TERGAL AND SEXUAL ANOMALIES IN BOTHRIURID SCORPIONS (SCORPIONES, BOTHRIURIDAE)

2005·7.3 MB·English

by  Camilo I Mattoni

2005. The Journal of Arachnology 33:622-628
TERGAL AND SEXUAL ANOMALIES IN BOTHRIURID
SCORPIONS (SCORPIONES, BOTHRIURIDAE)
Camilo I. Mattoni: Division of Invertebrate Zoology, American Museum of Natural
History, Central Park West at 79th Street, New York, NY 10024-5192, USA. E-mail:
@
cmattoni amnh.org
ABSTRACT. New data concerning developmental anomalies observed among species of the family
Bothriiiridae (Scorpiones) are presented. Tergal malformations in Bothriurus coriaceiis, Brachistosternus
roigalsinai and Bothriurus noa are described and illustrated. Two new cases ofintersexuality in scorpions,
in specimens of Brachistosternuspentheri and Bothriurus araguayae, are reported and discussed.
Keywords: Developmental anomalies, tergites, intersexuality, Scorpiones, Bothriuridae
There are numerous reports ofdevelopmen- Expression of both states in one specimen is
tal anomalies in scorpions (Table 1). Most re- clearly an abnormality and the existence of
ports relate to the duplication of posterior rare abnormalities does not necessitate the
body segments (Vachon 1952; Hjelle 1990; need to abandon these character systems. Fur-
Sissom & Shelley 1995, see the latter for thermore, many systematists have observed
overview); reference to other types of devel- this kind ofvariation on the chelicerae ofsev-
opmental anomalies in scorpions is scarce. eral species, including cases where both che-
One work includes information about anom- licerae are different from the usual morphol-
alies of the legs and pedipalps (Armas 1977) ogy of the species (Mattoni 2003; Prendini
and another describes a tergal and two cara- pers. comm.). They would not consider these
pacial malformations (Armas 1976). Most re- represent any obstacle for identifying taxa in
cently, Teruel (2004) presented a list and brief question, because these occurrences are rare
description of tergal (see below) and pedipal- in scorpion populations, and there are many
pal anomalies; however, only Armas (1977) additional characters that can assist with an
illustrated the anomalies described, a prereq- identification.
uisite for understanding the anomalies report- The only references to tergal anomalies in
ed. scorpions are the works ofArmas (1976), who
Teruel (2004: 237) references a “cheliceral described a specimen of Didymocentrus trin-
anomaly’' on one specimen of a buthid, Ly~ itarius Franganillo 1930 (Diplocentridae) with
chas obsti Kraepelin 1913. This specimen has fusion ofthe carapace and the first tergite, and
two teeth on the ventral surface of the fixed Teruel (2004) who described anomalies in one
finger of one chelicera and one on the other, male of Microtityus jaumei Armas 1974
the latter expression being the typical condi- (Buthidae), that possessed a double anomaly,
tion forLychas (Vachon 1963; Kovafik 1997). with tergite V completely divided on the pos-
Teruel (2004) notes that this is interesting terior half, and tergite VII fused dorsally to
from a taxonomic viewpoint, because, tradi- metasomal segment 1. Teruel (2004) also re-
tionally, the number of ventral teeth on the ported two female diplocentrids {Cazierius
C
fixed finger has been used as a strong char- parvus Armas 1984 and gundlachii (Karsch
acter in the generic differentiation ofthe scor- 1880) and one euscorpiid (Euscorpius flavi-
pions ofthe family Buthidae (Kraepelin 1899; caudis (DeGeer 1778)), possessing totally di-
Sissom 1990). Teruel (2004) suggested that vided tergites.
using this character to identify buthids from The references to sexual malformations are
Northwest Africa could present problems, be- restricted to 5 reports, involving hermaphro-
cause it could cause erroneous identifications. ditism (with male and female genitalia), gyn-
The two states clearly represent normal vari- andromoiphism (with both sexes discretely
ation in morphology, and are not anomalous. combined) and intersexualism (where the en-
622
MATTONI—ANOMALIES IN SCORPIONS 623
—
Figures 1-3. Carapace and tergites ofmalformed scorpions. 1-2. Females ofBothriuriis coriaceus\ 1.
specimen from 4 km N Los Vilos; 2. specimen from Cuesta de Chacabuco. 3. female ofBrachistosternus
roigalsinai, carapace and tergites. Scale = 5 mm.
tire body is intermediate between sexes). Mat- aly reported by Teruel (2004) on Centromach-
thiesen (1968) described a hermaphrodite etes pocockii (Kraepelin 1894) and Urophon-
specimen ofthe buthid Tityus bahiensis (Perty ius granulatus Pocock 1898, are the only
1833). Cokendolpher & Sissom (1988) de- references to malformations among Bothriur-
scribed two gynandromorphic diplocentrids (a idae.
Cazierius gundlachii (Karsch 1880) and Bio- The main goal of this contribution is to de-
culus comondae Stahnke 1968). Armas (1990) scribe and illustrate the tergal anomalies that
reported a case of one hermaphrodite Alayo- were found in specimens ofthree Bothriuridae
tityus juraguaensis Armas 1973 and a gyn- species, and to report two more cases of in-
andromorphic specimen of Tityopsis inae- tersexuality in scorpions.
qualis (Armas 1974) (Buthidae). Maury The specimens studied are preserved in 80 %
(1983) described an adult hermaphrodite of ethanol and belong to the following collec-
Brachistosternus pentheri Mello-Leitao 1931 tions: AMNH = American Museum of Nat-
(Bothriuridae) showing intersexual and gyn- ural History (New York, USA); MACN-Ar =
andromorphic characteristics, and with both Museo Argentino de Ciencias Naturales “Ber-
embryos and hemispermatophores. Another nardino Rivadavia” (Buenos Aires, Argenti-
interesting malformation was reported in two na) and CDA = Catedra de Diversidad Ani-
males ofthe bothriuridBothriurus bonariensis mal I, Universidad Nacional de Cordoba
(C.L. Koch 1842), found mating with females (Cordoba, Argentina). Illustrations were pro-
in the field, yet presenting only one hemi- duced using a Leica MS5 stereomicroscope
spermatophore, the right paraxial organ (that equipped with a camera lucida. Photographs
produces the hemispermatophore) being ab- were taken with an Olympus Stylus 400 dig-
sent in both specimens (Peretti 2000). The last ital camera under long-wa—ve ultraviolet light.
two reports, togetherwith the pedipalps anom- Specimens examined. Bothriurus cori-
624 THE JOURNAL OF ARACHNOLOGY
ciceiis Pocock 1893. CHILE: Santiago Region, mation, except for the specimen of B. cori-
Chacabuco Province: 1 $, Cuesta de Chaca- aceus from Chacabuco that has a slightly
buco, S side, elev. 3900 ft, dry mountainside abnormal telson vesicle, with the left ventral
(32°59' S, 70°44' W), 14 I 1985, N. Platnick, side a little depressed.
O.E Francke, AMNH; Coquimbo Region, The pigmentation pattern of the malformed
Choapa Province: 1 $, 4 km N Los Vilos tergites is normal on the Bothriurus coriaceus
(31°72' S, 7L3U W), 5 I 1985, N. Platnick, and B. noa specimens, and apparently in the
O. F. Francke, AMNH. Bothriurus noa Maury. Brachistostenus (L.) roigalsinai female as
ARGENTINA: Tucuman Province: 1 $ (par- well. However, in the latter case the specimen
atype), Tafi del Valle (26°52' S, 65°5U W), is not well fixed, and not all the pigmentation
1970 m, 16 I 1981, E. Maury, MACN-Ar has been preserved.
7571. Brachistosternus (Leptosternus) roigal- Tergal malformations include division of
sinai Ojanguren-Affilastro 2002. CHILE: At- tergites and fusion of tergal parts to one an-
acama Region, Huasco Province: 1 9, Llanos other. Armas (1976) described a fusion ofter-
de Challe National Park, (28°09'39.8" S, gite I to carapace, and Teruel (2004) observed
71°03'20.0" W), 205 m, XII 1997, J. Cepeda- division of tergites and fusion to metasomal
Pizarro, CDA. Brachistosternus (L.) pentheri. segment I. All the specimens with anomalous
ARGENTINA: Mendoza Province: 1 d (?), tergites examined here were adult females. Te-
Reserva de la Biosfera Nacunan (34°02' S, ruel (2004) observed the same pattern but
67°54' W), 540 m, 20 XI 2003, C. Mattoni, with four females and one male, and the spec-
L. Prendini, J. Ochoa, CDA. Bothriurus ara- imen referred by Armas (1974) is an adult
guayae Vellard 1934. BRAZIL: Sao Paulo male. I have examined 226 specimens of B.
State: 1 S (?), Estagao Ecologica de Itirapina, coriaceus (57 females, 62 males and 107 ju-
Municipio de Itirapina (22°15' S, 47°49' W), veniles), and found this kind of anomaly only
pitfall, 27 VIII 1999, G. Machado. on the two females referred to here (Mattoni
Two of the females (both B. coriaceiis) 2003). Despite the few cases reported in scor-
were pregnant when preser—ved. pions, the presence of tergal malformations
Tergal malformations. The B. coriaceus only on adults suggests that they arise during
specimen from Cuesta de Chacabuco (Fig. 1) last molt.
shows completely longitudinally divided ter- The causes of these tergal malformations
gites IV and V. Both parts of each tergite rep- are completely unknown, but they do not
resent almost exactly in shape and size the seem to affect the life of the scorpion or its
corresponding half of the tergite; only a small mating. The pigmentation pattern in the ter-
central portion is lacking from the posterior gites of all the specimens appears not to be
edge. The B. noa female shows the same kind altered. —
of anomaly but only on tergite III. Sexual malformations. Brachistosternus
The specimen ofB. coriaceus from 4 km N (L.) pentheri: The specimen has intermediate
Los Vilos (Fig. 2) also presents some divided sexual characteristics: the small size and num-
tergites, with a different arrangement: tergite ber of pectinal teeth (26/30, left/right) suggest
IV is completely divided but tergite V is fused that it is from a female, males posess larger
sinistraly with the dextral half of tergite VI. and more numerous teeth (in the B. pentheri
The recognition of each part of the tergites is population from Nacunan the females usually
difficult because tergites V and VI are almost have 25-32 teeth, and the males 32-41, Roig
the same size. Alsina & Maury 1984); the telson is also more
The Brachistosternus (L.) roigalsinai spec- similar in shape to that of a female; the ped-
imen (Fig. 3) displays a different kind ofmal- ipalp chela has almost all the morphometric
formation: the sinistral half oftergite I is free, characteristics of a male, but the internal
and the dextral half is joined to the sinistral apophysis near the base of the movable finger
halfoftergite II (one can recognize the tergite (a sexual secondary structure present only on
because I and II differ in size). The dextral the males) is extremely reduced to approxi-
halfof tergite II isjoined anteriorly to the ter- mately half of normal size (Figs. 4-6); the
gite III. carapace surface is densely covered withblunt
All observed specimens with tergal anom- granules, as in regular males (females display
alies do not show any other evident malfor- fewer granules), but the tergites are smooth as
MATTONI—ANOMALIES IN SCORPIONS 625
—
Figures 4-9. Right pedipalp chelae, ventrointernal view. 4-6. Bmchistostermis pentheri; 4. male; 5.
intersexual specimen; 6. female. 7-9. Bothriurus araguayae; 7. male; 8. intersexual specimen; 9. female.
Scale = 1 mm. The arrows show the secondary sexual structures.
in females (males display a fine granulation); males are smooth); and the ventral surfaces of
sternites I-III present sparse granulation, and metasomal segments I to III are smooth as ob-
IV and V are smooth (on more typical males, served in females (these surfaces are granular
all sternites are granular, whereas those of fe- on males). The specimen presents a paired
626 THE JOURNAL OF ARACHNOLOGY
glandular surface on the dorsal side of meta- apophysis on the chela, which is absent in the
somal segment V (another sexual secondary B. araguayae specimen, and present, but re-
structure of males, Cekalovic 1973; Peretti duced, in the B. pentheri specimen; and the
1997), but these glands are less well devel- metasomal glands, which are absent on the B.
oped, being shorter than in regular males. The araguayae, and present, but reduced, in the B.
specimen also has well developed hemisper- pentheri.
matophores, with sperm in the seminal duct, These secondary sexual structures have a
and testis tubules present; female genitalia clear function during mating: the apophyses
(ovari-uterus, seminal receptacles and genital on the male chelae help to secure the female
atrium) could not be found. chelae during mating (Maury 1975; Peretti
The presence of male, seemingly function- 1993), and the metasomal glands produce a
al, sexual organs suggests that this specimen secretion that reduces female resistance during
is an adult male with intersexual external mor- mating (Peretti 1997). Further observations
phology. Some of these characters are similar are necessary to understand the incidence of
to those observed by Maury (1983) in a her- such developmental anomalies in scorpion
maphrodite B. pentheri male: poorly devel- populations, and the influence that they might
oped apophyses on the pedipalp chela, re- have on life history (e.g., in reproductive bi-
duced dorsal glands on metasomal segment V, ology), because of possible disadvantages of
intermediate granulation on the carapace and intersexual males in comparison with normal
tergites. The specimen described here presents males.
more feminine external characters, like the The cause of these mutations among scor-
pectines and telson, than those described by pions is unknown. Among other arthropods,
Maury (1983). The main difference between intersexual specimens have been demonstrat-
these specimens is the simultaneous presence ed to be the result of bacterial infection (Bou-
of well developed embryos and hemisperma- chon et al. 1998; Rigaud & Juchault 1998).
tophores in Maury’s specimen, which identi- We suspect that the intersexual phenomenon
fies it as a true hermaphrodite. is not limited to the species described here but
Bothriurus araguayae: The specimen ex- has been largely ignored in other species in
hibits many external characteristics of a fe- which it may occur. Many external characters
male: smooth carapace and tergites (males are widely used for determining the gender of
typically present a fine and even granulation); scorpions, but only the dissection of a speci-
absence of a sexual secondary gland on the men can unequivocally confirm its sex, there-
dorsal side of the telson (present in adult by allowing the identification of intersexual
males); metasomal segment V more robust and hermaphrodite specimens. Also, one
than males, (which have slender segments, anomalous specimen can lead to a mistake,
Lourengo & Maury 1979); and without an that was the case with the “male” of Alayo-
apophysis on the internal surface of the chela, tityus juraguaensis described by Armas
behind the movable finger, that is present in (1984), a specimen with external female char-
the males, and is replaced in this specimen by acteristics and with one paraxial organ, that
a blunt granule (more pronounced than in reg- led to Armas to say that this was the only
ular females) (Figs. 7-9). The male character- species on the genus without sexual dimor-
istics of the specimen are as follows: both phism. But in fact, as later discovered by Ar-
hemispermatophores present, pectines with mas (1990), the specimen was a hermaphro-
larger and with more pectinal teeth, and gen- dite, with one hemispermatophore and
ital operculum formed by two triangular isos- ovari-uterus.
celes plates (these are equilateral in females). I am indebted to Andres Ojanguren-Affilas-
I could not observe sperm in the seminal ves- tro for the information about the specimen of
icles, because of the poor preservation of the B. noa, to Glauco Machado for the donation
reproductive organs. As in the previous case, of several specimens of B. araguayae, to Er-
1 regard the B. araguayae specimen as a male, ich Volschenk for the help with the language,
with intersexual external characteristics. and to the curators of the collections from
The main differences between the intersex- which material was loaned for study: Lorenzo
ual specimens of both species are related to Prendini (AMNH), Cristina Scioscia (MACN-
secondary sexual structures: the internal Ar) and Luis Acosta (CDA). This note was
MATTONI—ANOMALIES IN SCORPIONS 627
—
Table 1. Reported cases and kind of anomalies in families of scorpions. The number of registered
species showing the anomaly is in parentheses. The taxonomy presented in the table in accordance with
Fetet al. (2000). However, see Stockwell (1989), Prendini (2000) and Soleglad & Fet (2003) foralternative
hypotheses.
Anomaly Family and species Main references
Duplication of metasoma Euscorpiidae (2) Sissom & Shelley 1995
Buthidae (8) Vachon 1952; Sisson & Shelley
1995
Tergite division and/or fusion Diplocentridae (3) Armas 1976; Teruel 2004
Bothriuridae (3) This work
Buthidae (1) Teruel 2004
Euscorpiidae (1) Teruel 2004
Leg malformation Buthidae (4) Armas 1977
Pedipalp chela compression on Bothriuridae (2) Teruel 2004
females Buthidae (18)
Chactidae (1)
Chaerilidae (1)
Diplocentridae (3)
Euscorpiidae (3)
Hemiscorpiidae (1)
Liochelidae (1)
luridae (1)
Scorpionidae (1)
Pedipalp fusion Buthidae (1) Cao & Solorzano 1991
Males with intersexual characters Bothriuridae (2) Maury 1983; this work
Males with one paraxial organ Bothriuridae (1) Peretti 2000
Hermaphrodite Bothriuridae (1) Maury 1983
Buthidae (2) Matthiesen 1968, Armas 1990
Bothriuridae (1) Maury 1983
Gynandromorphy Buthidae (1) Armas 1990
Diplocentridae (2) Cokendolpher & Sissom 1988
highly improved by suggestions by Alfredo Cubano. VII. Adiciones y enmiendas (Scorpi-
Peretti, Lorenzo Prendini and Erich Vol- ones: Buthidae, Diplocentridae). Poeyana275:1-
schenk. I would also like to extend a special 37.
thanks to Gail Stratton for her help during the Armas, L.F 1990. Dos casos de anomalia sexual en
escorpiones cubanos (Scorpiones: Buthidae).
review process and for assistance with the fig-
Ciencias Biologicas 21-22:173-175.
ures. This research was conducted at Catedra Bouchon D,, T. Rigaud & P. Juchault. 1998. Evi-
de Diversidad Animal I, Facultad de Ciencias dence forwidespread Wolbachia infection in iso-
Exactas, Efsicas y Naturales, Universidad Na- pod crustaceans: molecular identification and
cional de Cordoba, Argentina; with the finan- host feminization. Proceedings of the Royal So-
cial support of the Consejo Nacional de In- ciety ofLondon, Biological Sciences 265(1401):
vestigaciones Cientificas y Tecnicas 081-1090.
&
(Argentina). Cao, J. L. Solorzano. 1991. Escorpion con pe-
dipalpo anomalo. Resumenes II Simposio de
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