. 9. Tubular eggsac of Uloborus bispiralis with female sitting in cryptic posture at one end of the eggsac (arrow).
42
Psyche
[Vol. 89
The long, tubular eggsacs of U. bispiralis (34-40 mm long and 1 .5 mm wide) have no angular projections (Fig. 9) and resemble those of Miagrammopes (Lubin et al. 1978). They are suspended along the radius of a former web of which only a few radii and frame threads remained intact. There was no evidence of sticky silk in the four eggsac webs examined. Spiders sat in line with the eggsacs, with legs I and II extended forward and legs IV grasping the eggsac, and were reluctant to move even when prodded.
Uloborus albolineatus*
One individual of U. albolineatus was observed on a cone web similar to that of U. bispiralis. The rim spiral had one or two zigzag outer loops, and both the cone and inner orb had jagged loops of sticky spiral. The inner orb non-sticky spiral extended almost to the rim spiral. The female sat at the hub with legs I and II extended forward and held together and legs IV extended backward.
Uloborus sp. (2072)
Only a single web was seen. It consisted of a somewhat inclined orb (43° with horizontal) with a cone underneath it which contained loops of sticky spiral (Fig. 10a, b). This web differed from those of U. Conus in having sticky spiral threads near the center of the horizontal orb (Fig. 10c) as well as near its edge, as well as having some of the “radial lines” of the cone attached directly to the frame of the orb while others ended on radii as in U. conus webs.
At the hub the spider sat in a “crouched” position (Fig. 10a) similar to that of Philoponella (Opell and Eberhard in prep.), and was reluctant to move away when disturbed.
Uloborus trilineatus Keyserling
Most of the many webs of mature and immature U. trilineatus individuals observed were typical, more or less horizontal orbs like those spun by other Uloborus species (e.g., Szlep, 1961; Wiehle, 1927; Eberhard, 1972). Webs of mature males were similar to those of newly emerged uloborid spiderlings (Szlep, 1961; Eberhard,
♦This is a new species, described below.
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
43
Figure 10. Web of Uloborus sp. (#2072). A. Side view with spider (arrow) at hub. B. Top view. C. Enlargement of the hub. Both cone and orb spirals are sticky. Most cone radii are attached to orb radii, but some end on frame lines. The cone sticky spiral seems not to be continuous with the orb spiral.
44
Psyche
[Vol. 89
1977b). However, at both Finca Chenevo and Finca Mozambique one immature was found at the hub of a web like that shown in Figs. 11a, b. Each web consisted of a small, more or less horizon- tal orb which had only a non-sticky spiral. Below this was a cone which also had a non-sticky spiral. Only one of these spiders was collected, the other was left on its web, and the next day the web was deserted and an exuvium was found clinging to its hub. Identity of the collected immature specimen is not certain, but abundance of U. trilineatus at these sites plus the failure of extensive collecting of orb weavers to reveal similar species in these habitats indicates that these immatures were U. trilineatus.
Conifaber parvus *
This species was fairly common in a periodically flooded forest on Finca Mozambique. Only mature females were found with webs. The webs all had an “orb” similar or identical to those spun by most newly emerged uloborid spiderlings (Szlep, 1961; Eberhard, 1977b), having radii, hub, frames, and a non-sticky spiral as in typical orbs but lacking a sticky spiral and having instead a dense mat of very fine threads (so fine that in Figs. 12a, b they do not show up as individual threads, and one only sees the grains of cornstarch). Below this orb was a conical web consisting of radii which converged below to a single downward-directed line, and a more or less regularly spaced spiral, also of non-sticky silk. The hubs were often decorated with linear stabilimenta.
The spider crouched at the hub with its legs I folded ventrally in the typical Philoponella posture (Opell and Eberhard in prep.). Sometimes when a spider was disturbed she let herself fall from the hub and hung suspended inside the cone on her dragline and bounced actively there. On other occasions spiders bounced on their orbs.
Attack behavior was observed twice and seemed to be typical for uloborids. The spider turned to face away from the prey and threw silk over it with her legs IV, gradually cut it loose as she wrapped it, then held it with the palps and/or chelicerae as she reattached the ends of the broken radii, took it to the hub, and then resumed
These are a new genus and species, described below.
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
45
Figure 11. Web of penultimate female of Uloborus trilineatus Keyserling. A. Side view. B. Top view. Most (or all?) of the cone radii are attached to frame lines. The central area of the cone has fewer radii than the upper portion, and gives the impression of having been partially dismantled, perhaps during the process of being connected to the central thread as in U. consu.
46
Psyche
[Vol. 89
wrapping while hanging there by her spread legs I.
The eggsacs were different from those described for any other uloborid. They were pure white, 2-3 mm diameter spheres with projecting spikes, and resembled the heads of maces; they were suspended in the plane of the orb portion of the web on a radial line (Figs. 13a, b).
Discussion
While the webs of all five species are similar in having more or less horizontal orbs with cones below, the details are strikingly different. The cones of U. conus, U. albolineatus, U. bispiralis, and U. #2702 have a sticky spiral while those of U. trilineatus and C. parvus do not. In U. albolineatus, U. bispiralis, and U. sp. #2702 both the outer (rim) and inner portions of the orb have sticky spirals, while in U. conus the main capture surface is the rim sticky spiral and only occasionally is a sticky spiral present in the inner orb. The “orbs” of Conifaber parvus have no sticky spiral, but the dense mat serves as a trapping surface, as in uloborid “baby webs”. Orb-plus-cone webs of U. trilineatus have no sticky silk at all.
The function of the cone in webs of all four species is probably primarily defense of the spider at the hub against predators and parasites. The cone forms a “cage” of threads around the spider, and a defense function is suggested both by the fact that U. conus and Conifaber parvus drop from the orb and hang inside this cone when disturbed or when the web becomes visible in sunlight, and by the fact that construction of conewebs by U. trilineatus occurs only when the spiders are about to enter the particularly vulnerable moulting period. The sticky threads in the cones of U. conus and U. albolineatus and U. #2702 sometimes trap prey (some U. conus webs have almost no other sticky lines), but the fact that the cones of U. conus, U. albolineatus, and U. bispiralis have only a few, irregularly spaced sticky spiral loops while those of U. trilineatus and C. parvus lack sticky threads suggests that prey capture is a secondary consequence rather than a primary function of at least some of the cones. Placement of sticky threads in cones could have evolved as an additional defense of the spider against predation or parasitism.
The uloborid cones resemble the barrier meshes made by the araneid Nephila maculata (Robinson and Robinson, 1973) at one or both sides of their more-or-less vertical orbs; in young N. maculata
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
47
Figure 12. Conifabar parvus web. A. Side view showing framework threads, radii, mat of non-sticky spirals, and cone radii. B. Top view showing non-sticky spiral mat, two stellate eggsacs, and the female (arrow) resting at the web’s hub.
Figure 13. Conifaber parvus web hub and eggsacs. A. Female (arrow) resting at hub. Two stellate eggsacs and some of the horizontal web’s fine, non-sticky threads are visible. B. Female (arrow) resting in crouched posture at the hub of a web decorated with linear stabilimenta.
48
Psyche
[Vol. 89
the mesh is a cone-shaped, rudimentary orb with no sticky spiral. The Robinsons attributed a defensive function to these structures, and indeed the arguments developed here suggest that barrier meshes made by a number of other araneids ( Metepeira , Leucauge, Argiope, Arachnura, Gasteracantha, and Phonognatho) may also function defensively.
The evolutionary origin of the orb-plus-cone web designs in uloborids is not clear. At least two other uloborid orb-plus-cone webs are known. Workman (1896) described the orb-plus-cone web of Uloborus quadrituberculatus (Thorell). His apparently schematic drawing shows a horizontal orb lacking spiral lines and a cone with a 14 loop spiral (he did not note whether or not the spiral was sticky). The cone is attached on all sides to surrounding vegetation by short lines. In Sembrong Jungle near Layang-Layang, Johore, Malaya, Frances Murphy photographed the orb-plus-cone web of a specimen matching Workman’s (1896) description of U. quadri- tuberculatus. This web was constructed about 1.5 m above the ground and had a zigzag outer loop and an irregular cone spiral. An unidentified species of Tangaroa collected in mesophyll rainforest in the Iron Range, northeastern Queensland, Australia had an orb-plus cone web with a zigzag outer loop of rim sticky spiral (V. Todd Davies, personal communication). It is not known if the cone spiral was sticky. However, a small, unidentified Tangaroa species from Yap, Caroline Islands constructed a horizontal orb-web in both the field and lab (Joseph Beatty and James Berry, personal communica- tion and BDO unpublished observations, respectively), indicating that the cone-web is not characteristic of all members of this most primitive uloborid genus (Opell, 1979) and, therefore, does not represent the “original” uloborid web design.
We do not know if the cones of the five species studied here are constructed in the same manner. Certain behaviors associated with cone construction in U. conus (and probably U. albolineatus and U. bispiralis ) including the laying of a jagged sticky spiral with few attachments to the radii, formation of a cone by cutting and reattaching radii to a central line, replacement and reposition of radii, and pulling the orb into a cone, have not been seen in other uloborids. When one takes into account the webs of other uloborids such as Philoponella vicina (Peters 1953, 1955), P. semiplumosa (Lahmann and Eberhard 1979), P. oweni (Eberhard 1969), P. divisa (Opell 1979), and P. para (Eberhard, unpub.) which are more or less
1982] Lubin, Opell, Eberhard, Levi — Uloboridae 49
reduced and modified planar or domed orbs in the midst of meshes which include sticky as well as non-sticky threads ( P . oweni also spins orbs without meshes— Eberhard, 1969), the “orb” of Polenecia ( =Sybota ) which lacks sticky spirals and has instead sticky radii (Wiehle 1931), the orbs cum sheet webs spun by young spiderlings and mature males of several species (Szlep, 1961; Eberhard, 1977b), and the various simplified webs of Hyptiotes (Wiehle 1927, Marples and Marples 1937) and Miagrammopes (Akermann 1932, Lubin et al. 1978), it becomes clear that there is an extraordinary diversity of web forms in the relatively small family Uloboridae. It is likely that, in conjunction with morphological studies, a fuller understanding of the webs and behavior of uloborids will shed more light on relation- ships within the family.
Systematic Section
Conifaber new genus*
Figures 14-15, 20-29
Type. The type species of Conifaber is Conifaber parvus, new species. The genus name is a masculine noun derived from the Latin nouns conus and faber and means “cone craftsman”.
Diagnosis. Conifaber contains the smallest known uloborids, females being 2.0 mm and males 1 .5 mm long. Because of their small size members of this genus are more likely to be confused with those of Ariston and Siratoba than with Zosis, Octonoba, and Purumitra, to which they are more closely related. Conifaber males and females are distinguished from those of Ariston and Siratoba (Opell, 1979; figs. 41, 72) by having a strongly recurved anterior eye row whose median eyes are located on a slight anterior carapace extension and have a diameter twice that of the other eyes (Figs. 20-23). Unlike Ariston and Siratoba females whose first femora are 1.5 and 2.0 times the carapace length, respectively, and whose thoracic grooves are in the carapace’s posterior two-fifths, Conifaber females have first femora equal in length to the carapace and have a centrally located thoracic groove. Like Ariston, but unlike Siratoba, Coni-
*For nomenclatural purposes B. D. Opell is the author of the genus Conifaber and the species C. parvus.
50
Psyche
[Vol. 89
faber females lack dorsal abdominal tubercles. Like Siratoba but unlike Ariston, their clypeus height in anterior view is equal to the AME diameter. Conifaber males lack first femoral macrosetae present in Ariston and Siratoba males (Opell, 1979, figs. 39, 70) and, like Ariston, lack abdominal tubercles.
Using Opell’s (1979) keys to uloborid genera, Conifaber males key to couplet 10, which separates Octonoba and Purumitra, and females key to couplet 10, which separates Octonoba and Uloborus. Conifaber males are distinguished from those of Octonoba and Purumitra by having first femora whose lengths are equal to rather than 1.5 to 2.0 times as long as the carapace, by lacking femoral macrosetae present in these genera (Opell, 1979; figs. 181, 183), and by having a longer, more conspicuous tegular spur than these genera (Fig. 14; Opell, 1979; plate 6-c, fig. 157). Conifaber females lack dorsal abdominal tubercles present in Octonoba and Uloborus (Opell, 1979; figs. 132, 140) and have inconspicuous, anteriorly directed epigynal lobes (Figs. 24-26) instead of conspicuous poste- riorly directed lateral epigynal lobes (Opell, 1979; figs. 137, 145, 178, 184).
Description. Maximum carapace width 0.84 carapace length, attained in posterior half of female carapace and in posterior third of male carapace (Figs. 21-22). Female carapace slopes up to a point just behind PLE and then down to AME (Fig. 20). Male carapace slopes more steeply up to a point slightly forward of its center and then down to PME (Fig. 23). Shallow, transverse female thoracic groove at carapace center; deep, U-shaped male thoracic groove in posterior quarter of carapace. In both sexes anterior eye row strongly recurved so that a line across AME’s posterior margins passes in front of ALE’s by a distance equal to one ALE diameter. Posterior eye row slightly recurved so that a line across PME’s posterior margins passes along PLE’s anterior margins. Median ocular area’s length and posterior width 0.8 its anterior width. Female AME diameter 0.75 that of male AME, remaining eyes equal to 0.66 female AME and 0.50 male AME. AME’s 1.3 as far from one another as from ALE’s, PME’s 1 .7 as far from one another as from PLE’s. Sternum 0.80 as wide as long, widest between first and second coxae. Female endite 0.80 and male endite 1.00 as wide as long. Labium 1.40 as wide as long. First femur equal in length to carapace. Male first tibia with six or seven short and one long
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
51
Figures 14 and 15. Apical (14) and retrolateral (15) views of Conifaber parvus n. sp. holotype male left palpus. The arrow in 15 shows the normal position of the tegular spur (TS) embolus (E) guide as it rests in the grooved tegulum (T). MAB = median apophysis bulb, MAS = median apophysis spur, MH = middle hemato- docha. Scale lines are 100 yum long.
52
Psyche
[Vol. 89
dorsoprolateral macrosetae, two or three long proximodorsal macrosetae, and two or three distoretrolateral macrosetae (Fig. 28). Abdomen without tubercles or abrupt peak (Figs. 20-23). Female abdomen 0.98 as wide and 1.38 as high as long, male abdomen 0.70 as wide and 0.93 as high as long. Distance between cribellum and epigastric furrow 0.44 abdomen length. Abdomen and cephalo- thorax were separated when the epigynum was removed. Examina- tion of the severed petiole revealed no large tracheal trunks, indicating that, as in Philoponella and Daramuliana (Opell, 1979 fig. 1), no tracheae extend into the cephalothorax or, as in Zosis, Purumitra, and Octonoba (Opell, 1979; fig. 2), only fine tracheoles extend into the cephalothorax.
Male Palpus. Femur without ventral tubercles. Like Zosis, Puru- mitra and Octonoba (Opell, 1979; plates 6-c,d, 7-c,d, fig. 157), Conifaber male palpi have a tegular spur which acts as an embolus guide (Figs. 14-15). This tegular spur is proportionately larger than those of other genera and rests in a tegular groove unique to Conifaber. Members of Zosis also have a large, grooved tegular spur, but the median apophysis bulb of Conifaber is a plate rather than a hemisphere, and its median apophysis spur a grooved plate rather than a hook. The tegular spur’s tip may rest in the median apopysis spur’s distal groove.
Epigynum. Two posterior lateral epigynal lobes extend anteriorly a short distance, concealing a pair of weakly sclerotized, anteriorly directed oval areas (Figs. 24-25). In posterior view the epigynum’s posterior plate is 0.6 as high as broad and has slightly curved and rounded ventral rim about one third the height of the posterior plate (Fig. 26). A highly coiled duct leads from each weakly sclerotized oval to a spherical spermatheca whose short fertilization duct appears to connect to the vagina’s ventrolateral margin (Fig. 27).
Distribution. This genus is known only from the type localities in eastern central Colombia.
Conifaber parvus new species Figures 14-15, 20-29
Types. Male holotype, male paratype, and female paratype from Finca Mozambique, 15 km S.W. of Puerto Lopez in the
1982] Lubin, Opell, Eberhard, Levi — Uloboridae 53
Colombian department of Meta; collected 1978 by W. G. Eberhard, in the Museum of Comparative Zoology. The specific epithet is a Latin noun in apposition, referring to the small size of members of this species.
Description. As most features of this species are presented in the genus description, only those of color and size are given here. Total length of female 1.92 mm, of males 1.50 mm. Female carapace 0.72 mm long, male carapace 0.66 mm long. Female sternum 0.44 mm long, male sternum 0.38 mm long. Female AME diameter 60 jum, male AME diameter 80 ^m, remaining eyes of both sexes 40 pm in diameter. Female leg length (I— IV): 2.86, 1.78, 1.52, 2.42 mm. Male leg length: 2.70, 1.56, 1.33, 1.94 mm. Female calamistrum composed of 10 setae and 0.22 mm long, extending 0.52 the metatarsus length. Female cribellum 180 wide, 60 ^m long. Female anterior spinnerets 0.30 mm long, male 0.16 mm long. Female posterior spinnerets 0.27 long, male 0.18 mm long. Female anal tubercle 0.14 mm long, male 0.10 mm long.
Except for dark circles around the eyes (Figs. 21-22) members of neither sex have conspicuous color markings. The thoracic groove is slightly darker than the rest of the carapace, and white guanine deposits under the abdomen’s integument are interrupted by the cardiac area which creates a tan median stripe (Figs. 21-22). Lacking these deposits, the anterior third of the female’s abdomen is also tan rather than white.
Distribution. Known only from the type locality in eastern central Colombia.
Uloborus conus new species*
Figures 16-19, 30-35
Types: All types from Papua New Guinea. Female holotype and
paratype from Madang Prov., 40 km south of Madang, collected 21 March 1979 by H. W. Levi and Y. D. Lubin. Two male and three female paratypes from Morobe Prov., Buso Forest Reserve, col- lected 25 Oct. 1979 by Y. D. Lubin. Four female paratypes from
*For nomenclatural purposes B. D. Opell is the author of this species.
54
Psyche
[Vol. 89
Figures 16-19. Uloborus conus n. sp. 16. Retrolateral view of holotype male left palpus (a trilobed piece of debris is lodged at the upper right). 17. Retrolateral view of MAS. 18. Apical view of MAS. 19. Ventral view of female paratype epigy- num. C = conductor; other abbreviations as in Figures 14 and 15. Scale lines are 100 jum long.
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
55
Central Prov., along Brown River, near Port Moresby, collected 29 April 1980 by Y. D. Lubin. One male and one female paratype deposited in the American Museum of Natural History, the remain- ing types are deposited in the Museum of Comparative Zoology. The specific epithet is a Latin noun in apposition, referring to the conical web produced by members of this species.
Diagnosis. Males and females are distinguished by a carapace
length of less than 1.00 and 1.30 mm, respectively. Males have a long, lobed palpal femoral tubercle, a reduced, flattened median apophy- sis, a long, broad conductor, and a blunt median apophysis spur (Figs. 16-18). Length of female femur I less than 1.2 carapace length rather than 1.4- 1.5 carapace length as in other uloborids. Central region of epigynum from which lobes arise about one third rather than half as wide as the posterior plate (Figs. 19, 34).
Description. Female. Total length 2.80-3.40 mm (X = 3.20), carapace length 1 .00-1.30 mm (X = 1 .09), maximum carapace width 0.90-1.00 (X = 0.96), carapace width at PLE’s 0.58-0.64 mm (X = 0.60), area. All eyes except AME’s surrounded by small black circles (Fig. 30). PLE nearer midline than in other Uloborus species. Sternum tan. Leg I of most specimens as shown in Fig. 33, but nearly black in two dark specimens. Dorsum of femur I of all specimens black. Abdomen of most specimens light tan or white. Abdomen of two dark specimens with white dorsum, black venter and two broad, white lateral stripes extending from anterior apex to posterior tips. Epigynum consists of two small, weakly sclerotized posterior lobes (Fig. 19) whose combined basal width is one-third that of the posterior plate (Fig. 34). An epigynal opening found dorsal to each lobe leads to a large, irregular spermatheca from whose posterior lateral margin a short fertilization duct extends (Fig. 35).
Male. Total length 2.00-2.20 mm, carapace length 1.00 mm, maximum carapace length 0.85 mm, carapace width at PLE’s 0.66 mm, sternum length 0.56 mm. Carapace and sternum coloration similar to that of female except that broad gray streaks extend anteriorly from the posterior eyes (Fig. 31). Legs light tan, tibiae II-IV with light gray dorsal tip. Femur I with three prolateral, one dorsal, central; and one distal, retrolateral macrosetae (Fig. 32).
56
Psyche
[Vol. 89
Figures 20-27. Conifaber parvus n. sp. 20. Lateral view of female. 21. Dorsal view of female. 22. Dorsal view of male. 23. Lateral view of male. 24. Anterior view of epigynum. 25. Ventral view of epigynum. 26. Posterior view of epigy- num. C = conductor. D = other abbreviations as in Figures 14 and 15. Scale lines are 100 jum long.
1982] Lubin, Ope 1 1, Eberhard, Levi — Uloboridae 57
Tibia I with eight prolateral, seven dorsal, and three retrolateral macrosetae. Sternum and abdominal venter with orange setae. Abdomen gray with a pair of thin, white, lateral longitudinal stripes running nearly its full length. Palpal femur with a large, lobed retrolateral tubercle and a very small prolateral tubercle (Fig. 16). Median apophysis bulb small and flattened (Fig. 16); median apophysis rectangular with a blunt apex (Figs. 17-18). Conductor long and broad, extending from median apophysis spur to area of palp adjacent to patella.
Distribution. Known only from the type localities in Papua New Guinea.
Uloborus albolineatus new species*
Figures 36-39.
Type. Female holotype from Lowlands Agricultural Experimental Station, Kerevat, East New Britain, Papua New Guinea, collected 6 July 1980 by Y. D. Lubin, deposited in the Museum of Comparative Zoology. The specific epithet is a noun in apposition, referring to the species’ white median abdominal stripe.
Diagnosis. Males are unknown. The female is distinguished by having reddish brown median eyes, a very convex sternum (Fig. 37), white guanine deposits in the cardiac region (Fig. 36), and weakly sclerotized epigynal lobes rising from the center rather than poste- rior of a transparent epigynum (Fig. 38). Unlike many Uloborus species, the carapace lacks a conspicuous median light stripe.
Description. Female. Total length 2.40 mm, carapace length 0.92 mm. maximum carapace width 0.74 mm, carapace width at PLE’s 0.50 mm. Carapace tan with gray, reticulate lateral markings (Fig. 36). Median eyes reddish brown. AME’s on a more conspicuous tubercle than most Uloborus species. Sternum tan, widest at coxae I rather than between coxae I and II as in other Uloborus species. Legs light tan with faint gray distal rings on most segments. Tibia I with very sparse distal setal brush. Abdomen height and width 0.9 its length, dorsum with a pair of centrolateral tubercles, posterior
For nomenclatural purposes, B. D. Opell is author of this species.
58
Psyche
[Vol. 89
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
59
tip projecting slightly posterior to anal tubercle’s base and separated from anal tubercle by a distance one third the abdomen’s height. White guanine deposits extend both in a narrow transverse band across the abdomen’s anterior ventral surface and along the cardiac area. A broader, more diffuse median guanine deposit extends from the abdomen’s humps to its posterior tip. A pair of large guanine spots is found anteriolaterally to the spinnerets. Epigynum convex with broad posterior extension, a pair of low, weakly sclerotized median lobes, and a transparent integument through which a single pair of spherical spermathecae is clearly visible (Figs. 38, 39).
Distribution. Known only from the type locality in Papua New Guinea.
Uloborus bispiralis new species*
Figures 40-48.
Types: Female holotype, three male and seven female paratypes
from Fowlands Agricultural Experimental Station at Kerevat, East New Britian Prov., collected 2, 4, and 6 July 1980 by Y. D. Fubin. Male and two female paratypes deposited in the American Museum of Natural History, remaining types in the Museum of Comparative Zoology. The specific epithet is a latin noun in apposition, referring to the male’s doubly coiled embolus.
Diagnosis. Females are distinguished by having a single, narrow median, posterior epigynal lobe (Figs. 42, 43) rather than a pair of posterior epigynal lobes, and by each epigynal duct making five rather than the usual single loop (Fig. 44). Males are distinguished by an embolus which loops twice rather than once around the
*For nomenclatural purposes B. D. Opell is the author of this species.
Figures 28 and 29. Conifaber parvus n. sp. 28. Dorsal view of male left first tibia. 29. Retrolateral view of expanded male left palpus (R = radix, BH = basal hematodocha, other abbreviations as in Figs. 14 and 15).
Figures 30-35. Uloborus conus n. sp. 30. Dorsal view of female carapace. 31. Dorsal view of male carapace. 32. Prolateral view of male first femur, patella, and tibia. 33. Retrolateral view of female leg I. 34. Posterior view of epigynum. 35. Dorsal view of cleared epigynum.
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
61
median apophysis and by a flattened, elongate median apophysis bulb which bears a broad conductor (Figs. 45, 46). Both males and females have a gray lateral abdominal stripe (Fig. 48).
Description. Female. Total length 3.28-3.68 mm (X = 3.47, S, 0.14, N = 8), carapace length 1.10-1.20 mm(X= 1.15, SD = 0.04), maximum carapace width 0.94-1.04 (X = 0.98, SD 0.04), carapace width at PME’s 0.54-0.58 mm (X = 0.56, SD 0.01). All eyes except AME’s surrounded by small black circles (Fig. 41). Carapace with light lateral margins, light posterior median stripe, and central gray patch. Sternum tan. First and second legs light gray with tan proximal ring on tibia, metatarsus, and tarsus. Tibia I without a conspicuous setal brush. Third and fourth legs tan with gray distal rings on tibia, metatarsus, and tarsus. Abdomen without humps, dorsal and lateral surfaces densely covered by white guanine spots except in cardiac region and along a faint lateral stripe similar to but not as sharply defined as that shown in Fig. 48. Venter tan with only sparse guanine spots. Epigynum a raised mound with single median lobe (Figs. 42, 43), probably representing a pair of fused lateral lobes. Under normal light microscopy a clove oil-cleared epigynum showed only a pair of oval spermathecae with a fertilization duct leading from the posterior lateral margin of each and a short, broad duct extending from the median surface of each to epigynum’s posterior margin. Examination with Nomarski optics revealed the more extensive system of thin-walled ducts shown in Figure 44. It was not possible to determine precisely where the ducts opened externally, but this appears to be between the spermathecae and near the base of the epigynal lobe.
Male. Total length 2.32-2.40 mm, carapace length 0.98-1.00 mm, maximum carapace width 0.78-0.80 mm, carapace width at PLE’s 0.50-0.52 mm. Carapace and sternum coloration similar to that of
Figures 36-39. Uloborus albolineatus n. sp. 36. Dorsal view of female holotype. 37. Lateral view of female carapace. 38. Ventral view of epigynum. 39. Dorsal view of cleared epigynum.
Figures 40-48. Uloborus bispiralis n. sp. 40. Male carapace. 41. Female holo- type carapace. 42. Ventral view of holotype epigynum. 43. Posterior view of epigynum. 44. Dorsal view of cleared epigynum. 45. Retrolateral view of male palpus. 46. Apical view of male palpus. 47. Prolateral view of male first femur, patella, and tibia. 48. Lateral view of male abdomen.
62
Psyche
[Vol. 89
females except for absence of central gray carapace spot (Fig. 40). Legs reddish brown. Femur I with three or four prolateral macro- setae, tibia I with nine prolateral, six or seven dorsal, and three retrolateral macrosetae (Fig. 47). Abdomen with fewer guanine spots than female, dorsum and lateral surface tan; gray lateral stripe, gray venter and gray posterior tip (Fig. 48). Palpal femur with a large proximal retrolateral tubercle and small prolateral tubercle. Median apophysis bulb flat and elongate (0.16 mm long), terminating in a bent median apophysis spur (Figs. 46, 47). Unlike other members of the genus, the embolus loops twice around the median apophysis bulb before passing into a broad, weakly scle- rotized conductor.
Distribution. Known only from the type locality in Papua New Guinea.
Acknowledgements
YDL and HWL thank the Wau Ecology Institute for use of the facilities in Wau, and S. Smith for making available the facilities at LAES (Kerevat). A portion of this study was supported by a Smithsonian Institute Scholarly Studies Research Award (to M. H. Robinson and YDL). A Small Projects Grant from the College of Arts and Sciences, Virginia Polytechnic Inst, and State Univ. (to BDO) made the S.E.M. work possible. WGE thanks Carlos Rod- rigues, the Dixon Stroud family. Dr. Luis Arango, Dr. Madhav Gadgil, and A. J. T. Johnsingh for help and hospitality in the field and the Comite de Investigaciones of the Universidad del Valle, Cali, Colombia and the Vicerectoria de Investigaciones of the Universidad de Costa Rica for financial support. HWL thanks National Science Foundation grant DEB 76-15568 and DEB 79-23004 for support and M. H. Robinson and B. Robinson for being instrumental in getting him to New Guinea and flavoring his stay with their hospitality and enthusiasm. We thank Frances Murphy, V. Todd Davies, Joseph Beatty and James Berry for allowing us to use their unpublished observations and M. H. Robinson and B. Robinson for their comments on and criticism of the manuscript.
1982]
Lubin, Opell, Eberhard, Levi — Uloboridae
63
Literature Cited
Ackermann, C.
1932. On the spider Miagrammopes sp. which constructs a single-line snare. Ann. Natal mus. 7:137-143.
Carico, J. E.
1977. A simple device for coating orb webs for field photography. Bull. Br. arachnol. Soc. 4:100.
Eberhard, W. G.
1969. The spider Uloborus diversus Marx and its web. PhD. thesis, Harvard Univ.
1972. The web of Uloborus diversus (Araneae: Uloboridae). J. Zool., Lond. 166:417-465.
1977a. Photography of orb webs in the field. Bull. Br. arachnol. Soc. 3(7):200-204.
1977b. The webs of newly emerged Uloborus diversus and of a male Uloborus sp. (Araneae: Uloboridae). J. Arachnol. 4:201-206.
1981. Construction behaviour and the distribution of tensions in orb webs. Bull. Br. arachnol. Soc. 5(5): 189-204.
Lahmann, E. and W. G. Eberhard
1979. Factores selectivos que afectan la tendencia a agruparse en la arana colonial Philoponella semiplumosa (Araneae: Uloboridae). Rev. Biol. Trop. 27(2):23 1-240.
LeGuelte, L.
1966. Structure de la toile de Zygiella x-notata C. (Araignees, Argiopidae) et facteurs que regissent le comportement de l’araignee pendant la con- struction de la toile. These. Pub. Univ. Nancy: 1-77.
Lubin, Y. D., W. G. Eberhard, and G. G. Montgomery
1978. Webs of Miagrammopes (Araneae: Uloboridae) in the Neotropics. Psyche 85(1): 1-23.
Marples, M. and B. J. Marples
1937. Notes on the spiders Hyptiotes paradoxus and Cyclosa conica. Proc. zool. Soc. Lond. Ser. A Part 3 1937:213-221.
Marples, B. J.
1962. Notes on the spiders of the family Uloboridae. Ann. Zool. Agra 4:1-11. Opell, B. D.
1979. Revision of the genera and tropical American species of the spider family Uloboridae. Bull. Mus. comp. Zool. 148(10):443-549.
Peters, H.
1953. Beitrage zur vergleichenden Ethologie und Okologie tropischen Web- spinnen. Z. Morph. Okol. Tiere 42:278-306.
1955. Contribuciones sobre la etologia y ecologia comparada de las aranas tejedoras tropicales. Comm. Inst. Trop. Inv. Scient. 4:37-46.
64
Psyche
[Vol. 89
Robinson, M. H. and B. Robinson
1973. Ecology and behavior of the giant wood spider Nephila maculata (Fabricius) in New Guinea. Smithson. Contrib. Zool. 149:1-76.
Szlep, R.
1961. Developmental changes in web-spinning instinct of Uloboridae: con- struction of the primary-type web. Behaviour 27.60-70.
Wiehle, H.
1927. Beitrage zur Kenntnis des Radnetzbaues der Epeiriden, Tetragnathiden, und Uloboriden. Z. Morph. Okol. Tiere 9:468 537.
1931. Neue Beitrage zur Kenntnis des Fanggewebes der Spinnen aus den Familien Argiopidae, Uloboridae, und Theridiidae. Z. Morph. Okol. Tiere 22:348-400.
Workman, T.
1896. Malaysian Spiders, volume F Published by the author. Belfast.
POPULATION STRUCTURE AND SOCIAL ORGANIZATION IN THE PRIMITIVE ANT AMBLYOPONE PALLIPES (HYMENOPTERA: FORMICIDA E)
By James F. A. Traniello1 Harvard University,
Museum of Comparative Zoology Laboratories Cambridge, Massachusetts 02138, U.S.A.
I INTRODUCTION
The genus Amblyopone contains the most morphologically and behaviorally primitive species in the poneroid complex of ants, and a detailed examination of their social structure could significantly contribute to the reconstruction of social evolution in the Formi- cidae. But because of their cryptic habits and distribution, the biol- ogy of the majority of species of Amblyopone and the related genera Mystrium, Myopopone, Prionopella, and Onychomyrmex remains almost entirely unknown. Previous investigations have provided information on colony foundation (Haskins, 1928; Haskins and Enzmann, 1938; Haskins and Haskins, 1951), ecology, behavior, and taxonomy (Wheeler, 1900; Brown, 1960; Gotwald and Levieux, 1972; Baroni Urbani, 1978), and physiology (Whelden, 1958). Still, many of the details of social organization in Amblyopone are lack- ing. I present in this paper the results of a two-year study on the behavior and ecology of Amblyopone pallipes.
Material and Methods Study areas and nest collection
Thirty-one colonies of A . pallipes were collected under stones in a damp, white pine woodland in Westford, Massachusetts. A single colony was taken under the bark of a rotting log. Nests generally consisted of one or two shallow (6-10 mm) depressions in the soil immediately beneath the stone, from which a single gallery opened to subterranean chambers. Gentle excavation usually revealed one or two additional loosely structured chambers. Workers, queens,
•Present address: Department of Biology, Boston University, Boston,
Massachusetts 02215
Manuscript received by the editor February 18, 1982.
65
66
Psyche
[Vol. 89
sexuals, and brood were found at all levels of the nest and were quickly aspirated.
Distribution and natural history
A. pallipes has been found in the eastern United States and in the St. Lawrence Valley in Canada in cool, moist, forested areas (Brown, 1960). General references on the natural history of this species are given by Wheeler (1900) and Haskins (1928).
Laboratory arrangements
Colonies were housed in artificial nests composed of a thick, moist filter paper bottom with cotton sides approximately 6 mm high covered with a glass plate. The nests were placed in 15 X 22cm plastic boxes in which the humidity was kept high. The total nest area was roughly 10cm2. A second chamber, similar in structure but somewhat larger, was connected to the nest as a foraging arena, where live prey were offered. Colonies were fed on whole, live geo- philomorph and lithobiid centipedes; in addition, elatyrid, bupres- tid, and tenebrionid beetle larvae were acceptable to the ants. This method of culture proved successful and greatly facilitated studies of social interaction since the activity of an entire colony could be monitored on the stage of a dissecting microscope. Ethogram data were compiled in this manner, and were analyzed using the methods of Fagen and Goldman (1977).
Results and Discussion
1. Life cycle and population structure.
Nest distribution and colony size. The spatial distribution of col- onies at the principal study site in Westford is presented in Fig. 1. An interesting feature of this population, in addition to its clumped distribution pattern is that three colonies were collected under stones in 1978 precisely where colonies were found the year before. This suggests that the colonies that were collected represented sub- units of a large, subterranean population. Each unit is small (modal size class = 9-16 workers). Complete collection data are presented in Fig. 2. Although distributional data are not given, a population of seemingly comparable density was discovered by Wheeler (1900), who uncovered 30 nests in a three hour period. Also, the colony size data correspond closely to the data of Francoeur (1965, 1979, and personal communication).
1982]
Traniello — Amblyopone pallipes
67
Queen number. The frequency distribution of the number of queens in a colony is given in Fig. 3. Of 19 queenright colonies, 10 (52%) contained more than one dealate female. Observations of multiple queened colonies in the laboratory revealed that in at least some of these colonies each queen was functionally reproductive. However, many queens in apparently polygynous colonies did not lay eggs, and engaged primarily in worker tasks.
Life cycle, colony reproduction, and population structure. Be- cause colonies were collected and censused throughout the spring and summer of 1977 and 1978, it is possible to outline the life cycle of A. pallipes (Fig. 4). Eggs are laid in late April or early May and larvae hatch and develop throughout June and July. Mature larvae pupate in mid-July and early August, and adults eclose approxi- mately two to three weeks later. Although small numbers of eggs and larvae are present in most colonies throughout the spring and summer, it appears that only one brood matures per year. The large number of eggs found in colonies collected in August hatch before September and overwinter as larvae (Talbot, 1957). It is possible that the winter chilling results in the determination of these larvae as sexuals. In late August and early September workers and sexuals simultaneously eclose unassisted from their pupal cases. The adults which eclose at this time are predominantly workers. In four colo-
68
Psyche
[Vol. 89
15 -«
CO
LU
O
CD
CD
CD
10 -
t — i — i — i — r
1 2 9 8 16 32
NO, WORKERS PER COLONY
Fig. 2. — Frequency distribution of colony sizes for 35 nests.
nies collected in late August which reared brood in the laboratory, the ratio of <5:$: $ ? was as follows: 2:1:36; 0:5:13; 3:0:7; and 0:4:19. In all cases the worker population of a colony was at a maximum at this time. If this is considered in conjunction with the available information on nuptial flights in A. pallipes, then it is possible to speculate on colony reproduction and population structure.
1982]
Traniello — Amblyopone pallipes
69
NO. OF QUEENS PER COLONY
Fig. 3. — Frequency distribution of the number of dealate females in 19 queenright colonies.
Although the complete sequence of colony reproduction has not been observed, the studies of Haskins (1928, 1979) and Haskins and Enzmann (1938) provide some evidence of its organization. Early in September, winged females leave the nest and disperse over short distances, finally alighting on the ground or low vegetation. Then, with gaster arched and sting partially extruded, they “call” males with a chemical sexual attractant. Males quickly locate females, copulation ensues, and soon after insemination females shed their wings and re-enter the soil; perhaps they return to the parent nest.
70
Psyche
[Vol. 89
At this point in the life cycle, the worker/ queen ratio is highest, as described above, yet colonies collected in the late spring are much smaller in size (approximately 50%). Therefore, colony reproduc- tion by budding may occur if one or more fecundated queens depart with a portion of the worker force. This hypothesis has previously been considered by Wheeler (1900) and Brown (1960), and is sup- ported by my data on colony growth, nest distribution, and nest structure. An additional feature of the nest distribution pattern sup- ports the hypothesis of limited dispersal. The most dense population of colonies occurred on the south side of an early stone wall (< 1 m high), although nest sites were abundant on both the north and south sides, and soil, vegetational, and exposure parameters ap- peared to be identical. Also, laboratory observations indicate that alate females may shed their wings before mating occurs. On several occasions newly eclosed females left the nest, shed their wings, and returned to the nest. Because mating occurs on the ground, such behavior does not exclude the possibility that these individuals could eventually become inseminated. These females may then return to the parent nest or may be adopted by a nearby colony. In several laboratory experiments queens were introduced into other queenright nests or orphaned colonies. In all cases they were accepted by both workers and queens. Similarly, workers could be transferred from one colony to another without aggression. There- fore, populations of A. pallipes appear to be unicolonial and secon- darily polygynous. Ecologically, the patchy distribution of this ant correlates with this type of population structure.
2. Social organization
The social ethogram. Social ethogram data were gathered from five colonies which were observed for a total of 73 hours, during which 6,500 individual acts were recorded. The behavioral catalog of a single colony of A. pallipes (2 queens, 18 workers, brood) that was studied for 25.7 hours is given in Table I. The total number of acts observed was 42 (95% confidence interval for catalog size [27, 47]), and the sample coverage was 0.9992. Behaviors listed in the ethogram having a frequency of 0 were observed in other colonies and are included as part of the species repertory. The majority of activities are common to many ant species; those that are unusual will be discussed briefly. Antennal tipping is a behavior previously described in Zacryptocerus varians (Wilson, 1975) which occurred
WORKERS
1982]
Traniello — Amblyopone pallipes 71
CD
aooaa do inhd N3d
72
Psyche
[Vol. 89
Table I. — The social ethogram. N = number of acts observed in each caste.
|
Behavioral Act |
Workers (16) N=2525 |
Queens (2) N=158 |
|
1 . Self-groom |
0.3303 |
0.4114 |
|
2. Allogroom queen |
0.0044 |
0 |
|
3. Allogroom worker |
0.0384 |
0 |
|
Brood care: |
||
|
4. Lay egg |
0 |
0.0127 |
|
5. Carry egg or egg pile |
0.0123 |
0.0696 |
|
6. Lick egg |
0.0305 |
0.1013 |
|
7. Lick larva |
0.0950 |
0.1139 |
|
8. Carry, drag, or role larva |
0.0337 |
0.0633 |
|
9. Bank mature larva with soil |
0.0048 |
0 |
|
10. Carry pupa |
0.1200 |
0 |
|
1 1. Lick pupa |
0.0824 |
0.0127 |
|
12. Place larvae on prey |
0.0032 |
0 |
|
13. Assist removal of meconium |
0.0004 |
0 |
|
14. Assist larval molt |
0.0012 |
0 |
|
15. Lick ecdysial skin |
0.0063 |
0.0380 |
|
Aggressive display: |
||
|
16. Undirected |
0.0250 |
0 |
|
17. To worker |
0.0051 |
0.0127 |
|
18. To queen |
0.0004 |
0 |
|
Predatory behavior: |
||
|
19. Forage |
0.0158 |
0 |
|
20. Sting prey |
0.0040 |
0 |
|
21. Drag prey to nest |
0.0019 |
0 |
|
22. Drag prey within nest |
0.0048 |
0 |
|
23. Lick prey |
0.0578 |
0 |
|
24. Handle prey within nest |
0.0051 |
0 |
|
Nest maintenance and defense: |
||
|
25. Guard |
0.0083 |
0 |
|
26. Handle nest material |
0.0190 |
0 |
|
27. Repair nest wall |
0.0277 |
0 |
|
28. Lick nest material |
0.0012 |
0 |
|
29. Excavate nest |
0.0111 |
0 |
|
30. Bury noxious object |
0.0004 |
0 |
|
3 1 . Carry or drag dead worker |
0 |
0 |
|
32. Carry or drag live worker |
0.0004 |
0 |
|
33. Extrude sting |
0.008 |
0.0190 |
|
34. Remove empty pupal case |
0.0008 |
0 |
|
35. Jitter |
0.0055 |
0.0190 |
|
36. Jolt body |
0.0135 |
0.0633 |
|
37. Lick meconium |
0.0008 |
0 |
|
38. Tip antennae |
0.0008 |
0 |
|
39. Flick antennae |
0.0099 |
0.0127 |
1982]
Traniello — Amblyopone pallipes
73
|
Behavioral Act |
Workers (16) N=2525 |
Queens (2) N=158 |
|
40. Pinch larvae |
0 |
0.0063 |
|
41. Cannibalize larva |
0.0170 |
0.0380 |
|
42. Discharge subpharyngeal pellet |
0 |
0.0063 |
|
Totals: |
1.0 |
1.0 |
infrequently in A. pallipes. During this behavior the body is raised, the gaster is curved forward, and with the mandibles agape the antennae are held forward with their terminal funicular segments slightly inclined toward each other. The significance of antennal tipping is unknown, but it appeared to be part of a grooming sequence. Vibrational displays were given by workers if the nest wall was breached or if an individual was mechanically disturbed. If the stimulus was intense enough, other workers would show the same vigorous jittering behavior, consisting of rapid vertical movements of the head and thorax. This behavior had the effect of producing a general arousal within the colony and resulted in an increase in the number of workers appearing at the source of stimulation. In the case of nest damage, building behavior eventually occurred but did not immediately follow. This signal appears to be a primitive form of mechanical communication, in which alarm is propagated di- rectly through body contact. A similar vibratory display has been documented in A. australis (Holldobler, 1977).
Workers and queens of A. pallipes have retained a number of behaviors that appear to reflect their wasp ancestry. Queens were seen grasping larvae and squeezing them in the neck region with their mandibles, thus causing them to regurgitate a droplet of clear liquid which they then consumed. Workers were never observed to regurgitate with other workers, queens, or larvae, and all individuals fed directly on prey. Aggression was observed between workers and queens. An aggressive display typically consisted of opening the mandibles and rising up on the extended legs. This behavior was usually exhibited by queens in the area of the egg pile and seemed to produce avoidance in contacted workers. These observations raise the question of whether queens maintain their reproductive status through behavioral dominance or inhibitory pheromones.
Polyethism. Studies on the division of labor within the worker caste have revealed that temporal castes are absent in the species. A
74
Psyche
[Vol. 89
complete account of polyethism in relation to the life history of A. pallipes is given by Traniello (1978).
Predatory behavior. Prey were found in only three of the colonies collected. In two colonies larvae were found clustered around litho- biid centipedes (length = 1.5-2. Ocm), and in the third colony a carabid beetle larva was taken. In the laboratory, colonies were offered a variety of live arthropods that workers might encounter in leaf litter, soil, or rotting wood. Wood lice ( Oniscus ), house centi- pedes ( Scutigera ), and various millipedes were consistently rejected while small elatyrid, tenebrionid, and buprestid beetle larvae were carried to the nest and fed upon. The diet of A. pallipes appears to be restricted to live, linear-shaped arthropods that can be captured by workers. A related species, A. pluto, is entirely specialized on geophilomorph centipedes (Gotwald and Levieux, 1972). When large, robust-bodied centipedes ( Lithobius sp.) were offered to col- onies of A. pallipes, workers were unable to grasp the prey due to its escape movements and body diameter. It is difficult to imagine a condition under which large prey could be captured, even if they were “cornered” in a narrow gallery. When Lithobius of similar size were held with forceps, workers were still unable to subdue the centi- pede. Freshly killed centipedes were not accepted. It is therefore difficult to support the hypothesis of a nomadic life style for A. pallipes. Although this species of Amblyoponini does not appear to move its colonies to the location of large, previously captured prey, other species, such as Onychomyrmex do provide evidence linking group predation and nomadism in this primitive group of ants (Wilson, 1958).
Prey capture and retrieval is very stereotyped, and solitary hun- tresses stalk prey in a highly methodical manner. As prey are approached, workers advance cautiously, apparently orienting to odors or air microcurrents produced by the prey. When within strik- ing range (2-3 mm) the mandibles are opened and the head is oriented orthogonal to the long axis of the prey. Then in a single motion the mandibles close around the prey, the legs elevate the body, and the gaster is swung forward. The prey is then repeatedly stung and the venom soon shows its paralytic effects. Initially, only the area adjacent to the cuticle penetrated by the sting is immobi- lized, and stinging continues until escape movements stop. Subse- quently, the retrieval of the prey begins after a brief period of self-
1982]
Traniello — Amblyopone pallipes
75
grooming. The retrieval process varies in duration depending upon prey size, but even long (4. 0-5. 0cm, 2. 0-2. 5 mm in diameter) geo- philomorph centipedes are easily dragged to the nest. A number of orientation trips made between the prey and the nest generally pre- ceded retrieval. During these orientation runs, which were made throughout the retrieval process, workers continually checked their position relative to the nest. The prey was then dragged several centimeters; the worker then stopped, released the prey, and con- tinued homeward until she contacted the nest entrance. She then returned to the prey and repeated this sequence, alternating prey movement with orientation trips. Once the prey was in the nest, other workers approached and began vigorously licking the areas of the prey’s body opened during capture. Larvae were either carried to the prey or, if close enough, moved toward it and adjusted their position on its body on their own accord. At times workers assisted in positioning larvae. Additional details of feeding behavior are nearly identical to those described by Gotwald and Levieux (1972).
Communication during foraging. At times, two or three ants attempted to jointly carry prey, but cooperative efforts were hap- hazard and inefficient. But cooperative retrieval seems unnecessary due to the physical capabilities of individual ants. The critical ele- ment in prey capture is probably not retrieving, but subduing rela- tively large arthropods. Often after a worker began stinging a prey item, a second or third worker approached and assisted in para- lyzing the prey. The fact that workers were attracted to the point of prey capture suggested that additional ants may be recruited over short distances by orienting to prey odor, air currents, or some signal produced by the forager. To test the hypothesis that phero- mones are involved in this process I stimulated foragers to grasp and attempt to sting the tip of a pair of forceps and then lowered the worker, still attacking the forceps tip, in front of the nest entrance. The response of workers in the nest was dramatic. In five replicates, 5.8 ± 2.3 workers/0.5 min approached the nest entrance under the experimental conditions. Only 0.2 ± 0.1 workers/0.5 min were attracted to the nest entrance in controls (agitated forceps alone). This difference is statistically significant (.001 < p < .01; t = 6.1, Student’s t-test). Although the possibility that stridulatory signals might be involved could not be ruled out, the results of these experi- ments suggest that chemical cues are involved in the attraction
76
Psyche
[Vol. 89
response. Subsequently, crushes of the head, thorax, and gaster were offered on applicator stick tips at the nest entrance. Also, crushes of dissected poison and pygidial glands (Holldobler and Engel, 1979) were offered. Only head crushes produced attraction. Whelden’s (1958) studies, in addition to our own histological investi- gations, revealed a group of large glandular cells at the base of the mandible. The indirect evidence described above suggests that dur- ing prey capture the contents of these cells are released, attracting workers in the vicinity to assist in subduing prey.
3. Ecology and social evolution
The results of this study and previous investigations suggest that populations of A. pallipes are unicolonial. Workers from different subnests within a population show no aggression toward each other. Such worker compatibility has been demonstrated in Rhytidopon- era metallica (Haskins and Haskins, 1979), whose populations appear to be structurally similar to those of A. pallipes, but occupy larger area geographically. Workers taken from nests three miles apart were not mutually hostile. The lack of aggression was consist- ent within, but not between populations. Ambylopone pallipes col- onies appear to be similarly viscous, but do not occupy as extensive an area.
Observations in the laboratory are in accord with Brown’s (1960) position which states that after mating, females “always or usually return to the parent nest”. Secondary polygyny in this species, in addition to its patchy distribution, indicates that this species is in the terminology of Holldobler and Wilson (1977) a habitat specialist. The characteristic A. pallipes habitat is cool, damp, heavily shaded woodland. Nest site and prey abundance are also important fea- tures. Populations apparently grow slowly, and through reproduc- tion by budding, eventually saturate the habitat. Such a scheme does not rule out the occurrence of dispersal flights, which have been witnessed on occasion (Haskins, 1928). As colonies become more populous within a habitat, dispersal flights should occur more frequently in order to colonize additional areas. Once a founding queen locates a preferred habitat, colony reproduction again is accomplished through budding. The strategy may be similar to that of the mound building species Formica exsectoides. However, it must be noted that in laboratory situations, A. pallipes queens have never been observed to successfully found colonies (Haskins, per-
1982]
Traniello — Amblyopone pallipes
11
sonal communication). But it is difficult to determine whether this is an abnormality which occurs only in the laboratory or represents an inability of A. pallipes queens to found a colony alone. Newly inseminated queens of A. australis found colonies in the partially claustral mode (Haskins and Haskins, 1951). However, A. australis is monogynous.
Within a habitat, A. pallipes escapes competition with the more advanced groups of ants by additional specializations on micro- habitat and diet. This is in contrast to other unicolonial species which are broad generalists.
Behaviorally, A. pallipes exhibits both primitive and advanced social traits, and many of the primitive characters are more conserva- tive than those of Myrmecia. Age polyethism is lacking, and commu- nication between individuals is primarily mechanical, although a rudimentary short-range recruitment system that is mediated by pheremones exists. Among the primitive trophic characteristics is the use of the sting to paralyze prey, which are subsequently fed directly to the larvae without prior dismemberment. Employing the sting to paralyze prey appears to be widespread in the Ponerinae, and recently Maschwitz et al. (1979) have demonstrated that the venom of the oriental ponerine species Harpegnathus saltatus and Leptogenys chinensis indeed has paralytic, and not toxic, effects. Prey paralyzation also occurs in Daceton armigerum and Paltothy- reus tarsatus (Wilson, 1962; Holldobler, pers. comm.). This is con- trasted to myrmicine species which use the sting as a defensive weapon. The importance of paralyzing but not killing arthropod prey in Amblyopone pallipes is obviously related to the direct provi- sioning of larvae; prey must be kept from decomposing until they are consumed. Also, immobilization is necessary for successful retrieval, and energetically it is more efficient for solitary foragers to carry paralyzed prey. The absence of regurgitation which is charac- teristic of the Ponerinae, also is a primitive trait. Although one of the more distinctive features of A. pallipes and other Amblyoponini, prey specialization, appears to be a conservative formicid trait, it is also possible that specialization was a response to competition.
Finally, based on the theories of Malyshev (1968), Wilson (1971) has speculated that the Amblyoponini may have approached euso- ciality in a way very different from the partially claustral colony founding route assumed by Haskins and Haskins (1951). Because
78
Psyche
[Vol. 89
these ants appear to be specialized on large arthropods, they may have passed through a phase of subsociality similar to that of the bethylid wasp Scleroderma. Although the evolution of ants from Scleroderma- like ancestors has been ruled out on morphological grounds, the possibility remains that the Amblyoponini represent an independent venture into eusociality. The present study, which sug- gests that A. pallipes is not dependent upon large arthropod prey, and the studies of Haskins (1928) and Haskins and Haskins (1951) on colony foundation, do not support or refute this theory. Addi- tional studies must be carried out on the behavior of newly insemi- nated females, their prey preferences during colony foundation and their reproductive physiology to test this hypothesis.
Acknowledgements
This research was carried out while the author was a doctoral candidate at Harvard University, and was supported by the Ander- son and Richmond Funds, NSF Grant BNS 80-02613 (B. Holl- dobler, sponsor), and NSF predoctoral grant DEB 78-16201. Drs. Gary Alpert, Bert Holldobler, and Edward Wilson provided useful comments on the manuscript. I would especially like to thank Dr. Caryl Haskins for sharing with me his great wealth of knowledge of primitive ants. Finally, I thank Michelle and Eric Scott, who were indispensable in the field.
Summary
1. The behavior of ecology of the primitive ponerine ant Amblyo- pone pallipes was studied in the laboratory and the field. Thirty- three colonies were collected over a two-year period, 94% of which were excavated from one locality where 68% of the colonies were strongly clumped in their spatial distribution. Workers and queens could be transferred between these nests without hostility.
2. The inability of workers to recognize members of other colo- nies within a population, the colony life cycle, limited dispersal, the presence of multiple queens in nests, and circumstantial evidence on the adoption of newly inseminated females by their parent nest suggest that A. pallipes is secondarily polygynous and unicolonial. Although dispersal flights do occur, colony reproduction seems to be accomplished through budding.
1982]
Traniello — Amblyopone pallipes
79
3. Studies on the ethology of A. pallipes show that this species has retained many conservative behavioral traits. Among these are the absence of age polyethism and the provisioning of larvae with whole prey (chiefly chilopods and beetle larvae). Observations of preda- tory behavior do not support the hypothesis that colonies are nomadic. Prey are paralyzed by stinging and are then retrieved. Larvae feed directly on the body of the prey.
4. A primitive form of alarm communication, presumably trans- mitted through body contact, is mediated by a vibratory display. Workers show attraction to head crushes, and mandibular gland pheromones appear to be involved in a weak form of recruitment.
5. Because of the lack of precise information on the behavior of colony founding queens, the question of whether sociality in the Amblyoponini arose in a manner different from the partially claus- tral colony founding mode of Myrmecia remains an enigma.
References
Baroni Urbani C., 1978. — Contributo alia conoscenza del genere Amb/vopone
Erichson (Hymenoptera: Formicidae). Bull. Soc. Entomol. Suisse, 51, 39-51. Brown W. L., 1960. — Contributions toward a reclassification of the Formicidae.
III. Tribe Amblyoponini (Hymenoptera). Bull. Mus. Comp. Zool. Harvard, 122(4), 230 pp.
Fagen R. M., Goldman R. N., 1977. — Behavioral catalogue analysis methods.
Anim. Behav., 25, 261-274.
Francoeur A., 1965. — Ecologie des populations de fourmis dans un bois de
chenes rouges et d’erables rouges. Nat. Canadien, 92, 263-276.
Francoeur A., 1979. — Les fourmis du Quebec. A nn. Soc. Entomol. Quebec, 24,
12-47.
Gotwald W. H., Levieux J., 1972. — Taxonomy and biology of a new west
African ant belonging to the genus Amblyopone. Ann. Entomol. Soc. Amer., 65, 383-396.
Haskins C. P., 1928. — Notes on the behavior and habits of Stigmatomma pal-
lipes Haldeman. J. New York Entomol. Soc., 36, 179-184.
Haskins C. P., 1979. — Sexual calling behavior in highly primitive ants. Psyche,
85,407-116.
Haskins C. P., Enzmann E. V., 1938. — Studies of certain sociological and
physiological features in the Formicidae. Ann. New York Acad. Sci., 37, 97-162. 79. — Worker compatibilities within and
between populations of Rhvtidoponera metallica. Psyche 86, 301-312. Holldobler B. K., 1977. — Communication in social Hymenoptera. In Sebeok
T., ed.. How Animals Communicate. Indiana Univ. Press, Bloomington, Indiana, pp. 418-471.
Holldobler B. K., Engel H., 1979. — Tergal and sternal glands in ants. Psyche,
80
Psyche
[Vol. 89
85, 285-330.
Holldobler B. K., Wilson E. O., 1977. — The number of queens: an important
trait in ant evolution. Naturwissenschaften, 64, 8-15.
Malyshev S. I., 1968. — Genesis of the Hymenoptera and the phases of their
evolution (tr. from Russian by B. Haigh; Richards O. W., Uvarov B., eds.). Methuen and Co., London, viii +319 pp.
Maschwitz U., Hahn M., Schoenegge P., 1979. — Paralysis of prey in ponerine
ants. Naturwissenschaften, 66, 213.
Talbot M., 1957. — Populations of ants in a Missouri woodland. Ins. Soc., 4,
375-384.
Traniello J. F. A., 1978. — Caste in a primitive ant: absence of age polyethism
in Amblvopone. Science, 202, 770-772.
Wheeler W. M., 1900. — The habits of Ponera and Stigmatomma. Biol. Bull., 2,
43-69.
Wilson E. O., 1958. — The beginnings of nomadic and group-predatory behavior
in the ponerine ants. Evolution, 12, 24-31.
Wilson E. O., 1962. — Behavior of Daceton armigerum (Latreille), with a classifi-
cation of self-grooming movements in ants. Bull. Mus. Comp. Zool. Harvard, 127, 403-421.
Wilson E. O., 1971. — The Insect Societies. Belknap Press of Harvard Univ.
Press, Cambridge, Mass. 548 pp.
Wilson E. O., 1975. — A social ethogram of the Neotropical arboreal ant Zacrvp-
tocerus varians (Fr. Smith). Anim. Behav., 24, 354-363.
THE BIOLOGY OF NINE TERMITE SPECIES (ISOPTERA: TERMITIDAE)
FROM THE CERRADO OF CENTRAL BRAZIL
By Helen R. Coles de Negret1 and Kent H. Redford2 Introduction
The Neotropical region is second to the Ethiopian in numbers of described termite species (Araujo 1970). However, little is known of their biology. The literature on Brazilian termites is largely re- stricted to isolated taxonomic descriptions of species from the Amazon Basin and southern states of Brazil (Araujo 1961, 1969, 1977 and Fontes 1979). Exceptions to this include information re- lating termite species and their distribution to vegetation types in Mato Grosso State (Mathews 1977), the effect of deforestation on termites in the Amazon (Bandeira 1979) and data on the ecology and defense of termites in the cerrado vegetation of the Distrito Federal (Coles 1980).
The present study was done in conjunction with a study on mammalian termite predators, in particular the giant anteater, Myymecophaga tridaetyla (Coles 1980 and Redford in prep.). Six aspects of termite biology of importance in defense by termites against mammalian predators were studied for nine of the most common mound-building termite species in the Distrito Federal, Brazil. Reported here are individual weights, morphology of soldier castes, worker-soldier ratios, mound sizes and forms, mound hard- nesses and nest materials, distributions and abundances of nests and feeding habits for these nine species.
All species studied were from the family Termitidae (see Fig. 1 for comparison of soldier heads), subfamily Apicotermitinae, Grigioter- mes metoecus (Matthews); subfamily Nasutitermitinae, Armitermes
•Laboratoria de Zoologia e Ecologia Animal, Universidade de Brasilia, Brasilia D. F. 80910, Brazil.
2Museum of Comparative Zoology, Harvard University, Cambridge, MA 02138; and Department of Zoological Research, National Zoological Park, Smithsonian Institu- tion, Washington, D.C. 20008.
Manuscript received by the editor March 3, 1982.
81
82
Psyche
[Vol. 89
euamignathus (Silvestri), Cornitermes cumulans (Kollar), Cortariter- mes silvestri (Holmgren), Nasutitermes sp., Procornitermes araujoi (Emerson), Syntermes dirus (Burmeister), Velocitermes paucipilis (Mathews); subfamily Termitinae, Orthognathotermes gibberorum (Mathews).
Methods and Results
This study was conducted primarily in the Distrito Federal, Brazil (15 47'S 47 56'W) with supporting work done in Emas National Park, Goias State (18 19'S 52 45'W). Both areas are located within the cerrado sensu latu vegetation type. Cerrado (sensu latu ) is a semi-deciduous xeromorphic savanna vegetation found in the inter- mediate rainfall (750-2000 mm/ yr) area of Brazil. It is characterized by woody plants with thick bark and coreaceous leaves and a sea- sonal ground layer of grasses and herbs. Although geographically and floristically the cerrado vegetation zone is very uniform, physi- onomically it shows considerable variation (Eiten 1972). The types of cerrado sensu latu which were examined in this study are campo limpo (grassland), campo sujo (grassland with shrubs), cerrado sensu strictu (woodland) and cerradao (dense, tall cerrado). Within the cerrado zone, gallery forest vegetation is found on the wet, more fertile soils along river courses; however this was excluded from the present study as it supports a termite fauna which differs greatly from that of the other vegetation types (Coles 1980).
I. The Termites A. Comparative Morphology
Figure 1 depicts soldiers of the eight species of termites examined in this study, with a worker head of the soldierless species Grigio- termes provided for comparison, while Tables 1 and 2 provide information on the fresh weights and total body lengths. Table 2 also provides measurements of mandible length, nasus length, head length, head width and head depth for the soldiers (position of measurements depicted in Figure 2).
As can be seen from these data, the termite species in this study can be placed along a spectrum based on soldier and head shape. The two ends of this spectrum are ‘well-developed nasus/ vestigial mandibles’ (such as Nasutitermes) and ‘no nasus /verv well-devel-
1982]
Negret & Redford — Termite Species
83
Figure 1. Soldier heads of eight of the species of termites studied; Grigiotermes metoecus worker included for comparison: a, Grigiotermes metoecus; b, Armiter-
mes euamignathus ; c, Cornitermes cumulans; d, Cortaritermes silvestri; e, Pro- cornitermes araujoi; f, Nasutitermes sp.; g, Syntermes dir us; h, Velocitermes paucipilis; i. Orthognat hotermes gihberorum.
84
Psyche
[Vol. 89
loped mandibles’ ( Orthognathotermes ). Intermediate positions are occupied by forms with ‘slight nasus development /well-developed mandibles’ (such as Cornitermes ) and ‘well-developed nasus/ well- developed mandibles’ ( Armitermes ). Grigiotermes, with no soldier caste, cannot be placed on this spectrum.
These data also show that soldiers with very well- to well- developed mandibles and poorly developed nasi are both heavier and longer than soldiers with vestigial mandibles and well-developed nasi, Armitermes once again occupying an intermediate position.
Complete taxonomic descriptions for Grigiotermes metoecus, Armitermes euamignathus, Cortaritermes silvest ri, Velocitermes paucipilis, and Orthognathotermes gibberorum can be found in Mathews (1977). Procornitermes araujoi is fully described in Emer- son (1952). Samples of Cornitermes cumulans collected during the study in Brasilia were identified following Emerson (1952). Al- though the general head and mandible forms were consistent with the published description, head length and width measurements were much lower than those previously described for this species. However, Emerson indicated that there is considerable variation in mean measurements between colonies from different localities. The samples from Brasilia were compared with various other species in the Museu Zoologia de Universidade de Sao Paulo (MZSP). The most closely related species was C. villosus which was clearly differ- ent in that it had a greater number of setae and differently shaped mandibles. As a result of this divergence the best classification appears to be C. cumulans. Specimens from Brasilia have been deposited in the MZSP and the Museum of Comparative Zoology, Harvard University.
Samples of Nasutitermes sp. collected from the Distrito Federal were compared extensively with material in the MZSP but differed from all species examined. N. coxipoensis most resembled the Nasu- titermes we studied but differed in being smaller and in having a more oval shaped head. Further studies on these two forms are necessary to determine whether these differences are sufficient to warrant calling it a new species.
B. Weights
Fresh weights were measured on a Mettler balance. Fifty workers and fifty soldiers from each of three different nests were weighed, except for Syntermes for which only fifteen individuals of each caste
1982]
Negret & Redford — Termite Species
85
from the three nests were weighed and Nasutitermes for which five nests were sampled. The results are presented in Table 1 and are ordered from heaviest soldiers to lightest soldiers. Syntermes dims has workers and soldiers much heavier than the next heaviest spe- cies, Cornitermes. The termite species with soldiers possessing strong or long mandibles are heavier than those termites whose soldiers have vestigial mandibles, and well developed nasi. These latter soldiers are also lighter than their workers, a relationship reversed in the other termite species.
Table 1. Individual wet weights of termites (measurements expressed in micro- grams; mean with standard deviation in parentheses).
|
Species |
Workers |
Soldiers |
|
Syntermes dims |
42.75a |
117.3 |
|
(2.34) |
(11.1) |
|
|
Cornitermes cumulans |
9.30 |
19.83 |
|
(0.36) |
(1.07) |
|
|
Orthognathotermes gibberorum |
6.91 |
19.09b |
|
(0.75) |
(0.69) |
|
|
Procornitermes araujoi |
6.63 |
8.26 |
|
(0.76) |
(0.40) |
|
|
Grigiotermes metoecus |
6.27 (0.95) |
— |
|
Armitermes euamignathus |
3.48 |
4.19 |
|
(0.15) |
(0.52) |
|
|
Cortaritermes silvestri |
3.23 |
2.08 |
|
(0.12) |
(0.20) |
|
|
Nasutitermes sp. |
3.46c |
1.56 |
|
(1.06) |
(0.42) |
|
|
Velocitermes paucipilis |
2.52c |
1.31b |
|
(0.55) |
(0.09) |
a Equal number of all three morphs weighed, b Only major soldiers weighed, c Mixture of two worker types weighed.
86
Psyche
[Vol. 89
C. Morphology of Soldiers
The positions of measurements taken on soldier heads are indi- cated in Figure 2 (adapted from Coles 1980). Total body length was measured from tip of mandible or nasus, whichever extended further, to the end of the abdomen. The figures presented in Table 2 are the averages of 15 individual soldiers and are ordered from greatest to least mandible length. As can be seen, these five morpho- logical measurements are, on the whole, positively correlated with each other, with total body length and with weight (Table 1). The major exception is Orthognathotermes, which has mandibles and a nasus of a different shape than the other species.
D. Worker-Soldier Ratios
Worker-soldier ratios were calculated by counting all of the workers and soldiers in a piece of termite mound. The piece was rapidly removed from the surrounding mound so as to prevent a change in the normal worker-soldier ratio. For all species except P. araujoi, A. euamignathus, S. dims and C. silvestri, five pieces of mound from at least three different mounds were counted. The result obtained from a piece of mound was not used if the piece contained less than 600 individuals. Because of the large variation obtained in the first five counts for P. araujoi, an additional three pieces were counted. The fifth count used for A. euamignathus was an average of 45 samples and was taken from Domingos (1980). Only four counts were taken for C. silvestri.
The large diffuse mounds inhabited by S. dims and the rapid retreat of soldiers and workers made it impossible to obtain worker- soldier ratios from populations within the mound for this species. Instead, the value presented in Table 3 is an average of counts made on eleven foraging parties. The method used (Coles 1980) was to plug the exit at least one hour after foraging had begun. After spraying with pyrethrin aerosol insecticide all soldiers and workers were collected and counted. Table 3 presents the data on worker- soldier ratios ordered from greatest to least percent soldiers.
Those termite species with soldiers having chemical-based defen- sive systems have fewer workers per soldier than the other termite species. In fact, for these species, Velocitermes, Nasutitermes and Cortaritermes, there is little variation between species in this worker-soldier ratio. Similarly, Cornitermes and Procornitermes,
Figure 2. Positions of morphological measurements of soldier heads: lh= Lat- eral head length; ln = nasus length; lm = mandible length; Wh = maximum head width; dh = head depth including postmentum.
88
Psyche
[Vol. 89
Table 2. Morphological measurements of soldiers (measurements expressed in millimeters; mean with standard deviation in parenthesis).
|
Species |
Mandible Length |
Nasus Length |
Lateral Length of Head |
Maximum Head Width |
Head Depth |
Total Body Length |
|
Orthognathotermes |
2.96 |
0 |
3.06 |
2.09 |
1.83 |
9.25 |
|
gibberorum |
(0.11) |
— |
(0.08) |
(0.06) |
(0.05) |
(0.40) |
|
Svntermes |
2.45 |
0.16 |
5.20 |
5.15 |
3.17 |
15.57 |
|
dirus |
(0.11) |
(0.02) |
(0.19) |
(0.15) |
(0.14) |
(0.65) |
|
Cornitermes |
1.36 |
0.36 |
3.90 |
2.67 |
1.95 |
9.55 |
|
cumulans |
(0.78) |
(0.03) |
(0.11) |
(0.09) |
(0.07) |
(0.42) |
|
Proeornitermes |
1.14 |
0.45 |
2.46 |
1.98 |
1.57 |
7.47 |
|
araujoi |
(0.05) |
(0.03) |
(0.03) |
(0.04) |
(0.05) |
(0.21) |
|
Armitermes |
0.58 |
0.91 |
2.05 |
1.10 |
1.04 |
5.35 |
|
euamignathus |
(0.02) |
(0.05) |
(0.05) |
(0.04) |
(0.05) |
(0.20) |
|
Nasutitermes |
0.17 |
0.63 |
1.65 |
1.05 |
0.82 |
4.32 |
|
sp. |
(0.03) |
(0.02) |
(0.64) |
(0.35) |
(0.34) |
(0.14) |
|
Velocitermes |
0.15 |
0.80 |
1.65 |
1.05 |
0.82 |
4.32 |
|
paucipilis |
(0.18) |
(0.03) |
(0.64) |
(0.35) |
(0.34) |
(0.14) |
|
Cortaritermes |
0.15 |
0.61 |
1.64 |
1.08 |
0.80 |
3.95 |
|
silvestri |
(0.02) |
(0.03) |
(0.06) |
(0.06) |
(0.06) |
(0.25) |
Note: Grigiotermes is excluded for it has no soldiers.
two similar species have very similar workers-soldier ratios. Armi- termes occupies an intermediate position while Orthognathotermes has a large number of workers per soldier.
II. The Mounds
A. Mound size and form
Table 4 presents data on mean heights, widths and lengths of ten mounds for each of the nine species of termites. Figure 3 (a-r) con- sists of two photographs of each species mound, one of an entire mound and the other of a mound in transverse cross-section. As can be seen from the data and the photographs, the shapes of these mounds range roughly from an inverted cone ( Cornitermes ) to a low dome ( Orthognathotermes ).
1982]
N egret & Redford — Termite Species
89
Table 3. Proportion of workers in nests (mean with standard deviation in parentheses).
|
Species |
Worker- Soldier |
% Soldiers |
|
Velocitermes paucipilis |
4.00 |
25.80 |
|
(0.72) |
(4.23) |
|
|
Nasutitermes sp. |
4.06 |
25.50 |
|
(0.83) |
(5.56) |
|
|
Cortaritermes silvestri |
5.12 |
21.20 |
|
(1.64) |
(6.90) |
|
|
Svntermes dir us* |
9.66 |
11.10 |
|
(2.72) |
(3.02) |
|
|
Armitermes euamignathus |
13.82 |
7.68 |
|
(3.79) |
(2.57) |
|
|
Procornitermes araujoi |
30.12 |
5.10 |
|
(18.30) |
(3.76) |
|
|
Cornitermes cumulans |
30.23 |
3.48 |
|
(7.61) |
(3.14) |
|
|
Orthognathotermes gibberorum |
80.75 |
1.30 |
|
(18.18) |
(0.32) |
♦Figures derived from foraging parties. See text. Grigiotermes excluded as it has no soldiers.
The nature and form of individual mounds vary greatly and the characteristics listed below are generalized descriptions of mounds found in the Distrito Federal and Emas Park.
Cornitermes cumulans (Fig. 3 a,b): The mound has a very hard outer shell of soil surrounding a soft inner core of carton (fecal material, communited plant material add bits of soil) which often extends below ground as much as 40 cms. The galleries are large and unlined.
Nasutitermes sp. (Fig. 3 c,d): The mound is domed with the outer several centimeters softer than the inner core (as in arboreal Nasuti- termes and Constrictotermes) and often extends 25cms under- ground. The internal structure consists of thin-walled, convoluted.
90
Psyche
[Vol. 89
Table 4. Dimensions of the epigeal portion of termite mounds (measurements expressed in centimeters; mean with standard deviation in parentheses).
|
Species |
Height |
Length |
Width |
|
Cornitermes cumulans |
91.6 |
92.8 |
79.5 |
|
(16.7) |
(17.1) |
(14.5) |
|
|
Nasutitermes sp. |
78.1 |
100.1 |
85.9 |
|
(14.3) |
(18.2) |
(16.4) |
|
|
Syntermes dims |
51.7 |
173.0 |
150.7 |
|
(19.4) |
(26.5) |
(20.5) |
|
|
Velocitermes paucipilis |
31.2 |
27.3 |
22.6 |
|
(4.5) |
(7.0) |
(5.8) |
|
|
Grigiotermes metoecus |
2.96 |
60.2 |
47.2 |
|
(4.5) |
(7.9) |
(7.2) |
|
|
Procornitermes araujoi |
28.8 |
69.5 |
60.0 |
|
(12.0) |
(33.9) |
(34.4) |
|
|
Armitermes euamignathus |
26.7 |
59.5 |
52.8 |
|
(5.1) |
(8.8) |
(8.1) |
|
|
Cortartiermes silvestri |
15.8 |
24.8 |
20.5 |
|
(4.7) |
(3.2) |
(2.6) |
|
|
Orthognathotermes gibberorum |
15.0 |
35.9 |
40.4 |
|
(3.0) |
(11.3) |
(13.6) |
irregular galleries with a mottled black and soil-colored lining of fecal origin.
Syntermes dims (Fig. 3 e,f): This species builds low-domed termi- taria, the major parts of which are below ground level (often to depth of 1.5 m.). The galleries are large and diffuse, often containing grass stores and are lined with regurgitated soil in which individual pellets are clearly visible.
Velocitermes paucipilis (Fig. 4 g,h): The mounds are pyramidal, very soft, crumbly and are generally built around a grass tussock. They often extend several centimeters underground in a series of very diffuse galleries which are lined with a discontinuous layer of black material of fecal origin. Large amounts of cut plant material are found inside the mound.
1982] TV egret & Redford — Termite Species 91
Figure 3. Mounds of the termite species studied; external view and longitudinal section: a and b, Cornitermes cumulans; c and d, Nasutitermes sp.; e and f,
Syntermes dims.
92
Psyche
[Vol. 89
Grigiotermes metoecus (Fig. 4 i,j): These medium-sized domed mounds are often occupied by other species of termites and ants. The galleries are distinguished by smooth, shiny soil-colored floors and by small pieces of stone incorporated into the ‘ceilings.’ Indi- vidual deposits of fecal material used in construction are visible on the mound surface.
Procornitermes araujoi (Fig. 4 k,l): These medium-sized, rounded mounds are often characterized by a thin layer of loose soil covering the outer shell. These mounds are quite brittle and homogenous and have galleries with a mottled lining of black soil and colored parti- cles, probably of fecal origin. They rarely extend below ground.
Armitermes euamignathus (Fig. 5 m,n): This species builds very characteristic slightly domed mounds. The walls are very hard but the mound itself is only loosely held to the substratum with a cavity frequently occurring between it and the soil. The internal structure consists of large irregular chambers connected by very small galler- ies. During the alate flight season mounds of this species are charac- terized by earthen turrets several centimeters high built on the outer surface and serving as ‘launching platforms’ for alates.
Cortaritermes silvestri (Fig. 5 o,p): This species builds soft, low rounded mounds with large irregular galleries. The mounds are fre- quently built around grass tussocks and extend several centimeters underground as in Velocitermes.
Orthognathotermes gibberorum (Fig. 5 q,r): The low mounds built by this species are covered with loose soil and bound together by living grass stems. The galleries are regular and homogenous throughout. The mound frequently extends several centimeters underground but can be separated easily from surrounding soil when pried up.
B. Mound hardness and nest material
The ‘hardness’ of a mound was measured using a soil penetrome- ter which measures the force necessary to push a metal cone into the soil. The resistance to penetration is obtained by dividing the load of penetration (force applied) by the area at the base of the cone, which was 637.939 mm3. The resistance to penetration was taken as a measure of hardness of the mound surface.
A termite mound is not a solid structure but consists of a complex system of galleries and chambers. The outer wall is often thick enough for penetration of the whole cone. However, at times, the
1982]
Negret & Redford — Termite Species
93
Figure 4. Mounds of the termite species studied; external view and longitudinal section: g and h, Velocitermes paucipilis; i and j, Grigiotemies metoecus; k and
1, Procornitermes araujoi.
cone pushed into a gallery and a low reading was obtained. In order to obtain a representative figure for the whole mound ten measure- ments were taken, each from different positions, e.g. base, middle, top.
The hardness of any mound varies considerably throughout the year with the amount of rainfall. To reduce these variations all the
94
Psyche
[Vol. 89
Figure 5. Mounds of the termites species studied; external view and longitudinal section: m and n, Armitermes euamignathus; o and p, Cortaritermes silvestri; q
and r, Orthognathotermes gibberorum.
measurements were made in one month (April) at the end of the rainy season. Some variation in hardness occurs from day-to-day and so on any one day of recording, one mound from each of the eight species was examined. Ten mounds from each species were examined and ten measurements were made from each mound. Care was taken to select approximately the same size of mound for the ten mounds of any one species.
The mean values for the hardness of termite mounds in each species are shown in Table 5. As the range is large (15.24-0.11 Newtons/ mm3) the data were transformed (\f~x) and the differences
1982]
Negret & Redford — Termite Species
95
Table 5. “Hardness” of outer mound and materials used in mound construction (In column 1, any two means not followed by the same letter are significantly different at p = 0.05. In columns 3 through 6, ++ = usually used; + = occasionally used).
Resistance to
Penetration (Newtons mm3) Nest Construction Material
|
Species |
Termite Mound |
Soil at Base |
Soil |
Regurgitated Soil |
Fecal Material Saliva |
|
Velocitermes |
0.11a |
0.48 |
++ |
++ |
|
|
paucipilis |
(0.05) |
(0.16) |
|||
|
Nasutitermes |
0.25b |
0.42 |
++ |
++ ++ |
|
|
sp. |
(0.05) |
(0.15) |
|||
|
Cortaritermes |
0.25b |
0.44 |
++ |
++ |
|
|
silvestri |
(0.04) |
(0.18) |
|||
|
Procornitermes |
0.36b |
0.42 |
++ |
. ++ |
++ ++ |
|
araujoi |
(0.11) |
(0.14) |
|||
|
Orthognat hotermes |
0.48 |
— |
++ |
++ |
|
|
gibberorum * |
(0.15) |
— |
|||
|
Syntermes |
0.57c |
0.42 |
+ |
++ |
+ |
|
dims |
(0.13) |
(0.14) |
|||
|
Grigiotermes |
1.25d |
0.70 |
+ |
++ |
|
|
metoecus |
(0.17) |
(0.18) |
|||
|
Armitermes |
4.66e |
0.36 |
++ |
+ |
|
|
euamignathus |
(1.08) |
(0.10) |
|||
|
Cornitermes |
15.241 |
0.37 |
+ |
++ |
++ |
|
cum u Ians |
(5.36) |
(0.16) |
* Determined for only 4 mounds so no statistics performed.
between these means tested for significance using Hartley’s multiple range test. The ranking obtained from this analysis is shown in Table 5 with the mean values of the raw data. Velocitermes, Nasuti- termes, Cortavitermes and Procornitermes had the softest nests while Cornitermes had the hardest nest, 140 times harder than the softest, Velocitermes.
The composition of material used to build mounds was deter- mined by direct observation of workers. Observations were made on at least ten mounds per species, at different times of the day and year. The results are presented in Table 5. Four types of material
96
Psyche
[Vol. 89
were observed to have been used by termite workers in nest construc- tion: soil, regurgitated soil, fecal material and saliva. In some cases, such as Procornitermes nests, all four were used. Soil and/or re- gurgitated soil were always the most common forms of building material.
C. Distribution and Abundance of Nests
Information on the distribution and abundance of termite mounds in each vegetation type was collected from a variety of sources and the results are presented in Table 6. Different sampling methods can produce different results, depending on the spatial distribution of the termite mounds, the size of area sampled and the number of areas sampled. It is often difficult to interpret figures on termitaria densities because investigators do not report whether all termitaria examined contained the mound-building species. Thus, the specific methods used to obtain each of the densities reported in Table 6 are detailed below.
Method a: (Coles 1980); method b (Domingos 1980); method e (Coles de Negret et al. in prep.).
Blocks of 50 X 50 meters were selected randomly in each of the four vegetation types studied in the Distrito Federal. As some of the termite species in the present study were occasionally found in mounds built by other species, in these methodologies, all the epi- geal mounds in the area were completely excavated. The abundance of each species was thus expressed in numbers of nests per hectare. In order to exclude sites with only foraging termites, a “nest” was defined as a structure in which termite nymphs and larvae were present.
Method d: (Redford in prep.).
Twelve separate transects, each of 100 by 20 meters were marked out in the campo limpo vegetaton of Emas National Park, Goias. All the mounds built by Cornitermes cumulans in each transect were counted. The figure in Table 6 is the mean calculated from these twelve transects (standard deviation = 16.1).
Method e: (Brandao in prep.).
Two blocks, 100 by 100 meters were marked out in separate areas of campo sujo and two others, of the same size, in areas of cerrado vegetation in the Distritb Federal. All the Syntermes dims mounds present in each area were counted. As this species frequently con- structs small soil domes, apparently for storing food, nests were
1982]
Negret & Redford — Termite Species
97
Table 6. Distribution and densities of termite nests/mounds per hectare in four vegetation types (Letters correspond to different sampling methods — see text for details).
|
Species |
Campo Limpo |
Campo Sujo |
Cerrado Sensu Stricto |
Cerradao |
|
Grigiotermes |
40a |
28a |
24a |
48a |
|
metoecus |
4c |
|||
|
Armitermes |
84a |
1 12a |
1 16a |
124a |
|
euamignathus |
236b |
116b |
152b |
120b |
|
4 1 f |
156c |
|||
|
Cornitermes |
0a |
12a |
32a |
0a |
|
cumulans |
58d |
0c |
||
|
Cortaritermes |
40a |
12a |
4a |
0a |
|
silvestri |
||||
|
Nasutitermes |
48a |
32a |
0a |
0a |
|
sp. |
16c |
|||
|
Procornitermes |
4a |
12a |
52a |
4a |
|
araujoi |
12c |
|||
|
Syntermes dirus |
4a |
20a |
0a |
0a |
|
33e |
Oe |
|||
|
54e |
8e |
|||
|
Velocitermes |
40a |
96a |
32a |
0a |
|
paucipilis |
lOlf |
24c |
||
|
27g |
||||
|
Orthognat hotermes |
12a |
0a |
16a |
4a |
|
gihberorum |
again defined as structures in which termite nymphs and larvae were present.
Method f: (Curado et al. in prep.).
All the mounds built by Armitermes euamignathus and Ve/oci- termes paucipilis in an area of campo sujo ( 100 by 100 meters) in the Distrito Federal were sampled and counted.
Method g: (internal report. University of Brasilia).
Mounds of Velocitermes paucipilis present in a transect 230 by 10 meters extending from campo limpo to campo sujo in the Distrito Federal were counted.
98
Psyche
[Vol. 89
III. Feeding Habits and Foraging Behavior
Feeding habits were deduced from field observations, examina- tion of worker mandibles and gut contents, information in the liter- ature and in some cases, from laboratory food preference experiments. Results are summarized in Table 7. Details of foraging behavior, methods of investigation and food sources are given below.
Grigiotermes metoecus
Field observations and examinations of worker mandibles and gut contents indicate that this species is entirely geophagous. It excavates subterranean galleries in the soil surrounding its mound and is also frequently found in old, disused termite workings, pre- sumably rich in organic material.
A rmitermes euamignathus
In the cerrado and cerradao vegetations foraging workers can be found under the bark of living trees and sound, dead trees. How- ever, this species also occurs with equal frequency in campo limpo where few or no woody shrubs exist. Field observations on the foraging behavior of 100 colonies of this species show that in the absence of woody vegetation they can exploit the root systems of grasses (Domingos 1980). Laboratory food preference experiments carried out by the same author on five colonies of A. euamignathus indicates that when presented with a range of food sources, all colonies selected wood in preference to bark, litter and grass roots. Further field observations confirmed that this species selects dead, sound wood in preference to live and to dead, decomposed wood. The workers forage diurnally and reach the food source via subter- ranean galleries. On average, mounds are 0.4 and 0.3 meters from their food sources in cerradao and cerradao respectively and 1.2 and 1.0 meters in campo sujo and campo limpo, respectively (Domingos op. cit.).
Cornitermes cumulans
Field observations on foraging parties indicate that workers of this species feed on living and dead grasses and herbs, which they reach through subterranean tunnels, occasionally foraging under a fine layer of soil-sheeting. Small pieces of grass are cut from stand- ing grass tussocks and carried to the mound. Feeding in situ has been observed occasionally. Preliminary food preference experi-
1982]
Negret & Redford — Termite Species
99
|
Table 7. Modal feed consumed). |
ing habits (+ + = commonly consumed; + = |
occasionally |
|
SPECIES |
FOOD SOURCE |
|
|
Grass & |
||
|
Sound Decomposing |
Herbaceous |
|
|
Humus Wood Wood |
Litter |
|
|
Grigiotermes |
++ |
|
|
metoecus |
||
|
Armitermes |
++ |
_|_ |
|
euamignathus |
1 |
|
|
Cornitermes |
++ |
|
|
cum u Ians |
||
|
Cortaritermes si Ivest ri |
+(?) |
+ (?) |
|
Nasut iterates sp.n. |
+ ' ! + ' |
++ |
|
Procornitermes |
++ |
|
|
araujoi |
||
|
Svntermes dirus |
++ |
|
|
Velocitermes paucipilis |
-++ |
|
|
Orthognat hotermes gihherorum |
++(?) |
ments carried out on laboratory colonies showed that workers col- lect dead grass in greater amounts than live. When presented with only dead roots or dead grass blades, they fed more on the latter.
Cortaritermes si /vest ri
Field observations made in the Distrito Federal and information presented in Mathews ( 1977) indicate that this species feeds in grass tussocks among the roots and stems. It is not clear, however, whether it feeds on the organic residues in the soil or on the grass roots themselves.
Nasutitennes sp.
These termites have not been observed foraging in the open and rarely construct runways over the ground as do many other species in this genus. It is probable that they excavate underground tunnels to their food source, the exact nature of which is not known. Recent
100
Psyche
[Vol. 89
experiments on laboratory colonies have shown that this species can feed on a range of plant material including sound wood and both living and dead grass.
Procornitermes araujoi
Field observations have been made on above-ground foraging parties in the open and under soil sheeting. Workers cut and collect grass litter, generally at night, but occasionally on dull, humid days.
Svntermes dims
This species forages above ground in the open, at night, and crepuscularly. Workers and soldiers leave the tunnels from small exit holes which are plugged with several millimeters of soil during inactive periods. These foraging holes may be on the mound or at distances of up to 20 meters from it. The above-ground foraging parties consist of major workers and soldiers. At the end of a partic- ular trail the workers spread out over several centimeters and start cutting grass. Some climb up stands of vegetation and cut long pieces of grass which drop to the ground. Other workers cut these into smaller pieces and carry them to the nest. Consumption in situ has not been observed.
Ve/ocitermes paucipiiis
These termites feed on grass and surface litter which they collect at night in the open. The workers form trails to the food source where they spread out to cover a large area, cut small pieces of grass and leaves, and return with them to the nest. The workers are flanked at regular intervals by soldiers oriented with their raised heads pointing outwards.
Orthognathotermes gibber ovum
Examination of worker mandibles and gut contents together with information from Mathews (1977) suggests that this species feeds on organic residues in the soil. Observations of foraging behavior have not been made.
Food sources were divided into four categories: humus, sound wood, decomposing wood, and grass and herbaceous litter. The few termites eating sound wood and the many eating grass and herba- ceous litter probably reflect the fact that most of the vegetation types included in this study were open with few trees. Examination of the termite fauna within the gallery forests would reveal many
1982]
Negret & Redford — Termite Species
101
more wood-eating species. The predominance of grass-eating ter- mites is understandable because of the large biomass and rapid turnover of their food source.
Of the 54 species of termites in the cerrado vegetation of the Distrito Federal (excluding gallery forests) only nine mound- building species were examined in this study. Many of the other species do not build mounds and are found instead living within mounds built by one of these nine species. It is probable that many of these non-mound-building species will be found to be geophagous or humivorous, feeding in or near the mounds they inhabit.
Discussion
The cerado vegetation of the Distrito Federal, Brazil has a diverse termite fauna with at least 54 species present (excluding those found in gallery forest vegetation) (Coles 1980). Estimates of the termite density in savanna areas in other continents are much lower with only 19 species in the Sahel, Senegal, 19 in northern Guinea, Nige- ria, 23 in southern Guinea, Nigeria and 36 in savannas of the Ivory Coast (Wood and Sands 1978).
A survey by Coles (1980) indicated that most cerrado species were present in all the physionomic vegetation types; however, in terms of abundance, certain species were more common in one particular type of vegetation. This is clearly illustrated by the data in Table 6. Nests of Nasutitennes sp., Velocitermes paucipilis, Cortaritermes si/vestri, Syntermes dirus and Cornitermes cumulans were all more abundant in the open vegetation types (campo limpo and campo sujo). Grigiotermes metoecus and Armitermes euamignathus were equally common in all types while Procornitermes araujoi was more common in woodland areas. Orthognathotermes gibberorum had an irregular distribution being less common in the cerrado sensu strictu of the Distrito Federal but more common in the campo limpo of Emas Park. These preferences for particular vegetation types can, to some extent, be related to the feeding habits of each species (Table 7); however, abundance of a species is also influenced by other species present. In some areas conditions were particularly favorable for one species, an example of which was found in Emas National Park where populations of Cornitermes cumulans were exception- ally high, with other species much less common.
The variation in abundance of a species in different regions can be
102
Psyche
[Vol. 89
accompanied by variations in mound form and size. Howse (1979) gives several different examples of termite species which build very different mounds in different regions. Macrotennes subhvalinus in western Uganda builds mounds with very thick walls and no open- ings but on the Serengeti Plains, where the soil is volcanic ash, the mounds are low with many pit-like openings. In the semi-arid regions of eastern Africa they are different again, being steeple- shaped and constructed around a central chimney. Even though regional differences can exist, the characteristics of mounds investi- gated in this study showed a remarkable consistency throughout the cerrado region reinforcing observations by Emerson (1938).
In constructing a mound, galleries are excavated within the soil by the termites and particles are often transported from considera- ble depth and incorporated in the epigeal portion of the mound. This not only increases aeration of the soil but can also alter its chemical composition (Lee and Wood 1971). Soil used in building is reinforced with excreta and in some instances wood and other plant material.
Studies on the chemical composition of termite mounds in the cerrado have recently been started in Brasilia. Preliminary results indicate that both Ve/ocitermes and Armitermes mounds have much higher concentrations of calcium, phosphorus, potassium and alu- minum than the soil surrounding the mound (Curado et al. in prep.). However, an analysis of Table 5 shows that the materials used in mound building are not directly related to the hardness of the outer layer of the mound. Such factors as the way in which the material is deposited by the workers at the actual site of construc- tion as well as the size and arrangement of galleries and the thick- ness of walls also contribute to the overall hardness of the mound.
The mounds are constructed entirely by the worker caste. This caste takes little active role in the defense of the mound, a role performed by the soldier caste. The proportion of these two castes varies with the species and is apparently finely regulated by phero- mones produced by the queen and the soldiers (Luscher 1961). Haverty (1977), in a comprehensive work, summarized the data available on the relative proportion of workers and soldiers in 1 12 species of termites. Unfortunately, many of these data, gathered by different investigators, are not strictly comparable because of differ- ences in sampling techniques and types of groups sampled. The
1982]
N egret & Red ford — Termite Species
103
homogeneity in methodology used in calculating worker-soldier ratios in this study allows for precise comparison between species within the limits of accuracy of this method. The worker-soldier ratios were found to vary greatly between nests in some species (i.e., Procornitermes ) and remain quite constant in others (i.e., Velocitermes).
The behavior of nasute soldiers, which respond to a break in the nest by rapidly recruiting to the break, can greatly alter the worker- soldier ratio calculated. As an example of this, on one occasion the number of soldiers counted from a piece of Nasutitermes mound, which had been excised from the surrounding mound but left in place for 30 seconds, was almost half again the number of soldiers counted from a piece taken from the same mound but removed immediately following excision. Although comparison can be made between the nine species of termites it must be noted that these data were taken during one period of the year and present a static picture of the proportions of workers and soldiers in given nests. It seems probable that in the species examined, as in other species (Sands 1965), the worker-soldier ratio varies seasonally and possibly also with the age and size of the nest.
It is evident from the data that some species have proportionally many more soldiers than other species. Even though the proportion of soldiers in a colony varies, in all cases (when there is a soldier caste) the soldier caste is largely responsible for the defense of the colony and has morphological features which allow it to do this. The type of defense used by soldier termites tends to be based on chemicals, mechanical defense or a combination of both. The sol- dier type using a chemical-based defense has vestigial mandibles (Table 2), is lighter than its workers (Table 1), and produces poten- tially toxic and repellent secretions which are ejected from the tip of a long tube or nasus at the front of the head (Nutting et al. 1974, Eisner et al. 1976; Howse 1975; Prestwich 1979). Of the termites studied in this work, Velocitermes, Nasutitermes and Cortaritermes fall into this category. The soldier type using a mechanical-based defense rarely produces defensive secretions and has a large head, and strong, sharp mandibles. Orthognathotermes is the only species within those here studied that has no development of the nasus, relying solely on its mandibles for defense. Syntermes, Cornitermes and Procornitermes all have strong mandibles which can pierce human skin, drawing blood, together with a greatly reduced level of
104
Psyche
[Vol. 89
chemical defense (see ‘nasus length’ Table 2 as one indicator of the extent to which chemicals are used in defense). Armitermes stands in an intermediate position between the principally chemical and the principally mandibulate type soldiers, with a long nasus and mandi- bles which can pierce human skin but not draw blood. Grigiotermes is very interesting in that it has no soldiers; the workers however produce a large drop of liquid on either side of the abdomen when disturbed, which may serve a defensive purpose.
Termites are probably the dominant form of animal life in many areas of central Brazil, both in number of species and biomass. They play major roles in herbivory, decomposition, soil formation and alteration, and as an important source of food for other animals. Ants are probably the major predators of termites, but in central Brazil mammals are common and important predators as well. The aspects of termite biology reported in this study are all important in defense by termites against mammalian predators. The small size of termites, the type of soldier defense and the proportion of soldiers to workers are all factors influencing feeding by mammals once the termite mound has been opened. The shape, size and hardness of a mound influence the ways in which a mammalian predator can break into a nest while the distribution and abundance of nests are a measure of the spatial availability of termites as a food source. Lastly, the feeding habits of termites are important in determining when, and if, termites are available outside of the mound. Food preference tests with large and small mammalian predators and observation of wild giant anteaters (Redford in prep.) have shown that all of these aspects of termite biology interact in determining which species of termites are preferred as food and how available they actually are to mammalian predators.
Acknowledgements
Helen Coles de Negret would like to thank the Trustees of the Royal Society Leverhulme Scholarships and the Science Research Council-Shell Research CASE award for financing this research. The data form part of a Ph.D. thesis submitted to Southampton University in 1980 under the supervision of Dr. P. E. Howse.
Kent Redford would like to thank the National Geographic Society, the Museum of Comparative Zoology, the Organization of American States and Sigma XI for help in financing this research.
1982]
Negret & Redford — Termite Species
105
Special thanks to the members of the Order of Saint Benedict and the Laboratory of Ecology, University of Brasilia. Both authors thank Barbara L. Thorne, Alan E. Mill, James F. A. Traniello and Bert Holldobler for reading and criticizing the manuscript.
Literature Cited
Araujo, R. L.
1961. New genus and species of Brazilian termite. Revta. Bras. Biol. 21, 105-111.
1969. Notes on Dentispicotermes with description of a new species. (Isoptera, Termitinae). Revta. Bras. Biol. 29, 249-254.
1970. Termites of the Neotropical Region. In: Biology of Termites, Vol. II, (Ed. by K. Krishna and F. M. Weesner) pp. 527-571, Academic Press, N. Y.
1977. Catalogo dos Isoptera do Novo Mundo. Academia Brasileira de Cien- cias. Rio de Janeiro, RJ.
Bandira, A. G.
1979. Ecologia de cupins (Insecta: Isoptera) da Amazonia central: efeitos do desmatamento sobre as populacoes. Acta amazonica 9, 481-499.
Brandao, D. in prep.
Ecologia de duas especies simpatricas de Svntermes (Isoptera; Nasu- titermitinae) no Distrito Federal do Brasil.
Coles, H. R.
1980. Defensive strategies in the ecology of Neotropical termites. Ph.D. thesis Southampton University. 243 pp.
Coles de Negret, H. R., Domingos, D. J. and Fontes, E. G. in prep.
Spatial distribution of termite mounds in the cerrado vegetation, Dis- trito Federal, Brazil.
Curado, W., Coles de Negret, H. R., Haridasan, M. in prep.
Composition of the nest material of two termite species and the soil of their bases.
Domingos, D. J.
1980. Biologia, densidade e distribuigao espacial de duas especies de Armi- termes (Termitidae) em cinco formagoes vegetais do cerrado. M.Sc. thesis Universidade de Brasilia. 22 pp.
Eisner, T., Kriston, I. and Aneshansley, D. J.
1976. Defensive behaviour of a termite Nasutitermes exitiosus. Behav. Ecol. Sociobiol. 1, 83-125.
Eiten, G.
1972. The cerrado vegetation of Brazil. Bot. Rev. 38, 201-341.
Emerson, A. E.
1938. Termite nests. A study of the phytogeny of behaviour. Ecol. Mono- graphs. 8, 247-284.
1952. The Neotropical genera Procornitermes and Cornitermes (Isoptera, Termitidae). Bull. Am. Mus. Nat. Hist. 99, 429-471.
106
Psyche
[Vol. 89
Fontes, L. R.
1979. Atlantitermes novo genero de cupim, com duas novas especies do Brasil. (Isoptera, Termitidae, Nasutitermitinae) Rev. Bras. Ent. 23, 219-227.
Haverty, M. I.
1977. The proportion of soldiers in termite colonies: a list and a bibliography. Sociobiology 2, 199-216.
Howse, P. E.
1975. Chemical defenses of ants, termites and other insects: some outstanding questions. Proc. 1USS1. (Dijon), 23 29.
1979. The uniqueness of insect societies: aspects of defense and integration. In: Biology and Systematics of Colonial Organisms (Ed. by G. Larwood and B. R. Rosen), pp. 345-374. Academic Press, New York.
Lee, K. E. and Wood, T. G.
1971. Termites and Soils. Academic Press, New York.
Luscher, M.
1961. Social control of polymorphism in termites. In: Insect Polymorphism (Ed. by J. S. Kennedy), pp. 57-67. Roy. Entomol. Soc., London.
Mathews, A. G. A.
1977. Studies on termites from the Mato Grosso State, Brazil. Academia Bra- sileira de Ciencias, Rio de Janeiro, RJ. 267 pp.
Nutting, W. L., Blum, M. A. and Fales, H. M.
1974. Behavior of the North American termite Tenuirostritermes tenuirostris with special reference to the soldier frontal gland secretion, its chemical composition and use in defense. Psyche, 81, 167-177.
Prestwich, G. D.
1979. Chemical defense by termite soldiers. J. Chem. Ecol. 5, 459-480.
Sands, W. A.
1965. Mound population movements and fluctuations in Trinervitermes ebenerianus Sjostedt (Isoptera, Termitidae, Nasutermitinae). Insect. Soc. 12, 49-58.
Wood, T. G. and Sands, W. A.
1978. The role of termites in ecosystems. In: Production biology of ants and termites (Ed. by M. V. Brian), pp. 245-292. Cambridge University Press.
THE LIFE HISTORY OF THE JAPANESE CARRION BEETLE PTOMASCOPUS MORIO AND THE ORIGINS OF
PARENTAL CARE IN NICROPHORUS (COLEOPTERA, SILPHIDAE, NICROPHORINI).*
By Stewart B. Peck
Department of Biology, Carleton University,
Ottawa, Ontario, K1S 5B6, Canada
Introduction
The subject of the origin and evolution of sociality in insects has a rapidly growing literature. Most of this pertains to the Hymen- optera. Within the Coleoptera, presocial or subsocial parental care and division of labor are known in at least nine families (Wilson, 1971). The most advanced form of parental care known in beetles is that of the Nicrophorus carrion or burying beetles (tribe Nicro- phorini). This generalization is based on the study of six European species by Pukowski (1933, 1934) which has since been abstracted and popularized by many (e.g., Balduf, 1935; Milne and Milne, 1944, 1976; Wilson, 1971, 1975). Briefly, a male and female form a conspecific pair at a carcass of a mouse or other small vertebrate. They work cooperatively to exclude competitors, to bury the carcass, and to shape it into a ball in a crypt. The male leaves after oviposition but the female tends the developing larvae, calling them to the carrion by stridulation, and repeatedly feeds them by regurgitation. Such behaviors do not exist in the other tribe of silphid carrion beetles, the Silphini.
The only work on the life cycle of a North American Nicrophorus is a short note by Leech (1934) on N. defodiens (under the name N. conversator). Thus, it is not really known how general or wide- spread is the phenomenon of parental care in the genus, nor if all species are equally advanced behaviorally. There are about 20 species in the New World, and at least 65 species in all the world, in several lineages within the genus.
As part of a series of studies on the comparative biology and evolution of silphid beetles, I undertook a study of the life history of Ptomascopus morio Kraatz of Japan, to learn something of the
* Manuscript received by the editor October 29, 1981.
107
108
Psyche
[Vol. 89
origin of parental care in Nicrophorus. Ptomascopus is the only other genus in the tribe Nicrophorini and contains only two Asian species, P. morio being more common and widespread than P. plagiatus Menetries (Hlisnikowski, 1942). It is illustrated in many general Japanese insect books such as Esaki et al. (1932, 1956), Nakane et al. (1963), and Nakane (1980). The larvae are illustrated by K. Kurosa in Kawada (1959).
The genus shares with Nicrophorus many derived morphological characters relative to the Silphini: adults with stridulatory files, reduced second antennal segment, fused gular sutures, sexually dimorphic membranous anticlypeus; larvae with abdominal para- notal projections and cuticular sclerotization reduced, and with only one pair of ocelli.
The main morphological characters in which Ptomascopus is more primitive than Nicrophorus are in its possession of a normally clavate antennal club, rather than with a strongly capitate club formed from the last four segments, and in its less fossorial tibiae.
Methods and Materials
Four pairs of P. morio were collected in August, 1980, at carrion baits in a warm-temperate mixed mesophytic forest in the Omogo Valley of Mount Ischizuchi Quasi-National Park, Shikoku, Japan. They were brought to Ottawa, Canada, and placed in culture at 18° C, with a normal daylight regime, from September to December. The pairs were kept in separate seven cm deep boxes of clear plastic, floored with five cm of coarse damp sand. Two cm cubes of chicken neck were given as carrion food at required intervals. Observations were made daily. The data gained are variable in quantity and quality and are usually not abundant enough for tests of signifi- cance. Only simple means, sample sizes, and ranges are reported, but these are sufficient for comparative purposes.
Results
Both sexes dug irregular tunnels in the sand but not in direct association with the carrion. Most of their time was spent in these tunnels. They fed at the carrion and sporadically dug under it, but there was no direct indication of digging with the intention of burying the food, or of manipulating the food into a food ball, or of forming a crypt for it. Mating was observed occasionally but no indication of a courtship ritual was noted.
1982]
Peck — Life History of Ptomaseopus morio
109
Eggs were laid singly in the sand several cm to the side of the carrion. A mean of 13 eggs (N = 9, r = 9-16) were laid per female in 6 days (N = 9, r = 5-8), and a new clutch was started after a refractory period of 6 more days (N = 8, r = 5-8). The eggs hatched in 5 days (N = 30, r = 4-7). Frequent adult attempts to fly and leave the culture containers after the egg clutch was laid may indicate that post-mating (for the male) or post-oviposition dispersal is normal, and that the adults are normally not present with their young.
The larvae fed together under and directly on the carrion. There was no indication of parental attendance to, or feeding of, the larvae. The adults and larvae may feed on fly larvae or other insects associated with carrion in nature, but carrion alone is adequate for complete development of larvae in culture. There were 3 larval instars; the first lasted 1 day (N = 30, r = 1-2), the second 2 days (N = 30, r = 2-3). The third instar larvae fed for 7 days (N = 30, r = 6-9) before crawling away from the carrion and burrowing into the sand to form pupal cells. In total, over 300 larvae were pro- duced, of which about 50 were preserved for morphological study.
Prepupae had a high mortality due to a fungal contamination. The prepupal phase seems to be about 30 days in duration (N = 7, r = 28-40). The pupal phase also seems to last about another 30 days before emergence of the adult (N = 2, r = 25-35). At culture temperatures the parental generation adults died by early Decem- ber, for a longevity of at least four months. This could be con- siderably different in the field depending on their sensitivity to cool fall temperatures and whether or not they overwinter as adults.
Discussion
There was no indication of any subsocial or other behavioral association between the larvae and the adults as known in Nicro- phorus. The brood size, reduced fecundity, and shorter larval developmental times are similar to those reported in Nicrophorus , but otherwise the life cycle characteristics are generally similar to those reported for the carrion-feeding Silphini (Balduff, 1935; Brewer and Bacon, 1975; Cole, 1942; Cooley, 1917; and Ratcliffe, 1972). It should be noted that some Silphines appear to have derived feeding characteristics, being strict predators and phytophages. How this may have changed behavior and life cycle characteristics is not known.
110
Psyche
[Vol. 89
The results were verified by Dr. Kazuyoshi Kurosa of Tokyo (pers. comm.) who reared the beetle some 30 years ago in Oita Prefecture, Japan, but did not publish the results. He found no parental care, no sign of burying the food, and no parental attendance on the larvae, which grew well on fresh beef. Still, further observations with a natural forest soil substrate and natural food items like mouse or shrew carcasses would be desirable. How the beetles survive and “partition resources” in the face of what seemed to me to be severe competition from the diverse fauna of Japanese carrion beetles remains unknown.
Conclusions
It appears that the origin of parental care of larvae did not occur in an ancestor common to Ptomascopus and Nicrophorus, but seemingly in Nicrophorus itself, after the differentiation of the genus. If the origin was sometime after that of the genus itself we may expect a wider range of parental care and related behaviors in Nicrophorus than is generally assumed in the recent literature on these beetles. A greater number of Nicrophorus species should be studied to investigate the questions of the origin and evolution of sub-sociality within the genus, and the results should be evaluated with reference to a cladistic (phylogenetic) analysis of the evolution of morphological characters.
Acknowledgments
I thank Dr. Shun-Ichi Ueno of Tokyo and Dr. Kazuo Ishikawa of Matsuyama for making my Japanese field work possible and exceptionally informative. Field support was from operating grants of the Canadian Natural Sciences and Engineering Research Coun- cil. The manuscript was read and helped by comments from R.S. Anderson, A.F. Newton, K. Kurosa, R.B. Madge, and D.S. Wilson.
Literature Cited
Balduf, W. V.
1935. The bionomics of entomophagous Coleoptera. J. S. Swift Co., St. Louis. 220 pp. Reprinted in 1969 by E. W. Classey, Hampton, England. Brewer, J. W. and T. R. Bacon
1975. Biology of the carrion beetle Silpha ramosa Say. Ann Entomol Soc Am 68: 786-790.
1982]
Peck — Life History of Ptomaseopus morio
111
Cole, A. C., Jr.
1942. Observations of three species of Silpha (Coleoptera: Silphidae). Am Midi Nat 28: 161-163.
Cooley, R. A.
1917. The spinach carrion beetle. J Econ Entomol 10: 94-102.
Esaki, T., H. Hori, S. Hozawa.
1932. Iconographia Insectorum Japonicorum. Hokuryukan, Tokyo. 4404 pp.
Esaki, T., T. Ishii, T. Kawamura.
1956. Iconographic Insectorum Japonicorum. Editio Secunda, Reformata. Hokuryukan, Ltd., Tokyo. 1737 + 203 pp.
Hlisnikowski, J.
1942. Coleopterologische Notizen. Mitteil Miinchner Entomol Gesells 32: 578-579.
Kawada, A.
1959. Illustrated Insect Larvae of Japan. Hokuryukan Co., Ltd., Tokyo. 712 pp + indexes.
Leech, H. B.
1934. The family history of Nicrophorus conversator Walker. Proc British Columbia Entomol Soc 1934: 36-40.
Milne, L. J. and M. J. Milne
1944. Notes on the behavior of burying beetles ( Nicrophorus spp.). J New York Entomol Soc 52: 311-327.
Milne, L. J. and M. J. Milne
1976. The social behavior of burying beetles. Scientific American, 235: 84-89.
Nakane, T., K. Ohbayshi, S. Nomura, and Y. Kurosawa
1963. Iconographic Insectorum Japonicorum, Colore naturali edita, Volumen II (Coleoptera). Hokuryukan, Tokyo. 443 pp.
Nakane, T.
1980. Coloured illustrations of the insects of Japan, vol. I, Coleoptera. Enlarged and revised, edited by the Japan Coleopterological Society. Hoikusha Pub., Osaka. 275 pp.
Pukowski, E.
1933. Okologische Untersuchungen an Necrophorus F. Zeit Okol Morph Tiere 27: 518-586.
Pukowski, E.
1934. Die Brutpflege des Totengrabers. Entomol Blatter 30: 109 113.
Ratcliffe, B. C.
1972. The natural history of Necrodes surinamensis (Fabr.) (Coleoptera: Silphidae). Trans Am Entomol Soc 98: 359-410.
Wilson, E. O.
1971. The Insect Societies. Belknap Press, Harvard University Press, Cam- bridge, Mass. 548 pp.
Wilson, E. O.
1975. Sociobiology, the new synthesis. Belknap Press, Harvard University Press, Cambridge, Mass. 697 pp.
TERGAL AND STERNAL GLANDS IN MALE ANTS*
By Bert HOlldobler and Hiltrud Engel-Siegel
Department of Organismic and Evolutionary Biology, MCZ-Laboratories, Harvard University, Cambridge, Massachusetts.
Introduction:
Several recent morphological investigations have uncovered a variety of hitherto unknown or neglected exocrine glandular struc- tures in ant workers (Holldobler and Haskins 1977; Holldobler and Engel 1978; Kugler 1978; Jessen et al 1979; Holldobler et al 1982; Holldobler 1982; Jessen and Maschwitz in press). The behavioral functions of several of these glands have already been determined (For review see Holldobler 1982).
These studies dealt almost exclusively with ant females and except for the results of Janet’s (1902) classical histological investigations of the internal anatomy of males of Myrmica rubra, nothing is known about exocrine glandular structures in the gaster of ant males. Since we consider this information important not only for a further analysis of the behavior of ant males, but especially for our understanding of the evolution of pheromone glands and chemical communcation in ants, we have undertaken a histological study of exocrine glandular structures in ant males. In this paper we present a survey of the abdominal glands not directly associated with the gonads. The purpose of this paper is not to give detailed descriptions of each gland found, but rather to present a comparative account of abdominal glands detected in representative species in the different subfamilies.
Materials and Methods:
For histological investigations live specimens were fixed in alco- holic Bouin or Carnoy (Romeis 1948), embedded in methyl methac- rylate, and sectioned 8 /x thick with a D-profile steel knife on a Jung Tetrander I microtome (Rathmayer 1962). The staining was Azan (Heidenhain). Especially small objects were embedded in a water soluble plastic (JB-4 embedding kit. Polysciences, Inc., Pennsyl-
* Manuscript received by the editor May 1, 1982
113
114
Psyche
[Vol. 89
vania) and sectioned 4-6^u thick with glass knives on a rotary micro- tome. In this case the staining was Hematoxylin-Eosin (triple strength). The SEM pictures were taken with an AMR 1000 A Scanning Electron Microscope. In a few cases only specimens were available which had been preserved in 70% ethanol.
Results:
The major results are summarized in table I. In the following we will discuss some of the details of our findings.
Penis and subgenital plate glands:
Janet (1902) described in males of the myrmicine species Myrmica rubra two major glandular structures directly associated with the copulatory apparatus. ( 1 ) The first comprise the penis glands, paired clusters of glandular cells located inside the penis valves (Fig. 1). Each cell sends a duct through a membrane into the lumen formed by the valves (sperm gutters). This gland was also detected in males of Formica rufa (Clausen 1938) in Conomyrma brunnei and Fore- lius sp. (Marcus 1953; cit. in Forbes 1954), in Camponotus pennsyl- vanicus (Forbes 1954), in Neivamyrmex harrisi (Forbes & Do-Van- Quy 1965) and we found it in representative species of all major subfamilies of ants. The size of the paired penis gland clusters (which are also called aedeagal gland, Forbes 1954) varies greatly among different species. In some it is a major gland (Fig. 1). In others it is represented only by a few glandular cells, and sometimes we were unable to identify the opening of the glandular ducts. (2) The other major gland, associated with the copulatory apparatus is located in the 9th sternite, which together with the coxopodites comprise the subgenital plate (Weber 1954). We therefore named these paired clusters of glandular cells “subgenital plate gland”. Each glandular cell sends a duct through the intersegnental mem- brane into the ventral part of the genital chamber (Fig. 1,2). The subgenital plate gland was found in representative species of all subfamilies studied.
Tergal glands:
In his study of the workers and males of Myrmica rubra, Janet (1898, 1902) discovered a pair of clusters of a few glandular cells under the 6th abdominal tergite. Each cell is drained by a duct that penetrates the intersegmental membrane between the 6th and 7th
19821 Holldobler & Engel-Siegel — Glands in Male Ants 115
A
Fig. 1 A. Schematic drawing of a longitudinal section through the gaster of a Novomessor B. Longitudinal section through 6th, 7th, 8th and 9th abdominal segments of a Novomessor albisetosus 51. A=anus; P=part of penis with penis gland; PG=pygidial gland; PPG=post-pygidial gland; SPG=subgenital plate gland.
116
Psyche
[Vol. 89
Fig. 2 A. Longitudinal section through pygidial gland of Novomessor a/bisetosus (5- B. Longitudinal section through subgenital plate gland of N. albisetosus ft. CS= cuticular structure; GC=glandular cells; DO=openings of glandular ducts.
1982] Holldobler & Engel- Siegel — Glands in Male Ants 1 17
abdominal tergites. In recent investigations this gland was found in workers of representative species belonging to all subfamilies, except in the Formicinae. Although the structure and size of the gland varies greatly, its wide distribution led us to conjecture that this gland might be a primitive monophyletic trait in ants generally, perhaps reaching back to the typhioid (or mutilloid) wasp ancestors of ants. In fact, we have recently found first indications that this gland is also present in some living typhiid wasps.
Since this gland is anatomically closely associated with the last exposed tergite in female ants (7th abdominal tergite = pygidium) Kugler (1978) suggested that it be called the pvgidial gland. Of the several tergal glands recently discovered, the pygidial gland appears to be the most frequent in occurrence. Moreover, in several species its secretions have been found to serve as pheromones (Holldobler et al 1976; Holldobler and Haskins 1977; Maschwitz and Schonegge 1977; Kugler 1979; Holldobler and Traniello 1980 a,b; Traniello and Jayasuriya 1981). The pygidial gland seems to be homologous with the “anal glands” of the dolichoderine ants described by Pavan and Ronchetti (1955). As we pointed out previously (Holldobler and Engel 1978) the term “anal gland” is misleading, because the gland does not exit from the anal or cloacal opening of the gaster, but between the 6th and 7th abdominal tergites. We therefore suggested to refer the dolichoderine structure to the pygidial gland. Recently Jessen and Maschwitz (in press) proposed to name the pygidial gland in honor of its discoverer Charles Janet. Thus we have now three names for this tergal gland: anal gland, pygidial gland and Janet’s gland.
Because the anatomical designation of the organ in ant workers (a criterion we prefer) has been used in several recent publications, we will continue to call the tergal gland opening between the 6th and 7th abdominal tergites pygidial gland.
Table 1. (Following pages) List of species that were investigated histologically, and of the types of tergal and sternal glands found. When the histological series was incomplete and we could not make a definite statement, or when we could not clearly identify glandular ducts, the column is marked with a “?”. r=with reservoir; c=with cuticular structure.
TABLE 1
|
Subfamily / species |
Collector and Locality |
|
M YRMECIINAE Myrmecia pilosula PONERINAE |
B. Holldobler, Brindabella Ranges, Australia |
|
Diacamma australis Ectatomma ruidum |
B. Holldobler, Townsville, Qld., Australia J. Traniello, BCI, Panama |
|
Ectatomma tuberculatum |
J. Traniello, BCI, Panama |
|
Leptogenys diminuta |
B. Holldobler, Kuranda, Qld., Australia |
|
Pachycondyla apiacalis Pachycondvla obscuricornis |
J. Traniello, BCI, Panama J. Traniello, BCI, Panama |
|
Paltothvreus tarsatus |
B. Holldobler, Shimba Hills, Kenya |
|
Rhvtidoponera metallica DORYLINAE |
B. Holldobler, Brindabella Ranges, Australia |
|
Eciton |
A. Aiello, R. Silberglied, BCI, Panama |
|
Neivamvrmex |
A. Aiello, R. Silberglied, BCI, Panama |
|
PSEUDOMYRMECINAE Pseudomvrmex pallidus |
P. Ward, Texas, USA |
|
MYRMICINAE Catalacus intrudens Leptothorax ( Macromischa) alardvcei |
B. Holldobler, Shimba Hills, Kenya B. Cole Florida Keys, USA |
|
Novomessor a/bisetosus |
B. Holldobler, Arizona, USA |
|
Novomessor cockereUi |
B. Holldobler, Arizona, USA |
|
Orectognathus versicolor Pogonomyrmex barbatus |
B. Holldobler, Eungella, Queensland, Australia B. Holldobler, Arizona, USA |
|
NOTHOM YRMECIINAE Nothomvrmecia macrops |
R. W. Taylor, Eyre Peninsula, Australia |
|
ANEURETINAE Aneuretus simoni DOLICHODERINAE |
Anula Jayasuriya, Sri Lanka |
|
Iridomyrmex purpureus |
B. Holldobler, Canberra, Australia |
|
Liometopum apiculatum |
B. Holldobler, Arizona, USA |
|
FORMICINAE Formica perpi/osa Mvrmecocystus mendax Oecophvlla longinoda |
B. Holldobler, Arizona, USA B. Holldobler, Arizona, USA B. Holldobler, Shimba Hills, Kenya |
Intersegmental tergal glands Intersegmental sternal glands
IX VIII VII VI V IV IX VIII VII VI V/ IV
VIII VII VI V IV III VIII VII VI V IV III
+ + r
9
9
r
+
r,c
+
r,c
9
r,c
+
r,c
+
+ + +
r
+ +
+
+
r
TABLE ! (continued)
|
Subfamily 1 species MYRMECIINAE Mvrmecia pilosula |
Other tergal glands |
|
PONERINAE Diacamma austra Us Ectalomma ruiclum Ectafomma tuberculatum Eeptogenys dim inula Pachycondyla apiacal is Pachycondyla obscuricornis |
glandular cells in 7th and 8th segment ducts open dorsally into genital chamber |
|
Pa It othyrei is tar sat i is Rhytidoponera metaUica |
IXth tergite; ducts open into genital chamber |
|
DORYLINAE Eciton |
lllrd |
|
Neivamyrmex PSEUDOMYRMECINAE Pseudomyrmex pallidus MYRMICINAE Catalacus intrudens Leptot borax (Macromischa) alardycei |
lllrd |
|
N o \ 'omessor alb isetosus Novomessor cockerel! i Orectognathus versicolor Pogonomyrmex bar bat us NOTHOM YRMF.CIINAE Not homy rmecia macrops ANEURETINAF, A new el us simoni DOLICHODFRINAF. Iridomyrmex purpureus l.iometopum apiculatum FORMICINAF Formica perpilosa Myrmecocystus mendax Oecophylla bnginoda |
postpetiole gland opens between lllrd tergite and postpetiole postpetiole gland |
Other sternal glands
Tergo-sternal
glands
Sub-
genital
plate Penis Anus
gland gland gland
VUIth
+
+
Between 4/5; 5/6; +
6/7 segments
Between 4/5; 5/6; +
6/7 segments
Between 4/ 5;5 / 6; +
6/7 segments
glandular cells in petiole; ducts +
open ventrallv through cuticle
VII Ith ? +
Vlllth ? +
Between 4/5; 5/6; ?
6/7; 7/8 segments
9 9
9
9
IMrd Vlllth IXth
+
+
Illrd Vlllth IXth
+
+
+ + +
9
9
122
Psyche
[Vol. 89
As mentioned before Janet found this gland not only in workers of M. rubra but also in males. Ant males differ from the workers in having one more exposed segment (8th segment); often even part of the 9th segment is visible. Thus in ant males the pygidial gland does not open at the last exposed tergite (Fig. 1).
As can be seen from tab. 1 we found a pygidial gland in species of the subfamilies Myrmeciinae, Ponerinae, Dorylinae, Pseudomyr- mecinae, Myrmicinae, Nothomyrmeciinae and Dolichoderinae. In Aneuretus simoni (Aneuretinae) we detected a few glandular cells, but we could not clearly see glandular ducts. In the males, as in the workers, there exists a considerable variation in the morphology of the pygidial glands, even within a single subfamily. In some species large clusters of glandular cells are