Brazilian species of Onychophora with notes on their taxonomy and distribution

A revision of the currently known distribution of Onychophora (velvet worms) in Brazil is presented. Twentyfour morphospecies (half of them undescribed) belonging to four genera of the Peripatidae (Peripatus Guilding, 1826, Epiperipatus Clark, 1913, Macroperipatus Clark, 1913 and Oroperipatus Cockerell, 1908) are recorded. This high number of “unidentified” morphospecies is due to three major reasons: the poor quality of the characters used in species-level identification, the inadequate specimen conservation in ethanol, and, in most cases, the lack of additional specimens for analysis of intraand inter-specific variation. The morphological characters currently used to separate Peripatidae species present a large degree of variation and may not be sufficient to allow accurate identification. There are records of these animals from 16 states, located in four political regions of the country (North, Center-West, Northeast and Southeast). Oroperipatus balzani is recorded for the first time from Brazil. The southernmost record for Onychophora is Itacuruçá island, Mangaratiba, Rio de Janeiro State (E. edwardsii) and the northernmost is Vila Tepequém, Amajari, Roraima State (Epiperipatus sp. 4). Considering the large territorial area of Brazil and the paucity of localities where Onychophora have been collected, we may expect a total diversity of these animals much larger than the currently known one.

ABSTRACT.A revision of the currently known distribution of Onychophora (velvet worms) in Brazil is presented.Twentyfour morphospecies (half of them undescribed) belonging to four genera of the Peripatidae (Peripatus Guilding, 1826, Epiperipatus Clark, 1913, Macroperipatus Clark, 1913and Oroperipatus Cockerell, 1908) are recorded.This high number of "unidentified" morphospecies is due to three major reasons: the poor quality of the characters used in species-level identification, the inadequate specimen conservation in ethanol, and, in most cases, the lack of additional specimens for analysis of intra-and inter-specific variation.The morphological characters currently used to separate Peripatidae species present a large degree of variation and may not be sufficient to allow accurate identification.There are records of these animals from 16 states, located in four political regions of the country (North, Center-West, Northeast and Southeast).Oroperipatus balzani is recorded for the first time from Brazil.The southernmost record for Onychophora is Itacuruçá island, Mangaratiba, Rio de Janeiro State (E.edwardsii) and the northernmost is Vila Tepequém, Amajari, Roraima State (Epiperipatus sp.4).Considering the large territorial area of Brazil and the paucity of localities where Onychophora have been collected, we may expect a total diversity of these animals much larger than the currently known one.KEY WORDS.Brazil; distribution; Peripatidae; taxonomy; velvet worm.
ZOOLOGIA 26 (3): 553-561, September, 2009 cas.Soon after, CLARK (1915) discussed and presented a list of hitherto known records of the species of Peripatidae and Peripatopsidae from all over the world.BRUES (1923) published the first map summarizing the geographical distribution of Onychophora throughout the world.Besides a general world map, he elaborated maps depicting the distribution of Onychophora in Australia, West Indies, Africa, South and Central America.Although, this publication analyzed only the distribution of the families and genera, but did not present a detailed list of species and their records.MARCUS (1937) described a new species, Peripatus (Epiperipatus) evelinae Marcus, 1937, from central Brazil.The new species presented a large number of lobopodes (32 and 34), an unseen characteristic in Brazilian velvet worms at that time.Four years later, CARVALHO (1941) described Peripatus (Peripatus) heloisae Carvalho, 1941, from Mato Grosso, also from central Brazil.This species has a distinctive white spot on the head.CARVALHO (1942) added new external and internal features for P. heloisae, based on more than 600 additional specimens he collected.MARCUS & MARCUS (1955) described a new species, Peripatus acacioi Marcus & Marcus, 1955, from Tripuí, in the vicinities of the city of Ouro Preto, state of Minas Gerais, also in Brazil.The shape of the cuticular papillae from the new species is similar to P. ohausi, however both species differ in color and presence of accessory teeth.
The first revisionary paper on Brazilian Onychophora was published by FROEHLICH (1968).He studied a small collection of Onychophora from the former Departamento de Zoologia, Faculdade de Filosofia, Universidade de São Paulo, Brasil.Comments on three species (M.acacioi, P. evelinae and E. edwardsii) were given, and a new species, Peripatus tucupi Froehlich, 1968, was described from the state of Pará.
The last summary of the Onychophora distribution was published by PECK (1975), but limited to the Neotropical region.In that paper, he described a new genus and gave a revised and updated version of the key to American genera of Onychophora of BOUVIER (1905), including the taxa proposed by Clark and himself.He cited nine species, belonging to four genera, collected in 14 different localities from Brazil.
Most papers on Brazilian Onychophora in the last decades dealt with biology and physiology of M. acacioi (e.g., CAMPIGLIA & LAVALLARD 1973, LAVALLARD & CAMPIGLIA 1973).Only after the beginning of the current century, studies on taxonomy and distribution of velvet worms began to be published again in Brazil. VASCONCELLOS et al. (2004)  Notwithstanding the above-cited papers, there is no comprehensive paper on the currently known geographical distribution of Onychophora in Brazil.This study presents a species list of Brazilian velvet worms, based on literature, museum specimens and firsthand records.Besides, some characters used in the identification of velvet worms are reexamined and the currently known distribution of Brazilian Onychophora is analyzed.

MATERIAL AND METHODS
The list below is based on the literature and the analysis of 798 specimens deposited at the following institutions (acronyms and curators given between brackets): Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro (MNRJ, A. B. Kury); Museu de Zoologia, Universidade de São Paulo, São Paulo (MZSP, R. Pinto-da-Rocha); Instituto Butantan, São Paulo (IBSP, A. D. Brescovit); and Departamento de Zoologia, Universidade Federal de Minas Gerais, Belo Horizonte (DZUFMG, A. Wieloch).The identification of the specimens follows BOUVIER (1905) for the most part, except for the species described after the publication of this revisionary paper.The generic classification used in the species list follows PECK (1975).Species records marked by an asterisk (*) are those of specimens that were not examined; all information for them are derived from, the literature.Data on localities (distribution section) were gathered from the gazetteers and locality directory of the Falling Rain internet site (http://www.fallingrain.com/world/).The locality record for each specimen was included in a database and afterwards exported to ARC-GIS for map elaboration.
Specimens examined: only types.Distribution: "Cerrado" areas (dry, open savannas) in the border of Minas Gerais and Goiás states.
Peripatus heloisae Carvalho, 1941 (  Epiperipatus edwardsii (Blanchard, 1847) (Fig. 3) Remarks: the only specimen known from Itacuruçá, Rio de Janeiro, is dubiously included in E. edwardsii.It is in bad state, and we have not been able to find any character to separate it from the other specimens of E. edwardsii.
Distribution: Venezuela and Brazil (Pará* and Rio de Janeiro states).
Remarks: the two specimens from Barra de São João are very similar to the redescription and illustration of the type of E. simoni presented by BOUVIER (1905).These two specimens have been dubiously included in E. simoni, but they differ in minor details as the presence or absence of frontal organs and the number of small papillae between the primary papilla basis (PPB).The specimens from Barra de São João do not present frontal organs and have 1-7 small papillae between the PPB, whereas E. simoni presents frontal organs and 1-4 small papillae between the PPB, which may prove to be of specific value following further studies.lozenges etc.) over and around the median dorsal line.The pattern of light lozenges over a darker background is found in at least three Epiperipatus species (E.trinidadensis (Sedgwick, 1888), E. broadwayi (Clark, 1913) and E. edwardsii) and also in M. acacioi.In contrast, the lozenges are not clearly seen in some E. edwardsii specimens from Espírito Santo State, and may even not be noticed at all.Most Brazilian Onychophora have brownish to purple-brown hues, often presenting a darker, thin, stripe over the median dorsal line.P. heloisae bears a contrasting whitish spot just behind the head.

Epiperipatus tucupi Froehlich, 1968
Among the nine Epiperipatus morphospecies we found, E. edwardsii and E. brasiliensis are easily identified.We were not able to examine any E. imthurmi specimen.Regarding the other Epiperipatus morphospecies, the analysis of the outer morphological characters were not enough to allow an accurate identification.For example, Epiperipatus sp. 5 has the leg number and irregular papillae disposition found in E. imthurmi, but it differs in coloration.Epiperipatus sp. 5 is dark purple, whereas E. imthurmi may present colors varying from orange to brown.
The only "unidentified" morphospecies of Macroperipatus seems to be close to M. ohausi, but it is found only in Pernambuco State, northeastern Brazil, while M. ohausi is known only from Rio de Janeiro State, southeastern Brazil.Both species present jaw blades with an inner accessory tooth and well-developed frontal organs.Macroperipatus sp. 1, though, displays a row of 11 teeth placed after the accessory tooth of the inner jaw, absence of secondary papillae placed laterally to the primary ones, and 30 pairs of legs, contrasting to the 10 teeth, presence of such secondary papillae and 27-28 pairs of legs found in M. ohausi (after BOUVIER 1905).Summing up, the gap found in the morphological characters and the distance between localities indicate that M. ohausi and Macroperipatus sp. 1 are probably distinct species.
As shown above, the morphological characters currently used to separate Peripatidae species present a large degree of variation and may not be sufficient to allow accurate identification.The use of characters of inner structures, as number of teeth in the jaws, and SEM may yield good results when applied to Brazilian Onychophora, as has been noticed by READ (1988 a, b) and MAYER (2007) in other countries.
Most papers on the distribution of Onychophora are worldwide-based, and do not present detailed records for each country.Considering Brazilian Onychophora, most records are restricted to the description of species.Also, many new records have been presented in abstracts of zoology meetings, including new but invalid scientific names.
During our studies, we examined specimens of velvet worms from twelve of the thirteen Brazilian states already cited in the literature (Amazonas, Pará, Ceará, Pernambuco, Alagoas, Bahia, Tocantins, Goiás, Mato Grosso, Minas Gerais, Espírito Santo and Rio de Janeiro).The exception is Paraíba, as we have not been able to examine upon any specimen from it.Besides, we added first-time records for three states (Roraima, Acre and Maranhão) and 27 new localities from Brazil.Summing up, Onychophora are currently known from 16 states, from all Brazilian regions, except the South.The southernmost record for Onychophora is Itacuruçá island, Mangaratiba, Rio de Janeiro State (E.edwardsii) and the northernmost is Vila Tepequém, Amajari, Roraima State (Epiperipatus sp.4) (Fig. 9).
Most described Brazilian species are certainly endemic, as they are known only from their type-locality (e.g., E. tucupi, M. acacioi, M. ohausi, M. machadoi and P. evelinae).Some species are known from just one additional collection outside the type-locality (e.g., P. heloisae, O. eiseni and O. balzani), but others have what seems to be wide distributions (e.g., E. edwardsii, E. simoni and E. brasiliensis).Epiperipatus edwardsii is the most widespread species in Brazil, but most records are from Pará and Espírito Santo states.
Species of Oroperipatus are known only from the state of Acre, northwestern Brazil.Macroperipatus spp.are found in several southeastern states and also from an isolated record from Pernambuco, northeastern Brazil.In contrast, species of Epiperipatus and Peripatus are found on a wide geographical area covering most states in Brazil (Fig. 9).
The 24 here recognized morphospecies of Peripatidae represent a substantial increase over the 11 species cited by OLIVEIRA &WIELOCH (2005) andSANTANA et al. (2008).Also, the known distribution of velvet worms now covers most Brazilian states, with the exception of the South region.Considering the large territorial area of Brazil and the paucity of localities where Onychophora have been collected, we may expect a total diversity of these animals much larger than the currently known one.
As we pointed out before, the method of preservation of the specimens exerts a large effect over the characters currently used in Peripatidae taxonomy.Most specimens kept in museums do not allow a precise identification but they are still useful as mementos of the distribution of velvet worms and pinpoints for future collection.Taking in consideration the apparently limited capacity of dispersal of most velvet worms, additional collection effort is badly needed, as many of the old localities are under intense human pressure and extinction looms at the corner.
recorded specimens of three Peripatus spp.(possibly new) for the first time from the states of Pernambuco and Alagoas.OLIVEIRA & WIELOCH (2005) described a new species of Macroperipatus, M. machadoi Oliveira & Wieloch, 2005, from the state of Minas Gerais.VASCONCELLOS et al. (2006) recorded Onychophora species from the Atlantic Rainforest in four states from northeast Brazil (Ceará, Pernambuco, Alagoas and Bahia).The specimens were identified only to the generic level.Later, SANTANA et al. (2008) added the first record of Onychophora from the state of Paraíba, north-eastern Brazil, represented by one specimen collected in the Atlantic Rainforest.