Miranda ZA 2018.Pdf

Zoologischer Anzeiger 273 (2018) 33–55

Contents lists available at ScienceDirect

Zoologischer Anzeiger

jou rnal homepage: www.elsevier.com/locate/jcz

Review of Trichodamon Mello-Leitão 1935 and phylogenetic

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placement of the genus in Phrynichidae (Arachnida, Amblypygi)

a,b,c,∗ a

Gustavo Silva de Miranda , Adriano Brilhante Kury ,

a,d

Alessandro Ponce de Leão Giupponi

Laboratório de Aracnologia, Museu Nacional do Rio de Janeiro, Universidade Federal do Rio de Janeiro, Quinta da Boa Vista s/n, São Cristóvão, Rio de

Janeiro-RJ, CEP 20940-040, Brazil

Entomology Department, National Museum of Natural History, Smithsonian Institution, 10th St. & Constitution Ave NW, Washington, DC, 20560, USA

Center for Macroecology, Evolution and Climate, Natural History Museum of Denmark (Zoological Museum), University of Copenhagen,

Universitetsparken 15, 2100, Copenhagen, Denmark

Servic¸ o de Referência Nacional em Vetores das Riquetsioses (LIRN), Colec¸ ão de Artrópodes Vetores Ápteros de Importância em Saúde das Comunidades

(CAVAISC), IOC-FIOCRUZ, Manguinhos, 21040360, Rio de Janeiro, RJ, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Amblypygi Thorell, 1883 has ﬁve families, of which Phrynichidae is one of the most diverse and with a

Received 18 October 2017

wide geographic distribution. The genera of this family inhabit mostly Africa, India and Southeast Asia,

Received in revised form 27 February 2018

with one genus known from the Neotropics, Trichodamon Mello-Leitão, 1935. Trichodamon has two valid

Accepted 28 February 2018

species, T. princeps Mello-Leitão, 1935 and T. froesi Mello-Leitão, 1940 which are found in Brazil, in the

Available online 10 March 2018

states of Bahia, Goiás, Minas Gerais and Rio Grande do Norte. The boundaries of the species are not

Corresponding Editor: Gabriele B Uhl

well established and the characters classically used in the group are poorly deﬁned. The relationship of

Trichodamon to the other genera in the family is also subject to debate. Some phylogenetic hypotheses

Keywords:

propose Trichodamon as sister to Eurphynichus Weygoldt, 1995 and Phrynichus Karsch, 1879, in the sub-

Whip spider

Neotropics family Phrynichinae. Others suggest Trichodamon in Damoninae, sister to Damon and Phrynichodamon

Amblypygi systematics Weygoldt, 1996. The present work has the aim to characterize Trichodamon species, update the species

Phylogeny distribution and ascertain the phylogenetic position of the genus in Phrynichidae using morphologi-

Taxonomy cal characters. Our results show that the diagnostic characters of Trichodamon species, i.e. number of

spines on the pedipalp, shape of the frontal process, number of teeth on the chelicerae, male and female

shape of gonopods, are highly variable. A gradual colour variation from the northern to the southern

areas of the distribution is also present. In face of the high variability, the synonymy of Trichodamon

froesi (syn. jun.) with T. princeps is suggested. The cladistic analysis recovered Trichodamon as sister to

Phrynichus + Euphrynichus in the subfamily Phrynichinae supported by eight characters, one exclusive to

the group (dorsal spines on pedipalp patella positioned on the apex of the article forming the phrynich

hand). In Damoninae, Phrynichodamon Weygoldt, 1996 was found as sister to Damon, forming the tribe

Damonini, a group supported by the number of ventral spines on pedipalp femur; Musicodamon was

recovered as sister to Damonini, forming the subfamily Damoninae, and the clade can be recognized

by the presence of sclerotization on the apex of the claw-like projection of the female gonopod. The

unranked taxon Euphrynichida Weygoldt, 2000 (Phrynichinae + Damoninae) was recovered with good

support and is identiﬁed by the rectangular shape of the female gonopod and by the presence of one

spine on the proximal series on pedipalp femur.

Contents

1. Introduction ...... 34

2. Material and methods ...... 35

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This article is part of a special issue entitled “In honor of Peter Weygoldt”, published in the Journal Zoologischer Anzeiger 273, 2018.

∗

Corresponding author at: Entomology Department, National Museum of Natural History, Smithsonian Institution, 10th St. & Constitution Ave NW, Washington, DC, 20560,

USA.

E-mail address: [email protected] (G.S. de Miranda).

https://doi.org/10.1016/j.jcz.2018.02.006

34 G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55

2.1. Cladistic analysis ...... 35

2.1.1. Taxon sampling ...... 35

2.1.2. Morphological phylogenetic analysis (ew, iw) ...... 36

2.1.3. Optimization, support and resampling ...... 36

3. Results and discussion ...... 36

3.1. Variation in non-genital characters in Trichodamon ...... 36

3.1.1. Chelicerae...... 36

3.1.2. Frontal process ...... 36

3.1.3. Pedipalp spines ...... 36

3.1.4. Size ratio of the carapace ...... 39

3.2. Variability of the gonopod of Trichodamon ...... 39

3.2.1. Spermatophore organ (male genitalia)...... 39

3.2.2. Female genitalia ...... 40

3.3. Description of Trichodamon ...... 41

3.4. Distribution...... 47

3.5. Cladistic analysis ...... 48

4. Discussion ...... 49

Acknowledgments ...... 51

Appendix A. Character list ...... 51

Appendix B. Supplementary data...... 54

References ...... 54

1. Introduction 2017; Prendini et al., 2005), so the position of the genus within

Phrynichidae is still contentious.

Whip spiders (order Amblypygi) are unique animals with ﬂat The ﬁrst record of Phrynichidae species from South America

bodies, strong spiny pedipalps, and an extremely elongate ﬁrst was the description of Trichodamon princeps Mello-Leitão, 1935

pair of legs (Weygoldt, 2000a). The order includes ﬁve fami- from Goiás, Brazil. Mello-Leitão (1936) also described T. pusil-

lies, of which Phrynichidae is the third largest with 35 species lus Mello-Leitão, 1936, from Goiás, which was later synonymised

(after Charinidae and Phrynidae). There has been large advances with T. princeps Mello-Leitão (1940). Mello-Leitão (1940) added yet

in the understanding of phrynichid reproductive biology and sper- another species to Trichodamon with the description of T. froesi from

matophore morphology (Weygoldt, 1977c, 1997, 1999c, 2002c,b, the state of Bahia. Previously, other Phrynichid species were erro-

2003; Weygoldt and Hoffmann, 1995), behaviour (Weygoldt, neously assigned as occurring in South America, such as Damon

2002c, 2008, 2009), post embryonic development (Weygoldt, variegatus (Perty, 1834) (thought to be from somewhere near the

1977b, 1995), taxonomy (Weygoldt, 1998, 1999b, 2000b, 2008) and Amazon river), Damon australis Simon, 1886 (now Damon johnstonii

systematics (Prendini et al., 2005; Weygoldt, 1996b, 1999a) which (Pocock, 1894), once considered as from Patagonia), and Damon

led to an unprecedented understanding of the family’s life history medius (Herbst, 1797) (once reported from the America) (Koch,

and character ontology. However, this knowledge was not evenly 1841; Weygoldt, 1999b).

distributed among all seven genera of Phrynichidae. Quintero (1976) raised the subfamily Damoninae to family level

Phrynichids seems to be well adapted to the dry environments and transferred the genera Damon, Musicodamon and Trichoda-

of most parts of Africa and the Arabian Peninsula (Weygoldt, 1998, mon to Damonidae. The family Damonidae, however, is no longer

1999b). Among the phrynichid genera, Musicodamon Fage, 1939, considered a valid family (Harvey, 2003; Weygoldt, 1996a). Fur-

Phrynichodamon Weygoldt, 1996a,b and Xerophrynus Fage, 1951 are ther, Quintero (1976) made new records of T. froesi and illustrated

monotypic; the ﬁrst genus is know from a few localities in Morocco characters of the species. Weygoldt (1977c) analysed the post-

and Algeria; the second has only two published records in South embryonic growth of T. froesi and commented on the relationship of

Africa; and the third genus is recorded from two localities, one Trichodamon with the other genera of the family. Weygoldt (1977b)

in Angola and one in Namibia. The genus Euphrynichus Weygoldt, studied the agonistic and mating behaviour, the spermatophore

1995 includes two species restricted to the east coast of Africa (Tan- and female gonopod morphology of females of T. froesi; the study

zania and Kenya) and Madagascar. The genus Damon Koch, 1859 provided more details of the female gonopod than Quintero (1976)

includes 11 species in 23 (more than 40% of the) African coun- and described the spermatophore of the male for the ﬁrst time.

tries. The genus Phrynichus Karsch, 1879 is the most specious and Since then, no detailed taxonomic or morphologic work has been

with the widest distribution in Phrynichidae. The 17 valid species conducted on Trichodamon; the genus and its species were only

can be found in Southeast Asia, India, Sri Lanka, Arabian Peninsula, discussed in the broader context of Phrynichidae phylogeny (not

Seychelles Islands, Mauritius Islands, Madagascar and ten African always being included in the analysis), as in Weygoldt (1996b),

countries (Fig. 1). In contrast, the genus Trichodamon Mello-Leitão, Weygoldt (2002c), Prendini et al. (2005) and Weygoldt (2008).

1935 is the only phrynichid that inhabits the Neotropics, with two In most arthropods, the genitalia are the most reliable source

endemic species on the Brazilian dry lands (Caatinga; Fig. 1). of characters for species’ identiﬁcation. Individuals with similar

Despite the interesting disjunct distribution, the taxonomy, non-genital characters, but with different genitalia are usually con-

phylogenetic position and biogeography of Trichodamon has been sidered different species (Eberhard, 2004; Hosken and Stockley,

hardly investigated. The genus has been proposed as either sister to 2004). The genital and other structures of sexual contact often

Phrynichus and Euphrynichus, forming the subfamily Phrynichinae evolve faster than other morphological characters because of sex-

(Weygoldt, 1995, 1996a, b, 1999b,c, 2000b,a), or sister to Musi- ual selection (Eberhard, 1985, 2004; Hosken and Stockley, 2004;

codamon + Damon inside the clade Damoninae (Weygoldt, 2008). Huber, 2003). Moreover, morphometric analysis of various insect

However, Trichodamon has not been incorporated into recent whip and spider species supported the perception that the genitalia

spider phylogenetic analysis (Esposito et al., 2015; Garwood et al., varies intraspeciﬁcally less than non-genital characters (Eberhard

G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55 35

Fig. 1. Distributional map of all Phrynichidae genera.

et al., 1998). This rapid modiﬁcation of external traits, combined Digital photographs were taken with a Sony Cybershot DSC-

with shape homogeneity of the genitalia in a population, explains V1 and MotiCam 5MP attached to the microscope. Images were

the importance of the genitalia in determining species (Huber, mounted with CombineZP (Hadley, 2011) and edited for brightness

2004; Huber et al., 2005; Tatsuta et al., 2001). and contrast in Adobe Photoshop CS6 (Adobe Systems Inc., San Jose,

Intraspeciﬁc variation is often higher in males than in females, CA). The scanning electron microscopy (SEM) images were gener-

which suggests that males are subject to cryptic female choice ated in a JEOL JSM-6390LV at the Centro de Microscopia Eletrônica

(Hosken and Stockley, 2004). However, variation is also found in de Varredura do Museu Nacional. The structures analysed with SEM

females, such as the size and the genitalia in spiders (Lucas and were dissected under microscope, cleaned with ultrasound, dried

Bücherl, 1965; Pérez-Miles, 1989). In whip spiders, there are only in critical point, mounted in stubs and gold coating.

two reports of female genitalia variation (in the shape and size of The map was created using ArcGis 10 (ESRI, 2014). Locations

the soft part): one in Phrynichus orientalis Weygoldt, 1998 and one of Trichodamon were obtained from vial labels. Those without

in P. exophthalmus Whittick, 1940 (Weygoldt, 1998). The limited coordinates were georeferenced in the data bank GeoNames

number of records of intraspeciﬁc variation in males and females (2013). Localities and coordinates of the other Phrynichid genera

of arachnids may result from the fact that species descriptions are and species were taken from Bastawade et al. (2005), Blick and

often based on the few specimens available (Huber, 2003). Seiter (2016), Fage (1939), Gouvêa (1993), Maquart et al. (2016),

Here, a large number of specimens from different localities Weygoldt (1996b, 1998, 1999b, 2003, 2008, 2009), Weygoldt et al.

within the distribution range of Trichodamon species were stud- (2002), Weygoldt and Hoffmann (1995) and Huber (pers. com.).

ied and the morphological diversity within the genus was explored

and discussed. The phylogenetic position of Trichodamon was 2.1. Cladistic analysis

investigated with a cladistic analysis of Phrynichidae using 100

morphological characters and 18 terminal taxa (nine ingroup and 2.1.1. Taxon sampling

nine outgroup). A morphological phylogenetic analysis was performed using

100 somatic characters and 18 terminal taxa (nine ingroup and

nine outgroup, see Table 1) with the aim to ﬁnd the best relation-

ship hypothesis of Trichodamon within the family Phrynichidae. At

2. Material and methods least one species of each phrynichid genus was included (Table 1).

Members of all other families of Amblypygi were used as outgroups

For nomenclature and measurements, the methods of Quintero (Charinidae, Charontidae, Paracharontidae and Phrynidae) and the

(1981) were followed. The terminology of pedipalp and leg seg- tree was rooted in Paracharon caecus, following Weygoldt (1996a)

ments followed Harvey and West (1998). Measurements of the and Garwood et al. (2017).

articles of the pedipalp were made between the external condyles The following institutions provided specimens to this study:

of each segment, as illustrated by Baptista and Giupponi (2002). AMNH American Museum of Natural History (New York,

Terminology of the male gonopod parts followed Giupponi and Lorenzo Prendini);

Kury (2013). Figure scales and abbreviations are indicated in their CHNUFPI Colec¸ ão de História Natural da Universidade Federal

respective legend of the ﬁgures. do Piauí (Floriano, Leonardo Sousa Carvalho);

Specimens were examined under a Leica, Olympus and Wild IBSP Instituto Butantan (São Paulo, Antonio Brescovit);

Heerbrug M8 microscopes (the latter attached to a camera lucida) ISLA Colec¸ ão de Invertebrados Subterrâneos de Lavras, Univer-

and a Nikon Eclipse E200 compound microscope. Drawings were sidade Federal de Lavras (Lavras, Rodrigo Lopes Ferreira);

done with a Wild Heerbrug M8 microscope attached to a camera MCZ Museum of Comparative Zoology (Cambridge, Gonzalo

lucida. Drawings were made with China ink or Corel Draw X5. Giribet);

36 G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55

Table 1

to 50 to ﬁnd the upper limit of supports. Subsequently, the subopti-

List of amblypygid taxa included in the cladistic analysis.

mal was increased stepwise by 1 up to 20 and so was the tree buffer

Repository number by 5000 for 20 cycles (Frick and Scharff, 2014). For the jackknife

support (JK; Farris et al. (1996)), 1000 jackknife pseudoreplicates of

Ingroup taxa

Damon annulatipes (Wood, 1869) ZMUC 42400 100 random sequence additions were performed, keeping 10 trees

Damon diadema (Simon, 1876) ZMUC 20672 each using TBR as swapping algorithm (Cabra-García and Brescovit,

Damon variegatus (Perty, 1834) ZMUC 20662

2016). A probability of elimination P = 0.36 was used. Symmetrical

Euphrinichus amanica (Werner, 1936) ZMUC 21590

resampling was calculated as for Jackknife support and the results

Musicodamon atlanteus Fage, 1939 MNHN

are reported in differences of group frequency values (GC) (Goloboff

Phrynichodamon scullyi (Purcell, 1902) SMNS

Phrynichus orientalis Weygoldt, 1998 AMNH Ambly 47 et al., 2003).

Trichodamon princeps Mello-Leitão, 1935 MNRJ

The characters were studied and optimized, and trees edited

Xerophrynus machadoi (Fage, 1951) SMNS

in WinClada 10.00.08 (Nixon, 2002). Ambiguous character opti-

Outgroup taxa

mizations were resolved so as to favour reversal or secondary loss

Catageus (former Stygophrynus; see Miranda et al. (2018)) ZMUC

Charinus dominicanus Armas and González, 2002 AMNH GSM 94 over convergence (ACCTRAN or Fast Optimization) (Farris, 1970;

Charinus a. elegans Weygoldt, 2006 MNHN (paratype) Swofford and Maddison, 1987).

Charon grayi (Gervais, 1842) MZUF 1108

Heterophrynus armiger Pocock, 1902 MCZ 39233

3. Results and discussion

Paracharon caecus Hansen, 1921 ZMUC

Paraphrynus raptator (Pocock, 1902) AMNH GSM 39

Sarax singaporae Gravely, 1911 SMF 64594 3.1. Variation in non-genital characters in Trichodamon

Sarax yayukae Rahmadi, Harvey and Kojima, 2010 AMNH LP 12119

Mello-Leitão (1940) and Quintero (1976) deﬁned Trichodamon

and its species based on characters of the chelicerae, pedipalp, cara-

MNHN Muséum National d’Histoire Naturelle (Paris, Mark Jud-

pace and colour, all of which are revaluated here.

son);

MNRJ Museu Nacional do Rio de Janeiro, Universidade Federal

3.1.1. Chelicerae

do Rio de Janeiro (Rio de Janeiro, Adriano B. Kury);

Trichodamon princeps and T. froesi were diagnosed by Mello-

MZUF Museo Zoologico “La Specola” (Firenze, Sarah Whitman);

Leitão (1940) as having four and three teeth on the cheliceral claw,

MZUSP Museu de Zoologia da Universidade de São Paulo (São

respectively (Fig. 2). He also described the shape of the middle

Paulo, Ricardo Pinto da Rocha);

tooth on the basal segment of the chelicerae as with wide base

SMF Senckenberg Museum für Naturkunde Görlitz (Frankfurt,

in T. princeps and with narrow base in T. froesi (Fig. 2).

Peter Jäger);

The chelicerae of several non-type specimens were analysed

SMNS State Museum of Natural History Stuttgart (Stuttgart,

(most specimens under material examined), of which 14 can be

Joachim Holstein);

seen in Fig. 3A–N; they were organized in latitudinal order, from

UFBA Universidade Federal da Bahia (Salvador, Rejane Sat-

the northernmost to the southernmost known record of the genus

urnino);

(Fig. 3A–N, respectively).

UFMG Universidade Federal de Minas Gerais (Belo Horizonte,

All non-type cheliceral claws analysed had four teeth, the distal

Adalberto José Santos);

one smaller in some specimens or larger in others (e.g. Fig. 3A, K,

UFSCAR Universidade Federal de São Carlos (São Carlos, Maria

respectively). The widening (or its absence) of the middle tooth on

Elina Bichuette);

the basal segment was observed regardless of the locality of the

ZMUC Zoological Museum, University of Copenhagen (Copen-

specimen and shape of the female genitalia (e.g., absent: Fig. 3A,

hagen, Nikolaj Scharff).

C; present: Fig. 3G, I, J). Contrary to what was presented by Mello-

Leitão (1940), the type series of T. princeps have the median teeth

2.1.2. Morphological phylogenetic analysis (ew, iw)

with a narrow base (Fig. 2D) and the type specimens of T. froesi

The morphological matrix was built in Mesquite v. 3.2

have the teeth with a wide base (Fig. 2F). Different states of the

(Maddison and Maddison, 2017). The logical character structure

same characters were also found in specimens of the same locality

nomenclature proposed by Sereno (2007) was followed. Parsi-

(Fig. 3A–C). Additionally, the different character states were equally

mony analyses were performed in TNT v.1.1 (Goloboff et al., 2008),

found in males and females. Taken together, dentition was not a

using heuristic methods (“traditional search”) under both equal and

good diagnostic character within Trichodamon.

implied weights. Tree bisection-reconnection (TBR) and the follow-

ing setting for starting trees (mult = tbr replic 1000 hold 1000;)

3.1.2. Frontal process

were used. Branches with no possible support were collapsed

The frontal process is a small projection in the frontal region

(collapsing “rule 3”) during and after the tree search (collapse

of the carapace, placed below the median eye tubercle (Fig. 2G–J).

1; collapse [;). All characters were unordered and the 29 multi-

This region varied greatly in shape and number of tubercles among

state characters were treated as non-additive (Fitch, 1971). The

different Trichodamon conspeciﬁcs (Fig. 2G–J). The frontal process

searches under implied weighting (iw) were run with the same

was analysed for all specimens here studied, but no morphological

search parameters as used for the equal weights analysis, and with

pattern was found. Despite being useful for the taxonomy in some

the concavity constant (k) set to 1–500 (piwe = 1; mult = tbr replic

species of Charinidae (Pinto-da-Rocha et al., 2002) and Phrynichi-

1000 hold 1000;). Implied weighting in TNT weights the characters

dae (Weygoldt, 1998), the frontal process in Trichodamon does not

according to a concave function of homoplasy (k) which is set by

seem to be a good character to distinguish species.

the user and negatively correlates with how strongly homoplastic

characters are down-weighted (Goloboff, 1993).

3.1.3. Pedipalp spines

Similar to other phrynichids, the pedipalp spines of Trichodamon

2.1.3. Optimization, support and resampling undergo a series of ontogenetic changes, as shown by Weygoldt

TNT was also used to calculate support values for trees. For the (1977b). Juveniles generally have six dorsal and six ventral spines

Bremer support values, (BS; Bremer (1988, 1994)) a batch ﬁle was on the femur, while adults have ﬁve dorsal and three ventral spines

built with a script for a rough precedent search setting suboptimal (Fig. 4A, D). On the patella, juveniles have three large dorsal spines

G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55 37

Fig. 2. Details of the chelicerae and frontal process (A, B: MNRJ 9114; C, D and E, F: type specimens of T. princeps and T. froesi, respectively). A. Teeth of the basal segment,

inner view of the left chelicerae. B. General view of the chelicerae, ectal view. C. Chelieral claw of T. princeps, ectal view. D. Basal segment of the chelicera of T. princeps, mesal

view. E. Cheliceral claw of T. froesi, ectal view. F. Basal segment of the chelicera of T. froesi, mesal view. G. Frontal process of T. princeps, lateral view. H. Frontal process of T.

princpes, dorsal view. I. Frontal process of T. froesi, lateral view. J. frontal process of T. froesi, dorsal view. Figures G–J modiﬁed from Mello-Leitão (1940).

38 G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55

Fig. 3. Chelicera of different Trichodamon specimens showing the variation in number of teeth on the claw (left in the rectangles) and shape of the teeth on the basal segment

(right drawing in the rectangles). The specimens are organized from the northernmost record of the distribution to the southern most; note there is no geographical pattern

in the distribution of the characters; sex and measurements of the specimens in Table S2. A. Bahia, Campo Formoso, Toca do Gonc¸ alo (MNRJ 09112). B. Bahia, Campo Formoso,

Toca do Gonc¸ alo (MNRJ 09114). C. Bahia, Campo Formoso, Toca da Tiquara (MNRJ 09179). D. Bahia, Andaraí, Gruta da Paixão (MNRJ 09192). E. Bahia, Elísio Medrado (MNRJ

09191). F. Bahia, Elísio Medrado (MNRJ 09193). G. Bahia, Itaetê, Poc¸ o Encantado (MNRJ 09195). H. Bahia, Itaetê, Gruta Natal (MNRJ 09180). I. Bahia, Itaetê, Poc¸ o Encantado

(MNRJ 09111). J. Bahia, Ituac¸ u (MNRJ 09009). K. Bahia, Santana, Gruta do Padre (MNRJ 09005). L. Bahia, Carinhanha, Lapa dos Peixes (MNRJ 09053). M. Bahia, Carinhanha,

Lapa dos Peixes (MNRJ 09113). N. Minas Gerais, Itacarambi, Gruta Olhos d’Água (MNRJ 09049).

at the distal apex and six ventral decreasing in size (Fig. 4C, D), and The different populations of Trichodamon analysed had the

adults have only two dorsal (spine III is reduced) and one ventral same number of spines on the pedipalp femur and patella. There-

spine (Fig. 4A, B, E, F, G). fore, pedipalp spines are not diagnostic for Trichodamon species.

G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55 39

Fig. 4. Pedipalp of an adult and juvenile male Trichodamon princeps Mello-Leitão, 1935 (A, B: MNRJ 09052; C, D: holotype of T. pusillus Mello-Leitão, 1936; E–G: paratype).

Dark numbers refer to dorsal and gray to ventral spines; only spines of the main seires marked. A. Dorsal view (MNRJ 09052). B. Ventral view (MNRJ 09052). C. Right pedipalp

in ventral view. D. Right pedipalp in dorsal view. E. Dorsal view of tibia and tarsus. F. Retrolateral of tibia and tarsus. G. Ventral view of tibia and tarsus. Scale bars: A, B 0.5 cm;

C-G 1 mm.

However, pedipalp spines, setae and tubercles were essential to as claw-like projections (Weygoldt, 1970, 1999c), but high variabil-

differentiate the families and genera of Amblypygi (see phylogeny ity in the gonopod has not been reported before. Here, we explore

characters 40–63, 66–83). The distalmost dorsal and ventral spines, the shape variation of the male and female genitalia in Trichodamon.

for example, form a raptorial structure that is characteristic for the

family Phrynichidae, the so called phrynichid hand (see phylogeny,

3.2.1. Spermatophore organ (male genitalia)

character 73) (Weygoldt, 1995).

Kraus (1970) was the ﬁrst to suggest that the spermatophore

organ could be useful for the taxonomy of whip spiders.

3.1.4. Size ratio of the carapace

However, as the male gonopod is membranous, the shape of its

To test if the ratio length/width of the carapace follows the pat-

parts are subject to variation, depending on the state of preserva-

tern described by Quintero (1976) (more than 0.70 for T. princeps

tion and handling of the specimen (Weygoldt, 1999c). Alternatively,

and less than 0.70 for T. froesi), 43 specimens of Trichodamon were

Giupponi and Kury (2013) suggested to use the structure’s division

measured, including the type series. Male and female adult speci-

and texture instead of shape as taxonomic characters and these

mens from a wide geographical distribution were chosen (see Table

characters have been shown useful within Heterophrynus Pocock,

S1). The size ratio of almost all specimens measured (except one)

1894 species (Giupponi and Kury, 2013).

was below 0.7 (including the type specimens), with median 0.62,

The male gonopod (Fig 5A–H) is formed by a pair of lateral tubes

standard deviation 0.05 (see Table S1). Consequently, this charac-

called ﬁstula (Fi) that can have a smooth or wrinkled surface (in Het-

ter cannot be used to differentiate the two proposed Trichodamon

erophrynus or in Trichodamon, respectively; Fig. 5A–D). The external

species.

lateral border of the ﬁstula can be straight (as in Heterophrynus) or

curved (as in Trichodamon; Fig. 5A, C). The median-dorsal portion

3.2. Variability of the gonopod of Trichodamon of the ﬁstula is either projected distally to form a pair of triangu-

lar lobes (in Heterophrynus), or curved converging (in Trichodamon)

Male (Fig. 5A–H) and female gonopods (Figs. 6A–D, 7A–F, 8A–F) called lobus dorsalis (LoD; Fig. 5A, C). The apex of the ﬁstula has a pair

are positioned in the dorsal region of the genital operculum. They of concentric parts (in Heterophrynus) or continuous bodies (in Tri-

are responsible for building and shaping the spermatophore (in chodamon); the proximal is the lobus lateralis primus (LoL1) that can

males) and collecting, storing and transporting sperm from the be covered by denticles (in Heterophrynus) or unarmed but rough

spermatophore for fertilization (in females). Several characters of (in Trichodamon; Fig. 5A–D). The distal is the lobus lateralis secundus

the female genitalia have been used in Amblypygi taxonomy, such (LoL2), which can be formed by a ﬂat projection (Fig. 5C) covered by

40 G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55

Fig. 5. SEM images of male gonopods of Trichodamon princeps Mello-Leitão, 1935 and Heterophrynus vesanicus Mello-Leitão, 1931. The colors relate to homologous structures.

A. Ventral view, T. princeps (Carinhanha, BA; MNRJ 09051). B. Posterior view, T. princeps (same as previous). C. Ventral view, H. vesanicus (Chapada dos Guimarães, MT; MNRJ

09056). D. Posterior view, H. vesanicus (same as previous). E. Ventral view, T. princeps (Morro do Chapéu, BA; MNRJ 09166). F. Posterior view, T. princeps (sampe as previous).

G. Ventral view, T. princeps (Itacarambi, MG; MNRJ 09160). H. Posterior view, T. princeps (same as previous). GO: gonopod; LaM: lamina medialis; Fi: ﬁstula; LoL1: lobus lateralis

primus; LoL2: lobus lateralis secundus; LoD: lobus dorsalis; PI: processus internus; MT: Mato Gosso; BA: Bahia.

“ﬁnger-print” marks (in Heterophrynus), or biﬁd with a pair of acute 3.2.2. Female genitalia

projections with rough surfaces (in Trichodamon; Fig. 5A–D). From The female genitalia (Figs. 6A–D, 7A–F, 8A–F) of whip spiders is

the inner part of these structures, (median region of the ﬁstula) formed by a membranous base with an aperture for the passage of

a pair of lamina called processus internus emerge (PI; Fig. 5A–D). the sperm (seminal receptacle) and, in some species, a pair of pro-

Between the pairs of the PI, a membranous structure called lamina jected, sclerotized appendages. The appendages are used to collect

medialis (LaM) is present that can be divided (in Heterophrynus) or the egg sac from the spermatophore to inside of the genital atrium

fused (in Trichodamon; Fig. 6A–D). (Weygoldt, 1969; Weygoldt et al., 1972). The shape of the gonopod

Despite being informative in Heterophrynus, the Fi, LaM, LoL1, or of the appendages vary among species, genera and families in

LoL2, LoD and PI did not show diagnostic patterns among the spec- Amblypygi, but show little variation among specimens of the same

imens analysed. SEM images from three specimens (Fig. 5E–H) and species (Weygoldt, 1999c).

the measurement of other males via dissection microscope (55 in The female genitalia of Phrynichidae and Phrynidae (families

total) showed that the most variable characters were LaM, which with the better known species) have shown to be uniform in shape

could be protracted or retracted (likely as result of the ﬁxation and reliable for species identiﬁcation (Mullinex, 1975; Quintero,

state), and LoL2, which has long and wide lateral projections in 1981; Weygoldt, 1972, 1974, 1977c). Weygoldt (1999c) argued

some individuals and narrow and short in others. that the male and female genitalia co-evolved to facilitate sperm

transfer, so it is expected that the female gonopod of each species

G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55 41

Fig. 6. Picture and SEM of female gonopods of Trichodamon. A. Paratype gonopod of T. froesi, Ituac¸ u, BA (MNRJ 09016). B. Holotype gonopod of T. princeps, Cana Brava, GO

(IBSP 038). C. Gonopod of specimen from Carinhanha, BA (MNRJ 09051). D. Gonopod of specimens from Campo Formoso, BA (MNRJ 09184). Scale bar A, B: 1 mm.

is unique, as observed in several whip spider species (Giupponi Fage (1954): 180; Weygoldt (1972): 131; Beck and Foelix (1974):

and Kury, 2013; Giupponi and Miranda, 2012, 2016; Jocqué and 327; Quintero (1976): 225; Weygoldt (1977b): 288, 296; Quintero

Giupponi, 2012; Miranda and Giupponi, 2011; Miranda et al., (1980): 341, 344; Weygoldt (1990): 87, 91; Gouvêa (1993): 383;

2016a; Miranda et al., 2016b; Rahmadi et al., 2010; Rahmadi et al., Weygoldt and Hoffmann (1995): 13, 16, 17; Weygoldt (1995): 82,

2010; Rahmadi and Kojima, 2010). 83; Weygoldt (1996a): 196, 198, 199; Weygoldt (1996b): 125, 128,

Trichodamon is the ﬁrst well documented case of female gono- 129, 130; Weygoldt (1998): 1, 4, 57, 58, 59; Weygoldt (1999b):

pod variability in Amblypygi. Two extreme types of the claw-like 2, 4, 41; Weygoldt (1999c): 62; Weygoldt (2000b): 339, 340, 343,

projections are observed in this genus: one with smooth curves 344, 345; Weygoldt (2000a): 22, 31; Weygoldt (2002c): 251–253;

◦

(curves with less than 90 ; Fig. 6A); and one with sharp curves Weygoldt (2002b): 313, 314; Weygoldt (2002a): 144; Baptista and

◦

(curves with more or equal to 90 ; Fig. 6B). Between these two Giupponi (2003): 84; Harvey (2003): 19; Weygoldt (2008): 224,

forms, all sorts of variations can be found. For example, individu- 230, 231; Weygoldt (2009): 180; Trajano and Bichuette (2010):

als of the same locality can have different shapes of gonopod claw 7; Armas (2011): 36; Vasconcelos et al. (2014): 155; Engel and

(Figs. 6C, 7C, D, 8B–D), and the same gonopod can have the two Grimaldi (2014): 3; Seiter et al. (2017): 126; Garwood et al. (2017):

types of curves in the claw (Fig. 8B, F). 13.

Type-species: Trichodamon princeps Mello-Leitão, 1935, by orig-

inal designation.

3.3. Description of Trichodamon

Trichodamon princeps Mello-Leitão, 1935

Trichodamon princeps Mello-Leitão (1935): 184, ﬁgs 1–3; Mello-

Due to the morphological variation in Trichodamon, separating

Leitão (1936): 298–300, ﬁgs 1–3; Mello-Leitão (1940): ﬁgs 1, 2,

the analysed populations in more than one species would not be

5, 6; Kästner (1940): ﬁg. 86; Lawrence (1968): 2; Delle Cave and

justiﬁed. Therefore, Trichodamon froesi is considered a junior sub-

Simonetta (1975): 147; Quintero (1976): 225–227, ﬁgs 12–15;

jective synonym of Trichodamon princeps. Below is provided an

Pinto-da-Rocha (1995): 80; Seiter and Hörweg (2013): 51, Table 1.

updated description of Trichodamon princeps including new char-

Trichodamon pusillus Mello-Leitöo (1936): 300–302, ﬁgs 4–6;

acters and considering the morphological variation.

Lawrence (1968): 2; (synonymized by Mello-Leitão, 1940: 131).

Prynichidae Simon: Pocock, 1900 Trichodamon cf. froesi Mello-Leitão: Pinto-da-Rocha (1995): 79.

Trichodamon froesi Mello-Leitão (1940): 133–135, ﬁgs 3, 4, 7,

Phrynichinae Simon, 1892 8; Quintero (1976): 225–227, ﬁgs 1–3, 5–15; Weygoldt (1977b):

287–296, ﬁgs 1–7; Weygoldt (1977a): 396; Weygoldt (1977c):

Trichodamon Mello-Leitão, 1935

278–283, ﬁgs 4a–i, 5a–c, 6a–b; Delle Cave (1986): 146; Igelmund

Trichodamon Mello-Leitão (1935): 183; Mello-Leitão (1936):

(1987): 76; Gnaspini and Trajano (1994): 554; Weygoldt (1994):

297–298; Fage (1939): 110–111; Mello-Leitão (1940): 131–132;

42 G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55

Fig. 7. Pictures of female gonopods of Trichodamon. A. Specimen from Mucugê, BA (UFBA 003). B. Specimen from Ituac¸ u, BA (MZUSP 15.858). C. Specimen from Ituac¸ u, BA

(MNRJ 09016). D. Specimen from Campo Formoso, BA (MNRJ 09114). E. Specimen from Itaetê, BA (MNRJ 09180). F. Specimen from Itaetê, BA (MNRJ 09185). Scale bars: 1 mm.

242, 243, ﬁg. 1; Weygoldt and Hoffmann (1995): 1, 13 15, 16; Pinto- by dorsal spines 1 + 2 and ventral spine I), the shape and size of the

da-Rocha (1995): 79; Weygoldt (1996a): ﬁgs 17 –19; Weygoldt carapace (narrower than the other genera) and the shape of the

(1996b): ﬁgs 25, 31; Weygoldt (1998): 57, 59; Weygoldt (1999c): male and female genitalia.

62; Weygoldt (1999a): 112, ﬁgs 36 –40; Weygoldt (2000a): ﬁgs 22, Material examined:

33–35, 68–69, 150–151, 257–261; Weygoldt (2002a): 144; Baptista BRASIL, state of Bahia: 1♀, 1♂, 1 juvenile [Trichodamon froesi

and Giupponi (2003): 82; Weygoldt (2008): 224, 230; Walter M-L, 1940; Ituac¸ u, Lapa da Mangabeira; Froes, H. leg.; no date; det.

(2013): 314, 315; Gonc¸ alves-Souza et al. (2014): 182; Vasconcelos Mello-Leitão, C.F.; MNRJ 0916 - TYPE MATERIAL OF T. froesi]; 1♀,

♂

et al. (2017): 1. [NEW SYNONYMY] 1 , 1 juvenile, [Trichodamon princeps M-L, 1935; Santana, Gruta do

Padre; Chaimowicz, F.; no date; det. G.S. Miranda; MNRJ 09005]; 1♂

Diagnosis: Trichodamon princeps can be recognized by the com-

[Trichodamon froesi M-L, 1940; Ituac¸ u; no collector; no date; det.

bination of the following characters: leg I with 37–38 articles in

Giupponi, A.P.L.; MNRJ 0909]; 1♀ [Trichodamon froesi M-L, 1940;

tibia and 70–81 in tarsus; tarsus I with a deep, longilineal rod sen-

Itaetê, Poc¸ o Encantado; Trajano, E. leg.; 1.ix.1991; det. Baptista,

silla on the ﬁrst (distal) and the 10th article (Fig. 14); basitibia IV

R. L. C.; MNRJ 0910]; 1♀ [Trichodamon froesi M-L, 1940; Itaetê,

divided in two articles; distitibia IV with trichobothria bm closer

Poc¸ o Encantado; Mendes, L. de F. leg.; vi.1993; det. Baptista, R.

to bf than to nbf; sbf with two trichobothria; frontal series with

L. C.; MNRJ 0911]; 1♀ [Trichodamon froesi M-L, 1940; Morro do

21–27 and caudal series with 24–30 trichobothria; bc with 5–8

Chapeú, Gruta dos Brejões I; Horta, L.; 6.xi.1994; det. Baptista,

trichobothria; female gonopod with sclerotized claw-like projec-

R. L. C.; MNRJ 09048]; 1♀, 2♂ [Trichodamon sp.n.; Carinhanha,

tion and receptaculum seminalis to store sperm; male gonopod with

Serra do Ramalho, Gruna do André; Baptista, R. L. C. & Giup-

bifurcated and wrinkled LoL2. Trichodamon princeps differ from all

poni, A. P. L. leg.; 28.vi.2001; det. Giupponi, A.P.L. & Baptista, R.

other species in the family by the unique phrynichid-hand (formed

L. C.; MNRJ 09051]; 1♂ [Trichodamon sp.n.; Carinhanha, Serra do

G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55 43

Fig. 8. Pictures of female gonopods of Trichodamon. A. Specimen from Santana, BA (MNRJ 09005). B. Specimen from Campo Formoso, BA (MNRJ 09112). C. Specimen from

Campo Formoso, BA (MNRJ 09114). D. Specimen from Itacarambi, MG (UFMG 9004). E. Specimen from Santana, BA (MNRJ 09005). F. Specimen from Elísio Medrado, BA (MNRJ

09191). Scale bars: 1 mm.

Ramalho, Gruna do André; Baptista, R. L. C. & Giupponi, A. P. L. 09114]; 1♂ [Trichodamon froesi M-L., 1940; Estrada de Pedra Igatu

−

leg.; 29.vi.2001; det. Giupponi, A.P.L. & Baptista, R. L. C.; MNRJ Andaraí; Bichuette, M. E; Scatoliri, T.; Passos, F. D. leg.; 19.i.2007;

09052]; 1 juvenile [Trichodamon froesi M-L., 1940; Carinhanha, det. Giupponi, A.P.L.; MNRJ 09116]; 1 juvenile [Trichodamon prin-

Serra do Ramalho, Lapa dos Peixes; Chagas Jr., A. leg.; 23.iv.2000; ceps M-L., 1935; Campo Formoso, Toca do Gonc¸ alo; Bichuette, M. E

det. Giupponi, A.P.L.; MNRJ 09053]; 1♂ [Trichodamon froesi M-L., leg.; 09.vi.1997; det. Giupponi, A.P.L.; MNRJ 09119]; 1 juvenile [Tri-

1940; Central – Toca da Cerca; Bichuette, M. E.; Passos, F. D. leg.; chodamon sp.; Jequié, Fazenda Piabanha, Km 43 próximo a Itajuru;

06.vii.2007; det. Giupponi, A.P.L.; MNRJ 09111]; 2♂ [Trichodamon Gavião, T. S. leg.; 12.v.2005; det. Giupponi, A.P.L.; MNRJ 09123];

♂

princeps M-L., 1935; Campo Formoso, Toca do Gonc¸ alo; Trajano, E. 1 [Trichodamon sp.; Jequié, Fazenda Piabanha, Km 43 distant

leg.; 13.v.1998; det. Miranda, G.S.; MNRJ 09112]; 1♀, 1♂ [Trichoda- from Itajuru; Gavião, T. S. leg.; 12.v.2005; det. Giupponi, A.P.L.;

mon froesi M-L., 1940; Carinhanha, Lapa dos Peixes; Pellegatti- MNRJ 09123]; 2♂ [Trichodamon sp.; Gruta de Brejões; Tiepolo-

Franco & Trajano, E. leg.; 25.ix.2005; det. Giupponi, A.P.L.; MNRJ col, L. M. leg.; 8.viii.2003; det. Giupponi, A.P.L.; MNRJ 09156]; 1♂

09113]; 2♀ [Trichodamon princeps M-L., 1935; Campo Formoso, [Trichodamon sp.; Gruta Natal, zona de entrada; Bichuette, M.E.

Toca do Gonc¸ alo; Trajano, E. leg.; 5.i.1997; det. Miranda, G.S.; MNRJ leg.; 10.xi.2004; det. Giupponi, A.P.L.; MNRJ 09157]; 2♂ [Trichoda-

44 G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55

mon princeps M-L, 1935; Morro do Chapéu, Gruta dos Brejões; det. Miranda, G.S.; CHNUFPI 0622]; 1♂ [Trichodamon princeps M-

Bichuette, M. E., Tanajura, V. S. & Rantin, N. B. leg.; 13.v.2009; L, 1935; Mata atrás do posto andorinhas, Milagres, Elev. 750m,

◦ ◦

det. Giupponi, A.P.L.; MNRJ 09166]; 3♂ [Trichodamon froesi M-L, 12 54 21.2 S 39 50 53.7W; E. S. Araújo et al. leg.; 16–18.iii.2012;

1940; Campo Formoso, Tiquara, Toca da Tiquara; Giupponi A.P.L & det. Miranda, G.S.; CHNUFPI 0627]; 1♀ [Trichodamon princeps M-L,

Baptista R.L.C leg.; 13.v.2009; det. Giupponi, A.P.L.; MNRJ 09179]; 1935; no data; det. Miranda, G.S.; UFBA ARA 049]; 1♀ [Trichodamon

♀

2 [Trichodamon princeps M-L, 1935; Itaetê, Gruta Natal, Fazenda princeps M-L, 1935; Pq. Sempre Viva, Mucugê; Stabile, L & Ferreira,

Rio Alegre; Pedroso, Dr. R., Bichuette, M.E. leg.; 04.iv.2005; det. P. leg.; 22.iv.2007; det. Miranda, G.S.; UFBA ARA 003]; 1♂ [Tri-

Giupponi, A.P.L.; MNRJ 09180]; 2 juveniles [Trichodamon sp.; Nova chodamon princeps M-L, 1935; Ituac¸ u, Lapa do Jó; no collector data;

Redenc¸ ão, Gruta Moreno, Mocambo II; Pedroso, D. R e Bichuette, 29.v.1990; det. Miranda, G.S.; UFBA ARA 001]; 1♂ [Trichodamon

M. E. leg.; 05.iv.2005; det. Giupponi, A.P.L.; MNRJ 09182]; 1 juve- princeps M-L, 1935; Campo Formoso, Gruta do Satélite; Antonio

nile [Trichodamon sp.; Nova Redenc¸ ão, Arredores Gruta Moreno, leg.; 05.03.183; det. Miranda, G.S.; UFBA ARA 002]; 1♂ [Trichodamon

Mocambo II; Pedroso,D. R e Bichuette, M. E. leg.; 05.iv.2005; det. princeps M-L, 1935; nod data; det. Miranda, G.S.; UFBA ARA 048];

♀

Giupponi, A.P.L.; MNRJ 09183]; 6♂, 1 juvenile [Trichodamon prin- 1 , 1♂ [Trichodamon princeps M-L, 1935; no data; det. Miranda,

ceps M-L, 1935; Campo Formoso, Lapa do Convento; Giupponi, G.S.; UFBA ARA 050]; 2♂ [Trichodamon princeps M-L, 1935; Gruna

A.P.L & Baptista, R.L.C. leg.; 06.xi.2002; det. Miranda, G.S.; MNRJ do Peixe, Carinhanha; no collector data.; 23.iv.2000; det. Miranda,

09184]; 1♂, 1♀ [Trichodamon princeps M-L, 1935; Elísio Medrado, G.S.; ISLA 3862]; 1♂ [Trichodamon princeps M-L, 1935; Campo For-

Reserva Jequitibá, Campo rupestre; Bertani, R., Nagahama, R.H. & moso, Toca do Gonc¸ alo; no collector data; 11.vi.2012; det. Miranda,

Fukushima, S. leg.; 06.x.2007; det. Miranda, G.S.; MNRJ 09191]; G.S.; ISLA 3862].

1♀ [Trichodamon princeps M-L, 1935; Andaraí, Gruta da Paixão; State of Ceará: 1♀ [Trichodamon sp.n.; Itatira, road Lagoa

Bichuette, M.E., Rantins, B., Scatoloni, T.L.C. leg.; 13.vii.2008; det. do Mato, Mina de Urânio, 420 m; Giupponi, A.P.L. & Kury, A.B.

Miranda, G.S.; MNRJ 09192]; 1♀ [Trichodamon princeps M-L, 1935; leg.; 20.iii.1999; det. Giupponi, A. P. L.; MNRJ 09020]; 1 juve-

Elísio Medrado, RPPN Jequitibá; Bertani, R., Nagahama, R.H. & nile [Trichodamon princeps M-L, 1935; Santa Quitéria, 413574mN

Fukushima, S. leg.; 06.x.2007; det. Miranda, G.S.; MNRJ 09193]; 9495569mE SAD69; I. Cizauskas & V. Felice leg.; 26–28.iii.2013; det.

♀

1 [Trichodamon princeps M-L, 1935; Central, Toca da Candeia; Miranda, G.S.; MZUSP 53.663]; 1 juvenile [Trichodamon princeps M-

Bichuette, M.E. leg.; 26.i.2007; det. Miranda, G.S.; MNRJ 09194]; 1♀ L, 1935; Santa Quitéria, 413555mN 9495509mE SAD69; I. Cizauskas

[Trichodamon princeps M-L, 1935; Itaetê, Poc¸ o Encantado; Gallão, & V. Felice leg.; 26–28.iii.2013; det. Miranda, G.S.; MZUSP 53.621];

♂

J.E. leg.; 31.vii.2010; det. Miranda, G.S.; MNRJ 09195]; 1 juvenile 1 [Trichodamon princeps M-L, 1935; Santa Quitéria, 413559mN

[Trichodamon princeps M-L, 1935; RPPN Jequitibá, Elísio Medrado, 9495568mE SAD69; I. Cizauskas & V. Felice leg.; 26–28.iii.2013;

Campo rupestre; Bertani, R., Nagahama, R.H. & Fukushima, S. det. Miranda, G.S.; MZUSP 54.240]; 1♀ [Trichodamon princeps M-L,

leg.; 06.x.2007; det. Miranda, G.S.; MNRJ 09207]; 1 juvenile [Tri- 1935; Santa Quitéria, 413548mN 9495574mE SAD69; I. Cizauskas

chodamon princeps M-L, 1935; RPPN Jequitibá, Elísio Medrado, & V. Felice leg.; 26–28.iii.2013; det. Miranda, G.S.; MZUSP 53.961];

♀

Campo rupestre; Bertani, R., Nagahama, R.H. & Fukushima, S. leg.; 2 [Trichodamon princeps M-L, 1935; Quixadá, Serra do Estevão,

◦ ◦

06.x.2007; det. Miranda, G.S.; MNRJ 09208]; 1 juvenile [Trichoda- road to Dom Maurício, 4 55 32,6 S 39 8 31.6 W, 482m; M.B. Silva

mon princeps M-L, 1935; Reserva Jequitibá, Elísio Medrado, under & N. Saraiva leg.; 18.iv.2014; det. Miranda, G.S.; CHNUFPI 1326]; 2♂

♀ stone, day collecting, BA 1334; Bertani, R., Nagahama, R.H. & 1 [Trichodamon princeps M-L, 1935; Quixadá, Jardim dos Monól-

◦ ◦

Fukushima, S. leg.; 06.x.2007; det. Miranda, G.S.; MNRJ 09209]; itos, inselbergs do Ac¸ ude do Euclides, 4 57 15,4 S 39 0 0.6 W,

2 juvenile [Trichodamon princeps M-L, 1935; Andaraí, povoado de 180–200m; M.B. Silva & N. Saraiva leg.; 20.iv.2014; det. Miranda,

Igatu; Giupponi, A.P.L., Miranda, G.S., Bichuette, M.E & Gallão, J.E. G.S.; CHNUFPI 1325].

leg.; 10–12.iii.2012; det. Miranda, G.S.; MNRJ 09210]; 1♀ [Trichoda- State of Goiás [TYPE MATERIAL OF T. princeps e T. pusillus]: 4♂,

♀

mon princeps M-L, 1935; Lajedinho; Fábio Bondezan leg.; 19.ii.2015; 1 , 1 juvenile [Trichodamon princeps M-L, 1935; Cana Brava e Nova

det. Miranda, G.S.; MNRJ 09269]; 1♂ [Trichodamon froesi M-L, 1940; Roma; Blaser, J. leg.; xii.1932; det. Mello-Leitão, C.F.; IBSP 038]; 1

Morro do Chapéu; C.E. Universitário leg.; i.1973; det. Giupponi, juvenile, [Trichodamon pusillus M-L, 1937; Cana Brava; Blaser, J. leg.;

A.P.L.; IBSP 046]; 1♀ [Trichodamon princeps M-L, 1935; no lacil- xii.1932; det. Mello-Leitão, C.F.; IBSP 037].

ity; Wremercol, P. leg; vii.1968; det. Giupponi, A.P.L.; IBSP 040]; State of Minas Gerais: 1♂ [Trichodamon froesi M-L, 1940; Jaíba,

6 ♂ [Trichodamon princeps M-L, 1935; Central, Toca Esperanc¸ a; Mocambinho, Serra Azul; Duarte, J. leg.; 10.iii.1995; det. Baptista,

Ramos, E.F. leg.; vii. 1997; det. Giupponi, A.P.L.; IBSP 070]; 1 juve- R. L. C.; MNRJ 09006]; 1♂ [Trichodamon sp.; Jaíba, Mocambinho;

nile [Trichodamon princeps M-L, 1935; Gruta D’água Patamute, Caetano, C. & Soares, A. leg.; 7.ix.1997; det. Giupponi, A.P.L.; MNRJ

◦ ◦

Curac¸ á, 09 18 49 S 39 30 20 O; Binael S. Santos leg.; 3.iii.1999; 09007]; 1♂ [Trichodamon froesi M-L, 1940; Itacarambi, Serra de

det. Miranda, G.S.; MZUSP 53.606]; 1♀, 1♂, 2 juvenile [Trichodamon Itacarambi, Caverna da Lapa; Trajano, E. leg.; 21.xi.1989; det. Bap-

princeps M-L, 1935; Lenc¸ ois, Poc¸ o encantado; Liana leg.; xii.1992; tista, R. L. C.; MNRJ 09008]; 1♀, 2♂ [Trichodamon froesi M-L, 1940;

det. Miranda, G.S.; MZUSP 15.852]; 1♂ [Trichodamon princeps M- Itacarambi, Gruta Olhos d’Água; Giupponi, A. P. L. & Baptista, R.

L, 1935; Caetité, Gruta PF-31, 0767090mE/8389502mN SAD69 ; L. C. leg.; 26.vi.2001; det. Giupponi, A.P.L. & Baptista, R. L. C.;

Andrade et al. leg; 08-15.xii.2008; det. Miranda, G.S.; MZUSP MNRJ 09049]; 1♀, 2♂ [Trichodamon sp.; Itacarambi, Gruta Olhos

54.241]; 1♂ [Trichodamon sp.; Campo Formoso, Lapa do Convento; d’Água; Giupponi, A. P. L. & Baptista, R. L. C. leg.; 26.vi.2001; det.

F. Chaimowicz leg.; no date; det. Froehlich, E.M.; MZUSP 54.241]/1♂ Giupponi, A.P.L. & Baptista, R. L. C.; MNRJ 09050]; 5♂ [Trichoda-

[Trichodamon sp.; Morro do Chapéu/Irecê, Lapa dos Brejões; F. mon froesi M-L, 1940; Itacarambi; Giupponi, A.P.L. leg.; 03.ix.2002;

Chaimowicz leg.; no date; det. Froehlich, E.M.; MZUSP 53.300]; 1♂ det. Giupponi, A.P.L.; MNRJ 09050]; 1♀ [Trichodamon princeps M-L,

[Trichodamon sp.; Santana, Gruta São Geraldo; Sessegolo, G. leg.; 1935; Itacarambi, Parque Nacional Cavernas do Peruac¸ u, Gruta do

12.vii.1987; det. Baptista, R.L.C.; MZUSP 53.279]; 1♀, 1 juvenile [Tri- Rezar, 15 8 36.4 S 44 14 6 W; G.F.B.P. Ferreira et al leg.; 22.x.2010;

chodamon sp.; Ituac¸ ú, Lapa da Mangabeira; F. Chaimowicz leg.; no det. Miranda, G.S.; UFMG 9404]; 1♂ [Trichodamon princeps M-L,

date; det. Baptista, R.L.C.; MZUSP 53.279]; 1♀ [Trichodamon prin- 1935; Itacarambi, Parque Nacional Cavernas do Peruac¸ u, Gruta do

ceps M-L, 1935; Milagres, Mata atrás do posto andorinhas, Elev. Cabloco, 18 17 14 S 43 51 24 W; Ferreira et al leg.; 17–22.x.2010;

◦ ◦

750m, 12 54 21.1 S 39 50 53.7W; E. S. Araújo et al. leg.; 16–18- det. Miranda, G.S.; UFMG 9404]; 1♂, 1♀ [Trichodamon princeps M-

.iii.2012; det. Miranda, CHNUFPI 0646]; 1♂ [Trichodamon princeps L, 1935; Montalvânia, Gruta do So Zé Prefeito; no collector data.;

M-L, 1935; Mata atrás do posto andorinhas, Milagres, Elev. 750m, 16.vii.2007; det. Miranda, G.S.; ISLA 3863].

◦ ◦

12 54 21.2 S 39 50 53.7W; E. S. Araújo et al. leg.; 16–18.iii.2012;

G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55 45

Fig. 9. Distributional map of Trichodamon showing variation in colour of the carapace among the different populations. A. Santa Quitéria, state of Ceará (CE) (MZUSP 53.961).

B. Santa Quitéria, CE (MZUSP 54.240). C. Itatira, CE (MNRJ 09020). D. Martins, state of Rio Grande do Norte (ISLA 3865). E. Lagoa, state of Paraíba (CHNUFPI 0656). F. Campo

Formoso, state of Bahia (BA) (ISLA 3864). G. Morro do Chapéu, BA (MNRJ 09156). H. Itaetê, BA (MNRJ 091157). I. Jequié, BA (MNRJ 09123). J. Ituac¸ u, BA (MZUSP 15.858). K.

Carinhanha, BA (MNRJ 091052). L. Itacarambi, state of Minas Gerais (MNRJ 09050). M. Montalvânia, MG (ISLA 3863).

♂

State of Paraíba, 1 [Trichodamon princeps M-L, 1935; Lagoa; Description (based on the type material; variations based on

Alencar, J.B.R. leg.; 05.iii.2011; det. Miranda, G.S.; CHNUFPI 0656]; additional material examined): Colour: carapace, (Fig. 9), abdomen

♂

1 [Trichodamon princeps M-L, 1935; Lagoa; Alencar, J.B.R. leg.; (Fig. 10) and leg coxae pale red; pedipalp, chelicerae and legs

05.iii.2011; det. Miranda, G.S.; CHNUFPI 0657]. reddish-brown. Juveniles and adults of some specimens with pale

♂

State of Rio Grande do Norte, 1 [Trichodamon princeps M- yellow bands on the carapace, abdomen and legs; juveniles always

L, 1935; Casa de Pedra, Martins; no collector data; no date; det. with bands, but paler, almost the same colour of the rest of the

Miranda, G.S.; ISLA 3835]. carapace (reddish brown), or limited the border of the carapace.

46 G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55

Fig. 10. Abdomen and sternum of different specimens of Trichodamon. The abdomen are disposed from the northernmost (A) to the southernmost record of the distribution

(J). A. Itatira, state of Ceará (MNRJ 9020). B. Martins, state of Rio Grande do Norte (ISLA 3865). C. Lagoas, state of Paraíba (UFPI 0043). D. Campo Formoso, state of Bahia (BA)

(MNRJ 9184). E. Campo Formoso, BA (MNRJ 9114). F. Morro do Chapéu, BA (MNRJ 9166). G. Itaeté, BA (MNRJ 9195). H. Elísio Medrado, BA (MNRJ 9193). I. Andaraí, BA (MNRJ

9192). J. Montalvânia, state of Minas Gerais (ISLA 3863). K. Sternum of holotype of T. froesi (MNRJ 09016). L. Sternum of specimen from Elisio Medrado, BA (MNRJ 9191).

Specimens from the northernmost areas of the distribution (states longitudinal groove from the fovea to the posterior region of the

of Ceará, Rio Grande do Norte, Pernambuco and northern Bahia) carapace, reaching the border over the abdomen. Sparse tubercles

with pale yellow bands well-marked both in juvenile and adults distributed on the surface of the carapace.

(Fig. 9); specimens from central Bahia and northern Minas Gerais Sternum (Fig. 10K, L): tri-segmented, all segments sclerotized

with less marked bands, i.e., the bright yellow marks are more and ﬂat. Tritosternum projected anteriorly between the chelicera

similar to the dark colour of the rest of the carapace (Fig. 9). with a pair of setae on its apex; base sub-pentagonal with lateral

Carapace (Fig. 9): cordiform, with a pair of median eyes and borders serrated; posterior border truncated; one pair of tubercles

three pairs of lateral eyes; median eye tubercle prominent; lateral close to the truncated border. Median piece rectangular. Posterior

and median eyes pale yellow; frontal process prominent; carapace piece elliptical. Bright region, with small sclerotization (between

border (lateral to the median eye tubercle) depressed; depres- the sternal plaques and the coxae) very reduced, with some plaques

sions followed by a pair of projections in front of the lateral eyes; more heavily sclerotized than others, being a pair of plaques by the

curved depression directed posteriorly after projections. Border of side of the tritosternum, and two pairs of plaques by the side of the

the carapace with a series of tubercles; small tubercles in front of median piece and the posterior piece.

the eyes, larger on the lateral (on the wider part of the carapace) Abdomen (Fig. 10A–J): oblong, with a pair of rounded median-

and absent in the posterior region (above the abdomen). Median lateral depressions; the central region of this region darker (reddish

longitudinal groove starts on the median eye tubercle and extends brown) than the tegument around it (brown). Bright area sur-

until the fovea; three pairs of transversal grooves from the fovea in rounded by a dark band posteriorly, which extends to the lateral of

direction to the border of the carapace, but not reaching it; anterior the abdomen. Area of brighter colour with higher number of tuber-

transversal groove behind gibbousness that contains the pair of lat- cles; tubercles similar those of the carapace (in size and amount).

eral eyes; median transversal groove on the middle of the carapace; Some specimens of the north of the distribution with bands well-

posterior transversal groove on the basal third of the carapace; one marked (e.g. Fig. 9C).

G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55 47

Fig. 11. Details of leg I of Trichodamon (MNRJ 9051). A. General view of the leg. B. Detail of the longitudinal sulc on the ﬁrst article. C. Detail of the longitudinal sulc on the

10th article.

Chelicerae (Figs. 2 and 3): basal article of the chelicerae with cleaning organ; cleaning organ half the size of the article; tarsus

four teeth; distal tooth biﬁd, distal apex longer than the proximal; and claw fusioned.

median pair of teeth subequal, one mesal and one ectal; proximal Legs: glabrous, with several tubercles covering all articles.

tooth wider and longer than the others; inner side of basal segment Patella with a pair of trichobothria, one in each face (frontal and

with several acute setae. Cheliceral claw with four teeth, being the caudal). Tibia of leg I divided in 37–38 articles (up to 47 in regen-

three proximal subequal and the distal smaller; dense covering of erated legs); tarsus I with 70–81 articles. Apical article of tarsus

setae on the inner distal surface. I with a modiﬁed claw with three subequal acute projections (on

Pedipalp (Fig. 4A–G): Trochanter: dorsal border with one the SEM image it is not possible to see the base because it is sunk

prominent spine on the median region and one small spine on the in the article). Short clavate setae spread on the surface of tarsus I

distal region; area between dorsal and ventral borders unarmed. (Fig. 11A–C). Longitudinal crevice 1/3 the length of the ﬁrst article;

Ventral border with three prominent spines and several small crevice with several setae (on the SEM image the setae were acci-

spines and tubercles interspersing them; median spine longer and dentally broken while preparing the material). Longitudinal crevice

wider; proximal spine and distal spine 1/3 the median. Femur: in present on the 10th article, occupying the whole length of the arti-

juveniles, the main series has six dorsal spines, spines 1 and 2 sube- cle. Basitibia IV divided in two articles. Median article with one

qual, spine 3 two thirds the second and half the fourth, the last three trichobothria (bt) on the middle of the article. Distitibia IV with

spines decreasing in size; spines of the main series interspersed by trichobothria bm closer to bf than to nbf; sbf composed by two tri-

smaller spines and/or tubercles; in adults, three prominent spines chobothria; the trichobothria named stc (Weygoldt, 1977b) is now

in the main series, the remainder reduced; spines 1 and 2 subequal; called smf (submedian-frontal) and is placed roughly on the middle

spine 3 1/3 the size of the ﬁrst two; on the base of the second spine of the article; a new trichobothria is identiﬁed close to the frontal

begins a line of tubercles that extends until the extremity of the series and is named stf; the frontal series has 21–27 trichobothria,

distal femur; juveniles with six ventral spines, spine 1 1/3 the sec- bc has ﬁve to eight trichobothria; sbc on the proximal third; stc on

ond, spine 3 subequal spine 1; last three spines decreasing in size; the end of the median third; caudal series with 24–30 trichobothria

main series interleaved by smaller spines and tubercles; adults with (Fig. 12A, B).

two prominent proximal spines on the main series and one smaller Female and male genital: described in the previous section.

distally; a row of tubercles on the base of all spines. Patella: juve-

niles with three long dorsal spines, subequal, around half the size 3.4. Distribution

of the article; one spine in the middle the article, 1/3 the size of

the distal spines; adults with one ventral spine distally. Tibia: one There are few records of Trichodamon in the literature, despite

dorsal spine approximately 2/3 the size of the article with one pair being conspicuous animals (Fig. 13A–E ). Mello-Leitão (1935,

of tubercles (tu) in juveniles and one tubercle only in adults, on the 1936,1940 recorded Trichodamon from Nova Roma, Cana Brava

base of the spine; one ventral spine on the base of the article, half (Goiás) and Ituac¸ u (Bahia); Quintero (1976) published a new record

the size of the article. Tarsus: unarmed, with long setae on the dor- from Januária (Minas Gerais); Weygoldt (1977c) recorded spec-

sal region; setae with feathery apex; two small spines above the imens from Andaraí (Bahia); and Baptista and Giupponi (2003),

48 G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55

Table 2

Statistics from the cladistic analysis of Phrynichidae: number of most parsimonious

trees, consistency index (CI), retention index (RI), length and ﬁt.

Analysis No. of trees retained CI RI Length Fit

EW 6 0.56 0.65 297 23.94

IW k = 1 1 0.55 0.64 300 23.80

IW k = 3 1 0.56 0.64 298 23.74

IW k = 6 1 0.56 0.64 298 23.76

IW k = 10 1 0.56 0.64 298 23.76

IW k = 30 1 0.56 0.65 297 23.94

IW k = 40 1 0.56 0.65 297 23.94

IW k = 50 1 0.56 0.65 297 23.94

IW k = 60 1 0.56 0.65 297 23.94

IW k = 70 1 0.56 0.65 297 23.94

IW k = 80 1 0.56 0.65 297 23.94

IW k = 90 1 0.56 0.65 297 23.94

IW k = 100 1 0.56 0.65 297 23.94

IW k = 200 1 0.56 0.65 297 23.94

IW k = 300 1 0.56 0.65 297 23.94

IW k = 400 1 0.56 0.65 297 23.94

IW k = 500 1 0.56 0.65 297 23.94

◦

although the mean maximum temperatures rarely exceed 40 C

(Nimer, 1972). Precipitation is low (less than 1000 mm per year)

and irregular, in general limited to a short period of the year

(Cardoso and Queiroz, 2011).

Trichodamon seem to be adapted to hot and dry environments,

similar to other genera in the family that inhabit arid regions

of Africa (Damon, Xerophrynus, Musicodamon; Weygoldt (2000a)).

Additionally, specimens of Trichodamon princeps are found in caves,

probably due to the stable environmental conditions provided by

such environment (climate stability and prey abundance) (Chapin,

2015; Ferreira et al., 2010).

The distribution of Trichodamon is probably not larger than

known due to two factors: (1) lack of collecting in several areas

of the Caatinga and Cerrado, places that are difﬁcult to access; (2)

competition with Heterophrynus longicornis (Butler, 1873) (Fig. 13F)

and H. vesanicus Mello-Leitão, 1931, large whip spider species that

inhabit the same micro-habitat (Giupponi, 2004). Heterophrynus

longicornis is widely distributed, covering from east Amazonia, Cer-

rado and Caatinga; Heterophrynus vesanicus occupies the Brazilian

Cerrado and competes with T. princeps, mainly in the north of Minas

Gerais. All three species are of large size (3–4 cm body length) and

feed on invertebrates and small vertebrates, and occupy similar

niches. The competition occurs so evidently that in the same munic-

ipality where T. princeps and Heterophrynus are found, they do not

co-occur in the same cave (Baptista and Giupponi, 2003).

3.5. Cladistic analysis

Fig. 12. Distribution of trichobothria on distitibia IV. A. Distitibia on frontal view.

The new trichobothria is here called stf. B. Distitibia caudal view. bf: baso frontal; bm:

baso medial; nbf: new baso frontal; sbf: sub-baso frontal; smf: sub-medio frontal; The cladistic analysis recovered six trees under equal weight

stf: sub-terminal frontal; sf: frontal series; bc: baso caudal; sbc: sub-baso caudal; stc: (ew; L = 297, CI = 0.56, RI = 0.65; Table 2), four of which had differ-

subterminal caudal; sc: caudal series.

ent topologies for the ingroup. One tree (Fig. 14) was consistently

recovered by both ew and implied weight (iw) analysis, under the

Dessen et al. (1980), Ferreira and Horta (2001), Ferreira and Martins majority of k values (k = 30–500) and with highest average support

(1999), Ferreira et al. (2010), Gnaspini and Trajano (1994), Gouvêa values (symmetric resampling, Bremer and jackknife; Fig. 14); this

(1993), Trajano (1992), Walter (2013) found specimens in caves was chosen as the preferred tree (Figs. 14 and 15). The iw trees had

in the states of Bahia, Minas Gerais and Rio Grande do Norte (see the same length, CI and RI as the trees found under ew (Table 2).

Table S3). Here we make new records of Trichodamon princeps in Phrynichidae was found monophyletic with Xerophrynus sister

the states of Ceará and Paraíba and several new localities in the to all other genera (Fig. 14). The remaining genera were grouped in

state of Bahia, all inside the Brazilian Caatinga (see list of material Euphrynichida Weygoldt, 2000, which encompasses Phrynichinae

analysed). and Damoninae. The unranked taxon Euphrynichida was used in

It is noteworthy that T. princeps occurs predominantly in dry the same sense as originally proposal by Weygoldt (2000a). Phryn-

areas, like Cerrado and Caatinga (Fig. 9). Ingressions in areas of ichinae were recovered with Trichodamon as sister to Phrynichini

Atlantic Forest are the result of environmental alterations, i.e., Weygoldt, 1995 (Phrynichus + Euphrynichus) and Damoninae was

deforestation. On the Caatinga biome, the annual mean temper- retrieved with Musicodamon as sister to Damonini (Phrynichoda-

◦

ature is among the highest in Brazil, varying from 26 to 28 C, mon + Damon).

G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55 49

Fig. 13. Photos of live specimens of Tichodamon princeps (A–E) and Heterophrynus sp. (F) from different localities. A. Specimen from Maracás, BA. B. Freshly molted specimens

from Andaraí, BA. C. Specimen from Andaraí eating a cricket. D. Specimen from Ceará. E. Specimen from Elísio Medrado, BA. F. Specimens from Araripe, CE.

Source: A. Leonardo Caravalho. B, C. Gustavo Miranda. D. Ivan Magalhães. D. Rogério Bertani. E. Rodrigo Lopes Ferreira.

The family Phrynichidae presented good branch support and palp femur dorsal; the presence of only one spine on the ventral

nine synapomorphic character states (Fig. 15). Five character states pedipalp patella; formation of phrynich hand by the second patella

were unique to the family: the dorsal position of the articulation ventral spine; and the presence of only one spine on the dorsal

(hinge) trochanter-femur; position of the ventral spine on pedipalp pedipalp tibia.

tibia (close to the border of the tibia); pedipalp patella catching The clade of Musicodamon, Phrynichodamon and Damon

tool forming a phrynichid hand (Weygoldt, 1977c); presence of tri- (Damoninae) had six synapomorphic character states recovered

chobothria nbf on distitibia IV; and presence of trichobothrium sbc (Fig. 15): socket of the setae on the frontal margin of the carapace

on distitibia IV. placed on a small spine; female gonopod claw-like projection with

Euphrynichida had good branch support with 15 synapomor- sclerotization in the apex only; presence of ﬁve spines ventrally

phic character states, of which three were unique to the clade on pedipalp trochanter; presence of central conspicuous setifer-

(Fig. 15): the rectangular shape of the female gonopod (lost in ous tubercle before or inner to spine one; the long size of the

Phrynichodamon); the presence of one spine on the proximal series spine between spine I and the distal margin; the presence of 3–4

of spines (between the proximal border of the article and the ﬁrst setae on the row close to the distal border of the tibia, ventrally.

spine of the main series); and the absence of spines between pedi- Damonini was recovered with six synapomorphic character states:

palp patella spine I and its distal margin. The female gonopod the absence of the ventral sac cover; the soft surface of the claw-like

in other whip spiders is oval (e.g., Charinidae; see Giupponi and tegument on the female gonopod; the presence of 44–47 pseudoar-

Miranda (2016)). ticles on tarsus I; ﬁve spines on ventral pedipalp patella; the middle

Phrynichinae was supported by eight synapomorphic character position of the trichobothrium bt on basitibia IV; and the presence

states (Fig. 15), only one of which was unique to the subfamily: the of nine trichobothria on sc (distititibia IV).

distal position of spines I, II and III (the last spine when present) on

the dorsal pedipalp patella. Phrynichini has 11 characters support-

4. Discussion

ing the clade, four of which were exclusive: the presence of one

spine ventrally on pedipalp femur; the absence of a small spine

In contrast to other Amblypygid groups, the genus Trichodamon

between spines 2 and 3 on pedipalp femur; the absence of a small

was found to have highly variable characters, such as chelicerae

spine between spines 1 and 2 and spines 2 and 3 on female pedi-

teeth and female gonopod shape. Consequently, the characters used

50 G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55

Fig. 14. Preferred tree of the cladistic analysis of Phrynichidae (297 steps, consistency index = 0.56, retention index = 0.65). Clade support is indicated above (symmetric

resampling) and below (Bremer and jackknife) branches. Sensivity plots (‘Navajo rugs’) indicate the recovery of the nodes in the analysis under equal and implied weights

with different values of k (black squares indicate monophyly; white squares indicate non-monophyly).

by Mello-Leitão (1940) and Quintero (1976) to diagnose the species plesiomorphic characters (Weygoldt, 1996b), and Phrynichodamon

of Trichodamon are not reliable. Thus, it is concluded that the genus has been considered the second most inclusive group, sister to

Trichodamon is monotypic (T. froesi syn. jun.), consisting only of the remainder genera. Weygoldt (1999b) proposed synapomor-

the species Trichodamon princeps. All citations of Trichodamon in phies (without analysis) to the subfamilies of Phrynichidae, and

the literature refer to T. princeps. placed Xerophrynus as the sister genus to all other in the family

Trichodamon princeps was known from few places in the state (or even outside Phrynichidae). Our analyses recovered Phrynichi-

of Bahia, Goiás, Minas Gerais and from one location in Rio Grande dae as monophyletic and conﬁrmed previous hypothesis of a sister

do Norte. Here, we expanded the known occurrence area of the group relationship between Xerophrynus and Euphrynichida; the

species to the states of Paraíba and Ceará and also reported several node supporting this split had good support and Xerophrynus was

new records in the state of Minas Gerais and Bahia, revealing that recovered with six autopomorphic states (Fig. 15).

the species is widely distributed in the Caatinga biome, both inside Weygoldt (1996b) recovered Musicodamon with a doubt-

caves and the epigean environment. ful position in the phrynichid tree and sister to Trichoda-

This was the ﬁrst time a thorough phylogenetic analysis was mon + Phrynichus + Eurphynichus. Weygoldt (1999b), on the other

performed with all genera of Phrynichidae. The data set used here hand, considered the clade Damon + Musicodamon as monophyletic

was different from the matrix used in other papers (Prendini et al., and supported by the presence of patella spine 3 reduced in size.

2005; Weygoldt, 1996a) and we still recovered a tree with similar Prendini et al. (2005) found Musicodamon as either sister to Phryn-

topology. This shows that the evolution of external morphologi- ichodamon or to Damon. In our analysis, Musicodamon was placed

cal characters reﬂect similar evolutionary pathways as behavioural as sister to Phrynichodamon + Damon, in the subfamily Damoninae

repertoires and molecular sequences. The main difference was (Fig. 14).

the close relationship of Phrynichodamon and Damon (in the clade Weygoldt (1999b, 2000b, 2000a) considered Phrynichidae

Damonini), instead of Musicodamon + Damon (such as proposed in divided in two groups, Damoninae and Phrynichinae. Weygoldt

the most recent published trees) (Prendini et al., 2005; Weygoldt, (1999b) reported that Damoninae was supported by the presence

2008). of a backwardly pointed spine on the pedipalp tibia, and that

The family Phrynichidae, with all the currently accepted gen- all Phrynichinae genera share the presence of two small spines

era, was established by Weygoldt (1996b), who transferred the above the cleaning organ and complex spermatophores with bars

species Hemiphrynus machadoi Fage, 1951 and Phrynichus scul- and levers. Weygoldt (2002c), on the other hand, published four

lyi Purcell, 1901 to the genera Xerophrynus and Phrynichodamon, different models for genera relationships. The only clade that

respectively. Since then, Xerophrynus has been considered the sis- was consistently recovered was Phrynichinae. Throughout, Phryn-

ter group to all other phrynichid genera due to a combination of ichus + Euphrynichus were recognized as sister genera and were

G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55 51

Fig. 15. The preferred tree with characters plotted on branches. Black circles indicate nonhomoplastic apomorphies; empty circles indicate homoplastic apomorphies and

reversals. A. Cladogram with outgroup represented. B. Relationships amongst Phrynichidae genera.

supported by the one-segmented basitibia IV and patella spine II as Acknowledgments

part of the phrynichid hand. In the current analyses, the subfamilies

were recovered with good branch support. The synapomorphies for This work was supported by the Conselho Nacional de

the clades, however, differed from those proposed before (details Desenvolvimento Cientíﬁco e Tecnológico (CNPq), Brazil (http://

on the character states supporting the branches under topic 3.6 and cnpq.br/, process number 135839/2011-4), Coordenac¸ ão de

Fig. 15). Aperfeic¸ oamento de Pessoal de Nível Superior (CAPES), Brazil

Prendini et al. (2005) published the ﬁrst phylogeny in Amblypygi (http://www.capes.gov.br/, process number 8922-13-6), Museu

based on a large data set that included molecular, behavioural Nacional graduate program “Programa de Pós Graduac¸ ão em Zoolo-

and morphological characters. However, the work focused on the gia do Museu Nacional”, Brazil (http://www.museunacional.ufrj.

species of Damon and lacked Trichodamon among its taxa. Based br/ppgzoo/), Research School in Biosystematics (ForBio), Norway

on these results and new characters in the male and female gen- (www.forbio.uio.no) and the SYNTHESYS Project (http://www.

italia, Weygoldt (2008) hypothesized that Trichodamon was part synthesys.info/) which is ﬁnanced by European Community

of Damoninae, sister to Musicodamon and Damon. Here, however, Research Infrastructure Action under the FP7 “Capacities” Program

we found Trichodamon sister to Phrynichini within Phrynichinae, a (DE-TAF-6158 and FR-TAF-5129).

relationship supported by eight synapomorphies. We are most grateful to Peter Weygoldt, whose pioneering work

Female gonopods with claw-like projections seem to have has been inspirational in different ﬁelds of Biology and is the scaf-

evolved more than once in whip spiders. The claw-like structures fold to all current and future generations of arachnologists. Thanks

are present as a pair of soft projections in Paracharon Hansen, 1921, also to Gabriele Uhl for organizing the special issue in honour of

some Charinus Simon, 1892 species and in some Phrynoidea (excep- Peter Weygoldt and for comments that greatly improved the qual-

tions in of some Phrynichus and Damon species). The evolution ity of the manuscript. We are also thankful to Maria Elina Bichuette

of sclerotization on the claws has also evolved independently in for the donation and loan of material and for arranging an expe-

the whip spider female genitalia and might be associated with the dition to Chapada Diamantina to collect Trichodamon and to Fabio

presence of horns in the spermatophore, i.e., the hardened claws Bondezan for donating material to MNRJ. Thanks to Ivan Magalhães,

on the female genitalia are used to move the head of the sper- Leonardo Carvalho, Rodrigo Lopes Ferreira and Rogério Bertani for

matophore structure (Weygoldt, 1999a). We consider, however, providing pictures of live specimens and to Kenneth Chapin for

that a more extensive discussion on the evolution of genital char- revising the English. We are indebted to all the curators who gen-

acters in Amblypygi should be based in a larger sample size within tly provided specimens to this study (listed in the Material and

the order. methods).

By having explored the morphology and character variation on

Trichodamon, we hope to stimulate further work on little known

Appendix A. Character list

whip spider groups. The new matrix generated here for cladistic

analyses might provide a basis for reﬁning whip spider phyloge-

List of the characters used in the current analysis. Some were

netic relationships and character evolution.

modiﬁed from Weygoldt (1995, 1996a), Quintero (1986) and

52 G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55

Garwood et al. (2017), but most characters (67) are new. This is with 24. *Female genital operculum, shape of the distal border: (0) con-

the aim to better resolve the relationship of clades within Phryn- cave; (1) straight; (2) convex; (3) with broad projection; (4) with a

ichidae and understand the character evolution in the family. New small projection.

characters are indicated with an asterisk. 25. Female gonopod, shape (Figs. 6–8): (0) circular or oval (1) rect-

Carapace angular (wider than long). | Weygoldt (1996a) (in part), character

1. *Carapace, setae on the frontal margin, placement of setae socket: 25.

(0) on carapace; (1) on spines. 26. *Female gonopod, presence of claw-like projection (Figs. 6–8):

2. *Carapace, number of setae or spines/setae on the frontal margin: (0) absent (1) present. | Quintero (1986), character 4; Weygoldt

(0) 4; (1) 6; (2) 8; (3) 10; (4) more than 10. (1996a) (in part), character 25.

3. Carapace, median eyes: (0) absent; (1) present. | Weygoldt 27. Female gonopod, tegument of claw-like projection (Figs. 6–8):

(1996a) (in part), character 29 (0) soft (1) sclerotized. | Weygoldt and Hoffmann (1995), character

4. Carapace, median eyes tubercle: (0) absent; (1) presence. | 8; Weygoldt (1996a) (in part), character 25.

Weygoldt (1996a) (in part), character 29. 28. Female gonopod, tegument of claw-like projection, extent of

5. *Carapace, presence of a pair of setae on or close to the median sclerotization (Figs. 6–8): (0) only in the apex; (1) from the base to

eye tubercle (or in the position where it was supposed to be when the the apex. | Weygoldt (1996a) (in part), character 25.

tubercle is absent): (0) absent; (1) present. 29. Female gonopod, shape of the central surface (Figs. 6–8): (0)

6. *Carapace, presence of a curved crest between lateral eyes and cushion-like; (1) sucker-like; (2) ﬁnger-like. | Weygoldt (1996a) (in

lateral border of the carapace: (0) absent; (1) present. part), character 25.

7. *Carapace, presence of setae behind the triad of lateral eyes: (0) 30. *Female gonopod, presence of sclerotization in the base of the

absent; (1) present gonopod (Figs. 6–8): (0) absent; (1) present.

Sternum 31. *Male gonopod, presence of sclerotizations at the distal border

8. *Sternum, presence of tritosternum anteriorly projected of the ﬁstula (Fig. 5): (0) absent (1) present.

(Fig. 10K, L): (0) absent; (1) present. 32. *Male gonopod, presence of sclerotizations at the base of

9. *Sternum, shape of middle piece and posterior piece of sternum LoL1: (0) absent (not sclerotized) (1) present (sclerotized).

(Fig. 10K, L): (0) one plaque only (one island sternum); (1) two Leg I

plaques (pair of islands sternum); (2) one ﬂat and broad plaque; 33. Tibia I, number of pseudoarticles: (0) 16; (1) 21–25; (2) 26–45;

(3) two ﬂat and broad plaques. (3) more than 43. | Weygoldt (1996a), character 18; Garwood et al.

Chelicera (2017), character 83.

10. *Basal segment of the chelicerae, presence of tooth by the side 34. Tarsus I, presence of leaf-like hairs on the articles: (0) absent;

of the biﬁd tooth (tooth 1): (0) absent; (1) present. (1) present. | Weygoldt (1995), page 82; Weygoldt (1996a), char-

11. *Basal segment of the chelicerae, size of tooth by the side of the acter 20.

biﬁd tooth (Fig. 2): (0) low (a small sclerotized bump); (1) high (a 35. *Tarsus I, number of pseudoarticles: (0) 6–8; (1) 23; (2) 26–28;

distinguishable projection). (3) 33–39; (4) 41–43; (5) 44–47; (6) 51–59; (7) 60–79; (8) 90–110.

12. *Basal segment of the chelicerae, presence of another tooth in 36. Tarsus I, number of the article with a slit sense organ (article

the row (parallel to the second tooth, tooth 2) (Fig. 2A, F): (0) absent; has a small elongation in its distal border): (0) 11–13; (1) 17; (2) 18;

(1) present. (3) 20; (4) 21; (5) 22; (6) 25. | Weygoldt (1996a), character 19.

13. Basal segment of the chelicerae, number of teeth in the internal 37. *Tarsus I, shape of rod sensilla (Fig. 11): (0) rounded, (1) ellip-

row (Fig. 2A, D): (0) 3; (1) 4; (2) 5; (3) 6; (4) 7; (5) 8. | Quintero tical, (2) longilineal.

(1986), character 2; Weygoldt (1996a), character 1; Garwood et al. Pedipalp

(2017), character 38. 38. Position of the dorsal articulation (hinge) trochanter-femur:

14. Basal segment of the chelicerae, number of cusps on the dis- (0) anterior surface of the femur; (1) superior surface (dorsal) of

tal tooth (Fig. 2A, B, D, F): (0) 1; (1) 2; (2) 3. | Weygoldt (1996a), the femur. | Weygoldt (1996a), character 6.

character 2; Garwood et al. (2017), character 39. 39. Pedipalp trochanter, ventral, shape of the ventromedian apoph-

15. Basal segment of the chelicerae, size relation of the cusps of the ysis pointing forward: (0) normal spine; (1) seta (broad projection

biﬁd tooth (Fig. 2A, B, D, F): (0) distal (upper) larger than proximal; with acute apex). | Weygoldt (1996a), character 4 (in part);

(1) proximal (lower) larger than distal; (2) subequal. | Weygoldt Garwood et al. (2017), character 65 (in part).

(1996a), character 3. 40. *Pedipalp trochanter, number of ventral spines (not considering

16. *Basal segment of the chelicerae, number of rows of clavate or the projection cited before, if it is a spine): (0) 1; (1) 2; (2) 3; (3) 4; (4)

ﬁne and long setae on the mesal side (the additional row(s) should go 5; (5) 6; (6) 7; (7) more than 7.

from base to apex): (0) one; (1) more than two rows. 41. *Pedipalp trochanter, presence of dorsal spines: (0) absent; (1)

17. *Basal segment of the chelicerae, dorsal setae, size of setiferous present.

tubercle: (0) not projected; (1) projected. 42. *Pedipalp femur, ventral, presence of a spine or conspicuous

18. *Basal segment of the chelicerae, number of dorsal setae: (0) 1; setiferous tubercle before or inner to spine one: (0) absent; (1) present.

(1) 2; (2) 5–10; (3) 11–20; (4) more than 20. 43. *Pedipalp femur, ventral, shape of the projection before o inner

19. *Basal segment of the chelicerae, frontal ectal border, presence to spine one (Fig. 4B): (0) setiferous tubercle; (1) spine.

of setae: (0) absent; (1) present. 44. *Pedipalp femur, ventral, position of the spine/tubercle before

20. *Basal segment of the chelicerae, frontal ectal border, number spine one (Fig. 4B): (0) parallel to spine I, inner; (1) by the side of

of setae: (0) 1; (1) 2. spine I, in the same row; (2) Ventral to spine I.

21. *Cheliceral claw, number of teeth (Fig. 2C, E): (0) 1; (1) 3; (2) 45. *Pedipalp femur, ventral, presence of a spine parallel to spine

4–5; (3) 6–7; (4) 8–9; (5) 10–13. one (in addition to the aforementioned spine): (0) absent; (1) present.

22. *Cheliceral claw, presence of rows of setae between the ectal 46. *Pedipalp femur, ventral, number of spines (Fig. 4B): (0) 1; (1)

and mesal rows (on the dorsal of the claw): (0) absent; (1) present. 2; (2) 3; (3) 4; (4) 5; (5) 6.

Abdomen and genitalia 47. *Pedipalp femur, ventral, presence of small spine between spines

23. Abdomen, presence of ventral sac cover: (0) absent; (1) present. 1 and 2 in females (dorsal to the main row): (0) absent; (1) present.

| Quintero (1986), character 15; Weygoldt (1996a), character 26; 48. *Pedipalp femur, ventral, presence of small spine between spines

Garwood et al. (2017), character 124. 2 and 3 in males (dorsal to the main row): (0) absent; (1) present.

G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55 53

49. *Pedipalp patella, ventral, number of spines (Fig. 4B): (0) 1; (1) 76. *Pedipalp patella, dorsal, presence of long setiferous tubercle

2; (2) 3; (3) 4; (4) 5. or spines between spine I and the distal margin: (0) absence; (1)

50. *Pedipalp patella, ventral, presence of a small spine between presence.

spine 1 and 2: (0) absent; (1) present. 77. Pedipalp tibia, number of dorsal spines (Fig. 4A, E): (0) 1; (1)

51. *Pedipalp patella, ventral, presence of a small spine between 2; (2) 3; (3) more than 3. | Quintero (1986), character 12.

spine 2 and 3: (0) absent; (1) present. 78. Pedipalp tibia, size relation of dorsal spines (when two spines):

52. *Pedipalp patella, ventral, shape of projection between spine I (0) proximal larger then distal; (1) distal larger than proximal. |

and distal margin (Fig. 4B): (0) setiferous tubercle; (1) spine. Quintero (1986), character 17.

53. *Pedipalp patella, ventral, number of spines between spine 1 79. Pedipalp tarsus, dorsal, presence of spine above the cleaning

and distal margin: (0) 1; (1) 2; (2) 3; (3) 4. organ: (0) absent; (1) present. | Garwood et al. (2017), character 76.

54. *Pedipalp patella, ventral, size of the apical or largest (when 80. Pedipalp tarsus, dorsal, number of spines (Fig. 6A, E): (0) 1; (1)

more than one) spine between spine I and distal margin: (0) small, 2; (2) 3; (3) more than 3. | Weygoldt (1996a) (in part), characters

one third spine I; (1) long, half spine I; (2) very long, two thirds 15–16.

spine I; (3) longer than spine I. 81. *Pedipalp tarsus, dorsal, size of the distal spine (or of the single

55. *Pedipalp patella, ventral, shape of the apical or largest (when spine when only one is present): (0) small (a bit higher than a setifer-

more than one) spine between spine I and distal margin: (0) straight; ous tubercle); (1) medium (one third the size of the distitarsus); (2)

(1) curved pointing forwards. long (half the size of the distitarsus: between 40 and 50 per cent).

56. *Pedipalp tibia, ventral, number of spines (Fig. 4B, D, E): (0) 1; 82. *Pedipalp tarsus, dorsal, size relation of the two spines (or the

(1) 2; (2) 3; (3) 4. two distal spines, when more than two) (the proximal in relation to

57. *Pedipalp tibia, ventral, (when one spine) position of the spine the distal): (0) subequal; (1) two thirds; (2) one half; (3) one third.

(Fig. 4B, D, E): (0) close to proximal border of the basitarsus; (1) 83. *Pedipalp tarsus, dorsal, presence of dorsal row of setae on

close to distal border of the basitarsus; (2) in the middle. cleaning organ: (0) absent; (1) present.

58. *Pedipalp tibia, ventral, presence of setiferous tubercle with a 84. Pedipalp, fusion of the tarsus and claw: (0) not fusioned; (1)

long setae between spine I and distal border of the segment: (0) absent; fusioned. | Quintero (1986), character 11; Weygoldt (1996a), char-

(1) present. acter 14.

59. *Pedipalp tibia, ventral, presence of a row of long and thin setae Leg IV

close to distal border: (0) absent; (1) present. 85. Basitibia IV, number of articles: (0) 1; (1) 2; (2) 3; (3) 4. |

60. *Pedipalp tibia, ventral, number of setae in the row close to Quintero (1986), character 14; Weygoldt (1996a), character 23.

distal border: (0) 1–2; (1) 3–4; (2) 5; (3) more than 5. 86. *Basitibia IV, position of bt: (0) ﬁrst third; (1) middle; (2)

61. Pedipalp tarsus, ventral, presence of spine: (0) absent; (1) second third.

present. | Quintero (1986), character 16; Weygoldt (1996a) (in 87. *Basitibia IV, presence of a strongly sclerotized denticulate bor-

part), characters 15, 16. der in the distal apex of the article: (0) absent; (1) present.

62. *Pedipalp tarsus, ventral, number of setae in the ventral row of 88. *Basitibia IV, presence of a strongly sclerotized denticulate bor-

the cleaning organ: (0) 18–24; (1) 25–34; (2) 35–40. der projection in the middle region: (0) absent; (1) present.

63. Pedipalp tarsus, presence of a row of setae on the base of the 89. *Distitibia IV, presence of trichobothria bc (Fig. 12): (0) absent;

cleaning organ: (0) absent; (1) present. | Quintero (1986), character (1) present.

10; Weygoldt (1996a), character 17. 90. Distitibia IV, presence of trichobothrium nbf (Fig. 12): (0)

64. *Pedipalp coxae, position of sclerites: (0) plaques close to each absent; (1) present. | Weygoldt (1996a) (in part), character 24.

other; (1) plaques separated from each other. 91. Distitibia IV, presence of trichobothrium series sbc (Fig. 12): (0)

65. *Pedipalp coxae, dorsal, presence of a sclerotized rounded or absent; (1) present. | Weygoldt (1996a) (in part), character 24.

oval carena: (0) absent; (1) present. 92. *Distitibia IV, position of the two most proximal trichobothria

66. *Pedipalp femur, dorsal, shape of the proximal series of of the sf and sc in relation to each other (Fig. 12): (0) far from each

spines/tubercles: (0) setiferous tubercle; (1) spines. other (>0,2); (1) close to each other (0.05 mm–0.1 mm, ratio of the

67. *Pedipalp femur, dorsal, proximal series, number of spines distance by the length of the distitibia between 0.01 and 0.09); (2)

(Fig. 4A): (0) 1; (1) 2; (2) 3; (3) 4. Parallel or subparallel to each other (<0,025 mm).

68. Pedipalp femur, dorsal, number of spines (Fig. 4A): (0) 1; (1) 93. *Distitibia IV, position of the proximal trichobothria of the sf

2; (2) 3; (3) 4; (4) 5; (5) 6. | Garwood et al. (2017), character 64 (in and sc (Fig. 12): (0) same distance as the other trichobothria; (1)

part). distinctly displaced from the series.

69. *Pedipalp femur, dorsal, presence of a small spine between 94. *Distitibia IV, number of trichobothria on sf (Fig. 12): (0) 4; (1)

spines 1 and 2 in females: (0) absent; (1) present. 5; (2) 6; (3) 7; (4) 8; (5) 9; (6) 10–12; (7) 20 (8) 26.

70. *Pedipalp femur, dorsal, presence of a small spine between 95. *Distitibia IV, number of trichobothria on sc (Fig. 12): (0) 3; (1)

spines 2 and 3 in females: (0) absent; (1) present. 5; (2) 6; (3) 7; (4) 8; (5) 9; (6) 10–11; (7) 12; (8) 13; (9) 19–21.

71. Pedipalp patella, dorsal, number of spines (Fig. 4A): (0) 1; (1) 96. *Distitibia IV, presence of trichobothrium tm (the tip of the triad)

2; (2) 3; (3) 4; (4) 5; (5) 6. | Garwood et al. (2017), character 71 (in (Fig. 12): (0) absent; (1) present.

part). 97. *Distitibia IV, presence of a marked division after all trichoboth-

72. Pedipalp patella, dorsal spines forming a catching tool (Fig. 4A): ria (Fig. 12): (0) absent; (1) present.

(0) absent; (1) present. 98. Tarsomere IV, presence of pulvillus: (0) absent; (1) present. |

73. Pedipalp patella, catching tool, shape (Fig. 4A): (0) catching Quintero (1986), character 1; Garwood et al. (2017), character 97.

basket; (1) Phrynichid hand. 99. Tarsomere IV, presence of oblique slit: (0) absent; (1) present.

74. Pedipalp patella, phrynichid hand, position of spines (Fig. 4A): | Weygoldt (1996a), character 21.

(0) spines I and II positioned distally and spine III proximally; (1) 100. *Tarsomere IV, presence of weakly sclerotized area of the sec-

spines I, II and III close to the apex of the patella, or spine III ond tarsal segment: (0) absent; (1) present.

reduced/absent.

75. Pedipalp patella, phrynichid hand, ventral spine forming hand

(Fig. 6B, G): (0) spine I (0) spine II. | Weygoldt (1995), page 82;

Weygoldt and Hoffmann (1995), character 7.

54 G.S. de Miranda et al. / Zoologischer Anzeiger 273 (2018) 33–55

Appendix B. Supplementary data GeoNames, 2013. The GeoNames geographical database covers all countries and

contains over eight million placenames that are available for download free of

charge.

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