2005. The Journal of Arachnology 33:622±628

TERGAL AND SEXUAL ANOMALIES IN BOTHRIURID (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: [email protected]

ABSTRACT. New data concerning developmental anomalies observed among species of the family Bothriuridae (Scorpiones) are presented. Tergal malformations in coriaceus, roigalsinai and Bothriurus noa are described and illustrated. Two new cases of intersexuality in scorpions, in specimens of Brachistosternus pentheri and Bothriurus araguayae, are reported and discussed. Keywords: Developmental anomalies, tergites, intersexuality, Scorpiones, Bothriuridae

There are numerous reports of developmen- 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 of variation on the chelicerae of sev- 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 populations, and there are many pal anomalies; however, only Armas (1977) additional characters that can assist with an illustrated the anomalies described, a prereq- identi®cation. uisite for understanding the anomalies report- The only references to tergal anomalies in ed. scorpions are the works of Armas (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 of the carapace and the ®rst tergite, and two teeth on the ventral surface of the ®xed Teruel (2004) who described anomalies in one ®nger 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 for Lychas (Vachon 1963; KovarÏõÂk 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 I. Teruel (2004) also re- tionally, the number of ventral teeth on the ported two female diplocentrids (Cazierius ®xed ®nger has been used as a strong char- parvus Armas 1984 and C. gundlachii (Karsch acter in the generic differentiation of the scor- 1880) and one euscorpiid (Euscorpius ¯avi- pions of the 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 identi®cations. ditism (with male and female genitalia), gyn- The two states clearly represent normal vari- andromorphism (with both sexes discretely ation in morphology, and are not anomalous. combined) and intersexualism (where the en-

622 MATTONIÐANOMALIES IN SCORPIONS 623

Figures 1±3.ÐCarapace and tergites of malformed scorpions. 1±2. Females of Bothriurus coriaceus;1. specimen from 4 km N Los Vilos; 2. specimen from Cuesta de Chacabuco. 3. female of Brachistosternus roigalsinai, carapace and tergites. Scale ϭ 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 of the 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 of three 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-LeitaÅo 1931 tions: AMNH ϭ American Museum of Nat- (Bothriuridae) showing intersexual and gyn- ural History (New York, USA); MACN-Ar ϭ 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 ϭ CaÂtedra de Diversidad Ani- males of the bothriurid Bothriurus bonariensis mal I, Universidad Nacional de CoÂrdoba (C.L. Koch 1842), found mating with females (CoÂrdoba, Argentina). Illustrations were pro- in the ®eld, 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-wave ultraviolet light. two reports, together with the pedipalps anom- Specimens examined.ÐBothriurus cori- 624 THE JOURNAL OF ARACHNOLOGY aceus 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 (32Њ59Ј S, 70Њ44Ј W), 14 I 1985, N. Platnick, side a little depressed. O.F. 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 (31Њ72Ј S, 71Њ31Ј 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: TucumaÂn Province: 1 & (par- well. However, in the latter case the specimen atype), TafõÂ del Valle (26Њ52Ј S, 65Њ51Ј W), is not well ®xed, 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-Af®lastro 2002. CHILE: At- tergites and fusion of tergal parts to one an- acama Region, Huasco Province: 1 &, Llanos other. Armas (1976) described a fusion of ter- de Challe National Park, (28Њ09Ј39.8Љ S, gite I to carapace, and Teruel (2004) observed 71Њ03Ј20.0Љ 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 ( (?), tergites examined here were adult females. Te- Reserva de la BioÂsfera NÄ acunÄaÂn (34Њ02Ј S, ruel (2004) observed the same pattern but 67Њ54Ј 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 ( (?), EstacËao EcoloÂgica de Itirapina, coriaceus (57 females, 62 males and 107 ju- Municipio de Itirapina (22Њ15Ј S, 47Њ49Ј 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. coriaceus) 2003). Despite the few cases reported in scor- were pregnant when preserved. pions, the presence of tergal malformations Tergal malformations.ÐThe 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.ÐBrachistosternus The specimen of B. 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 NÄ acunÄan the females usually dif®cult 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 of mal- ipalp chela has almost all the morphometric formation: the sinistral half of tergite 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 ®nger half of tergite 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- half of tergite II is joined anteriorly to the ter- mately half of normal size (Figs. 4±6); the gite III. carapace surface is densely covered with blunt 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 MATTONIÐANOMALIES IN SCORPIONS 625

Figures 4±9.ÐRight pedipalp chelae, ventrointernal view. 4±6. Brachistosternus pentheri; 4. male; 5. intersexual specimen; 6. female. 7±9. Bothriurus araguayae; 7. male; 8. intersexual specimen; 9. female. Scale ϭ 1 mm. The arrows show the secondary sexual structures. in females (males display a ®ne 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 in¯uence 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 , 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 ®es 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 ®ne and even granulation); scorpions, but only the dissection of a speci- absence of a sexual secondary gland on the men can unequivocally con®rm its sex, there- dorsal side of the telson (present in adult by allowing the identi®cation 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, LourencËo & 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 ®nger, 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 AndreÂs Ojanguren-Af®las- 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,toEr- I 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 MATTONIÐANOMALIES IN SCORPIONS 627

Table 1.ÐReported cases and kind of anomalies in families of scorpions. The number of registered species showing the anomaly is in parentheses. The presented in the table in accordance with Fet et al. (2000). However, see Stockwell (1989), Prendini (2000) and Soleglad & Fet (2003) for alternative 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) Iuridae (1) (1) Pedipalp fusion Buthidae (1) Cao & SoloÂrzano 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). Poeyana 275:1± 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 review process and for assistance with the ®g- escorpiones cubanos (Scorpiones: Buthidae). Ciencias BioloÂgicas 21±22:173±175. ures. This research was conducted at CaÂtedra Bouchon D., T. Rigaud & P. Juchault. 1998. Evi- de Diversidad I, Facultad de Ciencias dence for widespread Wolbachia infection in iso- Exactas, FõÂsicas y Naturales, Universidad Na- pod crustaceans: molecular identi®cation and cional de CoÂrdoba, Argentina; with the ®nan- host feminization. Proceedings of the Royal So- cial support of the Consejo Nacional de In- ciety of London, Biological Sciences 265(1401): vestigaciones Cientõ®cas y TeÂcnicas 081±1090. (Argentina). Cao, J. & L. SoloÂrzano. 1991. EscorpioÂn con pe- dipalpo anoÂmalo. ResuÂmenes II Simposio de LITERATURE CITED ZoologõÂa, La Habana, p. 48. Armas, L.F. 1976. Escorpiones del archipieÂlago cu- Cekalovic, K.T. 1973. Nuevo caracter sexual secun- bano. 6. Familia Diplocentridae (Arachnida: dario en los machos de Brachistosternus (Scor- Scorpionida). Poeyana 147:1±35. piones, Bothriuridae). BoletõÂn de la Sociedad de Armas, L.F. 1977. AnomalõÂas en algunos Buthidae BiologõÂa de ConcepcioÂn 46:41±51. de Cuba y Brazil. Poeyana 176:1±6. Cokendolpher, J.C. & W. D. Sissom. 1988. New Armas, L.F. 1984. Escorpiones del ArchipieÂlago gynandromorphic Opiliones and Scorpiones. 628 THE JOURNAL OF ARACHNOLOGY

Bulletin of the British Arachnological Society el comportamiento sexual (Scorpiones). Revue 7(9):278±280. Arachnologique 12(3):31±41. Fet, V., W.D. Sissom, G. Lowe & M.E. Braunwald- Peretti, A.V. 2000. Existencia de cortejo en el cam- er. 2000. Catalog of the scorpions of the world po de machos de Bothriurus bonariensis (Scor- (1758±1998). New York Entomological Society, piones: Bothriuridae) que carecen de un oÂrgano New York. pp. 1±670. paraxial. Revista de la Sociedad EntomoloÂgica Hjelle, J.T. 1990. Anatomy and morphology. Pp. 9± Argentina 59(1±4):96±98. 63. In The Biology of Scorpions (G.A. Polis, Prendini, L. 2000. Phylogeny and classi®cation of ed.). Stanford University Press, Stanford, Cali- the Superfamily Scorpionoidea Latreille 1802 fornia. (, Scorpiones): an exemplar approach. KovarÏõÂk, F. 1997. Revision of the genera Lychas Cladistics 16:1±78. and Hemilychas, with descriptions of six new Rigaud T. & P. Juchault. 1998. Sterile intersexuality species (Scorpiones, Buthidae). Acta Societatis in an isopod induced by the interaction between Zoologicae Bohemoslovenicae 61:311±371. a bacterium (Wolbachia) and the environment. Kraepelin K. 1899. Scorpiones und Pedipalpi. In Canadian Journal of Zoology 76:493±499. Roig Alsina, A.H. & E.A. Maury. 1984. SistemaÂtica Das Tierreich (F. Dahl, ed.). FriedlaÈnder und y distribucioÂn geogra®ca de Brachistosternus Sohn Verlag, Berlin, 8:1±265. (L.) pentheri Mello-LeitaÄo, 1931 (Scorpiones, LourencËo, W.R. & E.A. Maury. 1979. Quelques Bothriuridae). Physis (C) 42(102):17±21. consideÂrations sur la systeÂmatique du scorpion Sissom, W.D. 1990. Systematics, biogeography and breÂsilien Bothriurus araguayae Vellard, 1934 palentology. Pp. 64±160. In The Biology of (Bothriuridae). Bulletin du MuseÂum National Scorpions (G.A. Polis ed.). Stanford University d'Historie Naturelle, Paris (Zoologie, Biologie et Press, Stanford, California. È Ecologie Animales) 2:421±431. Sissom, W.D. & R.M. Shelley. 1995. Report on a Matthiesen, F.A. 1968. On the male reproductive rare developmental anomaly in the scorpion, organs in some brazilian scorpions. Revista Bras- Centruroides vittatus (Buthidae). Journal of Ar- ileira de Pesquisas Medicas e Biologicas 1(5±6): achnology 23:199±201. 273±274. Soleglad, M.E. & V. Fet. 2003. High-level system- Mattoni, C.I. 2003. Patrones evolutivos en el geÂnero atics and phylogeny of the extant scorpions Bothriurus (Scorpiones, Bothriuridae): anaÂlisis (Scorpiones: Orthosterni). Euscorpius 11:1±175. ®logeneÂtico. Doctoral Thesis, Universidad Na- Stockwell, S.A. 1989. Revision of the Phylogeny cional de CoÂrdoba, Argentina. i±vii ϩ 249 pp. and Higher Classi®cation of Scorpions (Cheli- Maury, E.A. 1975. Sobre el dimor®smo sexual de cerata). Ph.D. Thesis, University of California, la pinza de los pedipalpos en los escorpiones Berkeley. i±iv, 1±413 pp. Bothriuridae. Bulletin du MuseÂum National Teruel, R. 2004. Nuevos casos de anomalõÂas mor- d'Histoire Naturelle, Paris, Zoologie 215:765± foloÂgicas en escorpiones (Scorpiones: Bothriuri- 771. dae, Buthidae, Chactidae, Chaerilidae, Diplocen- Maury, E.A. 1983. Singular anomalõÂa sexual en un tridae, Euscorpiidae, Hemiscorpiidae, ejemplar de Brachistosternus pentheri Mello- Ischnuridae, Iuridae, Scorpionidae). Revista Ib- eÂrica de AracnologõÂa 7:235±238. Leitao 1931 (Scorpiones, Bothriuridae). Revista  de la Sociedad EntomoloÂgica Argentina 42(1±4): Vachon, M. 1952. Etudes sur les scorpions. Ar- chives de l'Institut Pasteur d'AlgeÂrie, Alger. 482 155±156. pp. Peretti, A.V. 1993. Estudio de la biologõÂa reprod- Vachon, M. 1963. De l'utiliteÂ, en systeÂmatique, uctiva en escorpiones argentinos (Arachnida, d'une nomenclature des dents des cheÂliceÁres chez Scorpiones): un enfoque etoloÂgico. Doctoral les Scorpions. Bulletin du MuseÂum National Thesis, Universidad Nacional de CoÂrdoba, Ar- d'Historie Naturelle, Paris 35(2):161±166. gentina. i±ix ϩ 307 pp. Peretti, A.V. 1997. RelacioÂn de las glaÂndulas cau- Manuscript received 31 December 2004, revised 15 dales de machos de escorpiones Bothriuridae con August 2005.