Description of the male of Tityus kuryi Lourenço, 1997 and notes about males of Tityus stigmurus (Thorell, 1877) and Tityus serrulatus Lutz & Mello, 1922 (Scorpiones, Buthidae)

Abstract The male of Tityus kuryi Lourenço, 1997 is described for the first time. Despite being very similar to the female, the male presents more robust metasomal segments. Additionally, the distribution of the sexual populations of another two species of the T. stigmurus complex is reported herein: T. serrulatus Lutz & Mello, 1922 and T. stigmurus (Thorell, 1877). Males of T. serrulatus were, until now, restricted to the Minas Gerais State (Southwestern region of Brazil), and with new records reported here, its known distribution now encompasses the Northeastern region of Brazil. Males of T. stigmurus were previously recorded only for two municipalities in the State of Bahia, and here we present eight new records for Bahia State and one for Pernambuco State. We present a key to related species of the T. stigmurus complex based on morphology and coloration pattern.


Introduction
The description of males in population of scorpions is an important contribution, not only as regards taxonomic knowledge of the species, but also to enable understanding of its reproductive strategy.Tityus kuryi Lourenço, 1997 was described based on a single adult female collected in Palmeiras Municipality, in the Chapada Diamantina region, Bahia State, Brazil (Lourenço 1997).Although this species has previously been described, the male has not been described yet.In the last taxonomic review, Souza et al. (2009) included T. kuryi in the Tityus stigmurus complex, together with other five related species: Tityus aba Candido, Lucas, Souza, Diaz & Lira-da-Silva, 2005; T. martinpaechi Lourenço, 2001;T. melici Lourenço, 2003;T. serrulatus Lutz &Mello, 1922 andT. stigmurus (Thorell, 1887).This was due to the fact that they share the spinoid granules of the posterior dorsal region of the metasomal segments III and IV (Souza et al. 2009).
The two more widely distributed species from the Tityus stigmurus complex are parthenogenetic: T. serrulatus and T. stigmurus (Matthiessen 1962, Ross 2010).Both species are considered scorpions of medical importance (Brasil 2009).Despite their recognized asexual reproductive strategy, especially observed in urban areas, sexual populations have been recognized in Brazil, where males were described (Souza et al. 2009).Males of these two species were first reported by Lourenço and Cloudsley-Thompson in 1999 stating sexual populations in Minas Gerais and Pernambuco states.In the last review of the T. stigmurus complex, Souza et al. (2009) redescribed the males of T. serrulatus and T. stigmurus with greater number of details, especially in relation to dimorphism.These last authors based their study on specimens of T. serrulatus from Espinosa Municipality, Minas Gerais State, and on specimens of T. stigmurus from Camaçari and Paulo Afonso Municipalities, Bahia State.As far as we know, these are the only published records of males from both species.
In this paper, we describe the male of T. kuryi and report new records of T. serrulatus and T. stigmurus males, widening the known distribution of their sexual populations.

Materials and methods
Specimens of Tityus kuryi (n = 9), T. serrulatus (n = 1595) and T. stigmurus (n = 380) present in the scientific collection of the "Museu de Zoologia da Universidade Federal da Bahia (MZUFBA)" were analyzed.Along with these, another 280 specimens of T. stigmurus present in the reference collection of the "Centro de Informações Antiveneno do Estado da Bahia" (CIAVE), Health Department of Bahia State, were also studied.Of the nine T. kuryi examined, four of them were kept in captivity for a year and a half (August 2009 to February 2011), a fact that allowed us to identify the spermatophore and to confirm the presence of two males.
The measurements were obtained following the methodology of Sissom et al. (1990) and using a digital Starrett 727 caliper.Trichobothrial notations follow Va-chon (1974) while morphological terminology mostly follows Hjelle (1990), except for pedipalp carinae (Stahnke 1970).Observations of the morphology were made using a LEICA Z4 stereomicroscope.The photos of the specimens were taken with a Nikon D7000 camera, Micro Nikkor 85mm and Micro Nikkor 105mm lenses.The photos and measurements of the hemispermatophore were taken using the software program Motic Images 2000 version 1.2 by means of a PC connected to a Motic Digital stereomicroscope SMZ 168.The map of geographic distribution was produced with the ArcGis 10.0 software.
The males of Tityus serrulatus and T. stigmurus were identified based on observation of the external morphological characteristics, as diagnosed by Souza et al. (2009).The identification of the male of T. kuryi was based on observation of the courtship behavior, copulation and deposition of spermatophore (MZUFBA 2569), carried out in captivity occurred in May 2010.The hemispermatophore here described was dissected and deposited in the arachnid collection (MZUFBA 2570).Diagnosis.Scorpion of medium to large size, ranging from 55 to 78mm in total length.General coloration dark reddish with blackish spots on the pedipalps, legs, lateral surfaces of mesosomal tergites and ventral submedian carinae of all metasomal segments, as well as transversal blackish spots on the posterior margin of sternites.Carinae moderately to strongly marked; granulations moderately to weakly marked.Fixed and movable fingers with 16-17 oblique rows of granules.Pectines with 24-25 teeth in males, 23-26 in female.Secondary sexual dimorphism evident.

Abbreviations
Comparisons with related species.Tityus kuryi Lourenço, 1997, belongs to the "Tityus stigmurus" species complex.The male of T. kuryi can be distinguished from the other males of the species complex, particular from T. aba, T. stigmurus and T. martinpaechi, by the absence of three longitudinal dark brown stripes on mesosomal tergites.Furthermore, in T. aba and T. martinpaechi, the pedipalp of the males is much thinner than of females, which also occurs in T. melici although there is no metasomal dimorfism in it (Souza et al. 2006, Souza et al. 2009).T. kuryi show pedipalps with no dimorphism (Figs 1-4).However, the male metasoma is more robust than the female, the same pattern of differentiation that can be observed in other species of the T. stigmurus complex, such as T. serrulatus and T. stigmurus (Souza et al. 2009).Coloration: Reddish brown with numerous dark areas (Fig. 1).Carapace dark with some light-brown areas (Fig. 5).Ocular tubercle dark.Mesosoma dark in tergite VI, tergite VII with a darker central region and lighter red-brown lateral region (Fig. 1); metasomal segments I-IV reddish brown with dark areas posteriorly in the lateral region and on the submedian ventral carinae (Figs 1 and 3); a dark spot occupying almost the entire segment V (Fig. 12).Telson: vesicle reddish brown, lighter than the metasomal segment V, with two small spots at the base; aculeus with dark spots at the base, red-brown medially and blackened distally (Fig. 12).Coxosternal region yellow with black spots in the coxapophyse I and II (Fig. 3); sternite III light brown, sternites IV-VI darker with the posterior medial region light brown, sternite VII darker with medially light brown T-shaped spots (Fig. 3).Chelicerae dark with a light brown base; apex of the fingers brown.Pedipalps reddish brown with dark spots in the patella (Figs 9-10) and chela (Figs7-8); fingers generally dark but distally light brown.Legs light brown with dark spots on tibia and tarsi (Fig. 1).

Key to related species of the T. stigmurus complex
Morphology: Carapace: anterior margin with a weak median concavity (Fig. 5); median ocular tubercle situated anterior to the center of the carapace and median eyes separated by more than one ocular diameter.Three pairs of lateral eyes; median ocular carina moderate with medium granules (Fig. 5); anterior median furrow moderately deep.Moderately granular.
Mesosoma: Tergites moderately granular with larger granules in the posterior region; presence of median carinae in all tergites.Tergites I-II with reduced carinae; in the tergites III-IV the carinae occupy the distal half and begin bifurcated and finish merged; tergite VII pentacarinate; transversal carinae present in all tergites.Pectines: pectinal teeth 24-25, basal middle lamellae of pectines not dilated (Fig. 6).Sternites weakly granular; a clear triangular zone in the posterior region of the sternite III and a reduced smooth and shiny slightly expanded triangular zone in the posterior region of the sternite V (Fig. 3).Sternite VI with two short median carinae occupying the distal half.Sternite VII with five carinae, two parallel submedian, occupying the entire sternite with a small carinae between them, and two lateral carinae restricted to the central region.Metasoma: Metasomal segments: I with ten complete paired carinae (ventral submedian, ventral lateral, lateral inframedian, lateral supramedian and dorsal lateral with adjacent granules, the dorsal lateral has one spinoid posterior granule) (Fig. 12); II with eight complete paired carinae (inframedian lateral carinae incomplete on anterior third and present sparse granules; others are complete with adjacent granules; dorsal lateral with one spinoid granule) (Fig. 12); III with eight complete paired carinae (inframedian lateral carinae absent; others complete with adjacent granules, the dorsal lateral with three spinoid posterior granules) (Fig. 12); IV with eight complete paired carinae (inframedian lateral carinae absent; others are complete with adjacent granules; dorsal lateral with four spinoid posterior granules) (Fig. 12) ; V with five complete carinae with uniform and adjacent granules (inframedian lateral carinae and dorsal lateral carinae absent; two complete paired carinae: ventral submedian and ventral lateral; one ventral median carina); intercarinal surface moderately granular (Fig. 12).Telson: vesicle with five carinae (four of which vestigial and only the ventral well defined); aculeus long and strongly curved; subaculear tooth strong and romboid with two small dorsal teeth (Fig. 12).
Hemispermatophore: Flagelliform, long and narrow, measuring approximately 13.5 mm, general color light brown; the trunk is trough-shaped; the flagellum is half the width of the trunk and approximately the same length (Fig. 13).Presence of three distal lobes: basal lobe, internal lobe and external lobe.The basal lobe is hook-shaped, protruding internally or externally; the internal lobe extends up to the base of the basal lobe flagellum, the external lobe extends from the medial basal lobe to the posterior third of the internal lobe (Fig. 14).The basal and external lobes are blackened.
Sexual dimorphism: Despite being similar to the females with regard to the coloration pattern and morphological details of the species (Figs 1-4), the male of T. kuryi presents metasomal segments 1.5 time more robust than those of the females (Figs 1-4; Table 1).
Distribution.Known only from the Chapada Diamantina region, Bahia State, Brazil.
Variation.The male of T. kuryi is usually larger than the female (male: 72.93-72.95mm; female: 58.54-78.03mm)and pectinal tooth counts varied as follows: 24-25 teeth in males and 23-26 in females.The number of principal rows of granules varied from 16-17 in both sexes.The spinoid granules on the posterior end of the dorsal lateral carinae of metasomal segments III and IV are greater in number, is larger and sharper on the left than on the right, and the counts varied as follows: 1-3 in metasomal segment III and 2-4 in metasomal segment IV.
Ecology.Tityus kuryi occurs in a restricted environment of montane savannas biome named "Campos Rupestres" of the Espinhaço Range (Cadeia do Espinhaço), in rocky areas of high altitudes in the Chapada Diamantina, Bahia State.The annual average temperature there is 22-24 °C, with 36-38 °C as absolute maximum and 4.8 °C as absolute minimum.It is found at altitudes above 840 m.They can also be found near to residential areas, but always near to natural fragments hidden in debris under or between stones.

Distribution of Tityus serrulatus and T. stigmurus males
In an attempt to explain the strategies of the life history in populations of scorpions, Vandel (1928apud Lourenço 2008) was the first to use the term "geographical parthenogenetics" to name the features that various authors had already observed: the parthenogenetics and sexual populations of the same species tend to occur in different habitats.
The sexual populations of Tityus serrulatus and T. stigmurus have a highly restricted geographic distribution, while asexual populations (parthenogenetic) of both species have a wide geographic distribution, occupying urban areas across the Country (Lourenço 2008).This reproductive strategy is advantageous, it allows rapid colonization and wider dispersion in disturbed environments (Lourenço andCuellar 1995, Lourenço 2002).Thus, it allows these scorpions to occupy areas where sexual populations have difficulties in establishing colonies (Lynch 1984, Cuellar 1994).This can increase the species reproductive capacity by about twofold, as parthenogenesis is of the thelytoky type (production of all-female progeny) (Glesener and Tilman 1978).
Although Tityus serrulatus has been known as parthenogenetic since 1962 (Matthiesen 1962), this not occur with T. stigmurus, whose confirmation of reproductive strategy came much later when Ross (2010) reported the occurrence of thelytokous parthenogenesis in this species.In both, parthenogenesis is not a mandatory feature, as shown in last review of the Tityus stigmurus complex that describes males for both species (Souza et al. 2009).The new records that we present in this study (Table 2) indicate the occurrence of sexual populations of T. stigmurus in eight municipalities of Bahia, in addition to those already known, Camaçari and Paulo Afonso (Souza et al. 2009) and one record in Pernambuco State (see Table 2).These records improve the knowledge on the distribution of the sexual populations of this species.
The male specimen of T. serrulatus used in this study is deposited in MZUFBA and came from the municipality of São Desiderio, Bahia.We can say now that sexual population of this species, previously restricted to the State of Minas Gerais (municipality Espinosa) and Southeastern Brazil (Lourenço andCloudsley-Thompson 1999, Souza et al. 2009), can also be found in the Northeast of the Country (Fig. 15).
In spite of the new records of sexual populations of Tityus serrulatus and T. stigmurus to previously unknown areas, parthenogenesis seems to be the main reproductive strategy of these species.This assertion is primarily based on the low frequency of males of these species in three of the largest scorpion collections in Brazil (Instituto Butantan-SP, Museu Nacional-RJ and MZUFBA) and on our field experience collecting with a UV flashlight.Unlike other parthenogenetic scorpions, T. serrulatus and T. stigmurus are actually the two species better adapted to urban environments.They are regarded as a public health problem due to their rapid expansion in urban ar- Salvador, Bahia 12°58'16"S 38°30'39"W eas, their proliferation and the toxic effects of their poison (Lourenço andCloudsley-Thompson 1999, Brasil 2009).We can emphasize here the large number of individuals analyzed as opposed to the few males found, providing evidence of the rarity of males, both in nature and in scientific collections.

Figure 15 .
Figure 15.Map showing the previous and new records of males of Tityus kuryi, T. serrulatus and T. stigmurus.

Table 1 .
Measurements (in mm) of two males and seven females used to investigate the sexual dimorphism in Tityus kuryi.