Taxonomy and distribution of Talitroides alluaudi ( Chevreux , 1896 ) and T . topitotum ( Burt , 1934 ) ( Amphipoda , Talitridae ) in Atlantic rain forests of southeastern Brazil

Th e family Talitridae Rafi nesque, 1815 is the only group, among the amphipods, that colonized the terrestrial environment, and more than half of its species live in tropical and subtropical forests. Nowadays, the family has approximately 270 species described in 64 genera. Leaf litt er samples from Atlantic forests and urban areas of the states of Rio de Janeiro, São Paulo, Minas Gerais, Paraná, Santa Catarina, and Rio Grande do Sul, provided material to redescribe the two terrestrial species known to Brazil, Talitroides alluaudi (Chevreux, 1896) and Talitroides topitotum (Burt, 1934), and enlarge their known distribution. Th ese species have a worldwide distribution, as they are commonly dispersed in a synanthropic way. Talitroides topitotum seems to be well established in Brazilian Atlantic forests: 96% of the 1787 individuals examined (51 samples) corresponded to this species. Also, females dominated the samples and only six males were found: four from T. alluaudi and two from T. topitotum. A detailed comparison of these two species, as well as their geographical distribution, is given. key words Taxonomy, Talitridae, Atlantic forest, introduced species, Brazil.


introduction
The family Talitridae Rafinesque, 1815 is the only group among the amphipods that colonized the terrestrial environment, including supralitt oral beaches, estuarine areas, caves and forests.During the past 10 years many species and genera have been erected for the family Talitridae and nowadays there are approximately 270 species described in 64 genera (Horton and De Broyer, 2015), with more than half of these species found in forests, indicating a strong adaptive radiation of the group in the terrestrial habitat (Bousfi eld, 1984).Th e classical ecological groups proposed by Bousfi eld (1984) for the Talitridae are: palustral talitrids; beach-hoppers (non-substrate modifying); sand-hoppers (substrate modifying) and land-Talitroides from Brazilian rain forest Nauplius, 24: e2016002 hoppers.More recently, Wildish et al. (2012) proposed another ecological classification for the group: terrestrial talitrids; wrack generalists; and substratum specialists.Among the last group three subgroups were recognized: sand burrowers, troglobionts (from caves) and driftwood talitrids.They play important roles in the dynamics of their habitat functioning as decomposers since they are essentially detritivorous animals (Friend and Richardson, 1986;Friend, 1987).
Terrestrial talitrids are commonly called landhoppers and are primarily distributed in New Zealand, Australia, the Pacific and Subantarctic Islands, South Africa, Indo-Pacific region and Central America (Hurley, 1968;Bousfield, 1984;Friend and Richardson, 1986).Some species have been introduced in many regions, including South and North America, western Eurasia, and the United Kingdom (Bousfield, 1984;Duncan, 1994).When dealing with truly terrestrial habitats there are no records of native talitrids in Brazil.On the other hand, the introduced species Talitroides topitotum (Burt, 1934) was first registered in Brazil from São Paulo by Lemos de Castro (1972).After that, Lemos de Castro and Pereira (1978) reported T. topitotum again from Rio de Janeiro (RJ) and recorded for the first time a large population of Talitroides alluaudi (Chevreux, 1896) from Madureira (RJ).However, the latter species is not so common and until the present study it has no further records in Brazil after its first record.Whereas T. topitotum seems to be very widespread and abundant in some areas, as shown by studies on reproductive biology and distribution at Serra do Mar, Guaratuba, Paraná (Lopes and Masunari, 2004a;2004b) and at Serra do Mar State Park, São Paulo (Matavelli et al., 2009).More recently, Eutrópio and Krohling (2013) recorded T. topitotum from coffee and Eucalyptus plantations in the state of Espírito Santo.Talitroides topitotum seems to be introduced in Brazil by imported plants from the United States that received Eucalyptus trees from Australia for commercial purposes (Lopes and Masunari, 2004a) and probably have been spread by human gardening and landscaping activities.
After Chevreux's early descriptions (Chevreux, 1896;1901;Chevreux and Fage, 1925), a recent study redescribed the type material of T. alluaudi deposited in the Paris Museum, which clarified the identity of this species (Morino and Ortal, 1993).Burt (1934) originally described T. topitotum from Ceylon (now Sri Lanka), India (as Talitrus), and later Stephensen (1935) and Shoemaker (1936) redescribed this species wrongly identified as Talitrus sylvaticus Haswell, 1879 and mentioned its introduction in North America.Hurley (1955) described Talitrus (Talitroides) pacificus from New Zealand, which was subsequently synonymized to T. topitotum by Bousfield (1982).More recently, Morino (2013) redescribed T. topitotum based on material from tropical East Asia.Both T. alluaudi and T. topitotum have a wide distribution in the tropics, subtropics and warm temperate forests of the world.At the same time, they occur in greenhouses, urban parks and silviculture areas as they are known to present a synanthropic dispersal (Vader, 1972;Bousfield, 1984;Friend and Richardson, 1986).Sampling in the Atlantic forest litter and urban areas of the states of Rio de Janeiro, São Paulo, Minas Gerais, Paraná, Santa Catarina and Rio Grande do Sul provided material to redescribe and enlarge the distribution of the two terrestrial species previously known in Brazil: T. alluaudi and T. topitotum.Detailed comparison between these two species with comments on its distribution is given.

Material and Methods
Material examined was collected since 1970 among urban areas and litter of a vast area of the Brazilian Atlantic forest including the states of Minas Gerais, Rio de Janeiro, São Paulo, Paraná, Santa Catarina, and Rio Grande do Sul.These specimens were deposited in the Crustacea Collection of the Museu Nacional (MNRJ), Universidade Federal do Rio de Janeiro and in the Collection of the Universidade Federal do Rio Grande do Sul (UFRGS).Part of the collection of the UFRGS was legged to the MNRJ, which received a MNRJ number, although the corresponding UFRGS catalog numbers are given in parenthesis.Both Talitroides alluaudi and Talitroides topitotum are herein redescribed based on the Brazilian material which will complement recent redescriptions made by Morino and Ortal (1993) and Morino (2013).Pooters and pitfall traps were used for collecting specimens.The material was examined under a Zeiss Stemi SV6 stereomicroscope and ZEISS Axioscope coupled with a camera lucida.The individuals were identified, counted and separated by sex, with females being also separated into ovigerous and not ovigerous.The mouthparts were dissected and mounted in semi-permanent slides made with glycerin jelly.Illustrations were prepared using Corel Draw X4 graphics program with the aid of a Wacom pen tablet 4 adapted from the methodology proposed by Coleman (2006).Photomicrographs were made in a scanning electron microscope (SEM) JEOL model 6390 series set in the Electron Microscopy Center of the Museu Nacional.The methodology used to prepare the material for SEM photos was adapted from Felgenhauer (1987).Setae nomenclature follows Zimmer et al. (2009).Burt, 1934: 184.Talitrus (Talitroides) Hurley, 1955: 147.Type species.Talitroides bonnieri Stebbing, 1906, by monotypy (= Talitroides alluaudi (Chevreux, 1896)).(Chevreux, 1896) and Talitroides topitotum (Burt, 1934).
Ecology.Found in forests of tropics, subtropics and warm temperate regions, and also from greenhouses of Europe and North America (Friend and Richardson, 1986).In Brazil, T. alluaudi was also found in urban areas of Rio de Janeiro, in a moist environment under rubbish (Lemos de Castro and Pereira, 1978) and among the litter of green areas of Universities of São Paulo and Rio Grande do Sul (present study).
The specimens analyzed herein agree with the description of the lectotype in presenting diagnostic features s u c h as: absence of oostegite 2; inner ramus of pleopod 1 2-articulated; inner ramus of pleopod 2 1-articulated and dactylar dentition present in pereopod 4. Morino and Ortal (1993) described the article 4 of maxilliped as partially fused to article 3. The material analyzed herein showed a complete separation between articles 3 and 4. Difference in the number of robust setae on telson was noticed, with the Brazilian material having from 4-5 setae on each side instead of 3-4 setae described by these authors.Nevertheless, dactylar dentition noticed by these authors in pereopod 4 was also seen in all our specimens, including the juveniles, being an important diagnostic feature to be considered.Morino and  Ortal (1993) also described a slight prominence in the dactyl of pereopod 3 in most of his material, but individuals from Azores had a dactylar dentition similar to that of the pereopod 4. In all specimens analyzed herein the dactylar dentition in pereopod 3 was much weaker than that of pereopod 4. In individuals collected in IPH (Instituto de Pesquisas Hidráulicas), UFRGS, Rio Grande do Sul, also a prominence in dactyl of pereopods 5 was observed, similar to that of pereopod 3. Chevreux (1901) also mentioned a dactylar dentition on pereopod 5.
Variations in pleopods 1-3 are also a recurrent theme in studies of T. alluaudi as shown by Palmén (1947) with specimens from Finland.The pleopod 1 may have 1 or 2 articles in the inner ramus; pleopod 2 may have the first article of inner ramus more or less developed; pleopod 3 can be 1-or 2-articulated, in which the second is reduced and can have an apical seta.Morino and Ortal (1993) described inner ramus of pleopod 1 mostly with 2 articles, but there may be a variation of 1-4 articles, while the pleopod 2 always showed 1 article in the outer ramus, but one specimen in material from Azores had 3 articles.The samples analyzed here showed no variation in the number of articles in pleopods 1-3.They follow the predominant pattern described by Anderson (1962) and Morino and Ortal (1993).
Ecology.Found in forests of tropics, subtropics and warm temperate regions, and also from greenhouses of Europe and North America (Friend and Richardson, 1986).Most samples of the present study came from the tropical Serra do Mar Forests an ecoregion of the Brazilian Atlantic Forest, located in the south and southeastern coast of Brazil in states of Minas Gerais, Espírito Santo, Rio de Janeiro, São Paulo, Paraná, Santa Catarina, and Rio Grande do Sul (Galindo-Leal and Câmara, 2005).Talitroides topitotum also seems to be associated with areas that were reforested with Eucalyptus spp., a culture that covers extensive areas in Brazil (Lopes and Masunari, 2004a).The individuals analyzed in present study were found between 0−1761m altitude.
Remarks.The material examined generally agrees with previous descriptions of T. topitotum (Burt, 1934;Stephensen 1935;Morino, 2013) with few variations.Burt (1934) described the pleopod 3 with setae apically and on the peduncle.The specimens analyzed herein had no setae on pleopod 3, which agree with Stephensen (1935) and Shoemaker (1936) material.Morino (2013) described the peduncle of pleopod 3 with 1 robust sub-apical seta and 3 plumose apical setae in the reduced ramus.A variation in this character is shown by illustrations containing two robust setae on the peduncle and 1 plumose apical seta on the ramus (Morino, 2013).The number of setae can also vary on uropods.Richardson (1991) described peduncle of uropod 3 with 2 robust setae.Morino (2013) also found 2 robust setae on uropod 3, having noticed only two females with 3 robust setae.In the present study most individuals presented uropod 3 peduncle with 3 robust setae, agreeing with descriptions of other authors (Burt, 1934;Stephensen, 1935;Shoemaker, 1936;Hurley, 1955).Only few juveniles and young females had 2 robust setae.Morino (2013) described a dactylar dentition on pereopod 4 slightly weaker than that of T. alluaudi.Brazilian individuals of T. topitotum had no dactylar dentition on pereopod 4, although a slight prominence was noticed in 4 females (MNRJ 24811).However, these individuals were among the largest of the samples, reaching 15 mm.In any case, the dactyl of pereopod 4 is not like T. alluaudi, and this character is an important feature of differentiation between the two species (Tab.2).

discussion
Female/Male Ratio The present study showed that samples were composed of a vast majority of females, with only 6 males (4 from Talitroides alluaudi and 2 from Talitroides topitotum) found in the 51 samples (1787 individuals) analyzed.The small number of males in populations was observed in studies on reproductive biology in T. topitotum at Serra do Mar (Lopes and Masunari, 2004b;Matavelli et al., 2009).Alvarez et al. (2000), also studied the reproductive biology of T. topitotum from Mexico and found that this species reproduced all year around, and noticed a female biased sex ratio in every sample with a maximum of 4:1 in May.

Talitroides from Brazilian rain forest
Nauplius, 24: e2016002 Table 2. Morphological differences between T. alluaudi (Chevreux, 1896) and T. topitotum (Burt, 1934) based on literature and observed material.Comparison between T. alluaudi and T. topitotum Based on the literature and observed material o f T. alluaudi and T. topitotum, some distinguishing characters were selected between these species (Tab.2).Characters 9 (posterodorsal setae of peduncle of uropod 2) and 12 (presence/absence medial line of telson) of table 2 are established in this study and should be considered in future taxonomic works.Other characters were discussed and compared with the observed material.Besides, the presence of a distal point on the inner plate of maxilla 2 noticed in T. alluaudi by Morino and Ortal (1993) was also observed in T. topitotum and should not be used as a distinguishing character between these species.
Talitroides alluaudi and T. topitotum have been recorded for the first time for the states of Rio de Janeiro and São Paulo about 40 years ago (Lemos de Castro, 1972;Lemos de Castro and Pereira, 1978).Later on, Lopes and Masunari (2004a;2004b) studied the reproductive biology and distribution of T. topitotum, where 2191 specimens were found in a one year collection (1985 -1986) between two altitudes 270 m and 720 m around the Guaricana Hydroelectric Usine, at Serra do Mar, state of Paraná.Eutrópio and Krohling (2013) recorded T. topitotum from coffee and Eucalyptus plantations in the state of Espírito Santo.Considering these previous records and from data of the present study, T. topitotum seems to be the dominant species in our forests and silviculture areas.From the 1787 individuals analyzed (51 samples) and deposited in the Museu Nacional, 94% were identified as T. topitotum.Talitroides alluaudi appeared in only 3 samples respectively from Rio de Janeiro (RJ), São Paulo (SP) and Rio Grande do Sul (RS), representing 6% of the total number of analyzed individuals.Also, T. topitotum showed high abundance within some samples (up to 201 specimens), indicating that this is a well-established species.On the other hand, T. alluaudi appeared in a very low abundance indicating the need of more sampling in the area to a better understanding of its establishment in the region.
Several studies indicate that T. topitotum can become a successful established species after introduction, even displacing native species (Biernbaum, 1980;Friend and Lam, 1985;Richardson, 1992).Richardson (1992) noticed in Hawaii that no terrestrial talitrids occurred in the lowest dry part of transects studied and the first species to appear in leaf litter of forests (guava in about 300 m) were T. topitotum and T. alluaudi, the latter being less common.This author suggested the possibility that native species have been displaced by invasive species of the genus Talitroides.Richardson (1992) also concluded based on the reach of Talitroides spp. in drier habitats of lower altitude, that these species may have better desiccation tolerance and more easily be able to get moist refuges than native species.Talitroides topitotum and T. alluaudi have also been found in Hawaiian caves in sympatry with native species (Bousfield and Howarth, 1976).

acknowledgeMents
We would like to thank Dr. Georgina Buckup (UFRGS) and Dr. Paula Araújo (UFRGS) for collecting and making available the loan of the Talitridae collection for the present study.The first author thanks FAPERJ (Fundação de Amparo a Pesquisa do Estado do Rio de Janeiro) for an undergraduate grant process no.E-26/102.340/2011.