Phoneutria depilata (Strand, 1909) sp. reval.

Hazzi, Nicolas A. & Hormiga, Gustavo, 2021, Morphological and molecular evidence support the taxonomic separation of the medically important Neotropical spiders Phoneutria depilata (Strand, 1909) and P. boliviensis (F. O. Pickard-Cambridge, 1897) (Araneae, Ctenidae), ZooKeys 1022, pp. 13-50 : 13

Phoneutria depilata (Strand, 1909) sp. reval. Figs 1A, B , 4C, D , 7A-C , 8A, B , 9B, D , 10C, D

Ctenus depilatus Strand, 1910. Holotype male from Colombia ( ZMB 30615 , examined). Valerio 1983: 101, fig. 2 (female).

Ctenus peregrinoides : Strand, 1910: 318 (syntypes: two females from Guatemala, in ZMB 30717 , not examined). New synonymy .

Phoneutria depilata : Schmidt, 1954: 417-418.

Phoneutria colombiana Schmidt, 1956: 418; 1956: 28 (female holotype from Colombia, in SMF, not examined). New synonymy.

Phoneutria boliviensis : Simó & Brescovit, 2001: 74 (as senior synonym of P. depilata ); Rozwałka, Rutkowski and Bielak-Bielecki 2017: 61, fig. 1b, c (female); Hazzi et al. 2018: 112, fig. 10D (male).

Phoneutria cf. boliviensis : Cathrine & Longhorn, 2017: 13, figs 1-6 (female).

Comments.

In their revision of Phoneutria Simó and Brescovit (2001) distinguished the Amazonian specimens of Phoneutria boliviensis from the specimens from Colombia and Central America (which we identify now as P. depilata ) based on the epigynal morphology: "In specimens from Central America to Colombia it is triangular, with a wide base and a narrow apex, but in specimens from Ecuador to Bolivia the apex is more rounded". Based on the fact that Simó & Brescovit were able to distinguish these epigynal morphological differences among these two Phoneutria species and that the only species of Phoneutria in the trans-Andean region is P. depilata , we suggest that Ctenus peregrinoides (from Guatemala) is a junior synonym of P. depilata . Strand described Ctenus signativenter in 1909 based on immature syntypes from Paramba, Ecuador (one male and two female syntypes, all immatures, 3500 ft, 28 April 1898, Rosenberg leg., in ZMB 306 , not examined). We have designated Ctenus signativenter as a nomen dubium because the exact identity of this species cannot be ascertained with immature specimens, but we note that the type locality suggests that the C. signativenter syntypes belong to P. depilata . Based on the epigynal morphology ( Schmidt 1956, fig.3), we synonymize Phoneutria colombiana with P. depilata . Both Ctenus peregrinoides and Phoneutria colombiana had been synonymized with P. boliviensis by Simó and Brescovit (2001) .

Other material examined.

Nicaragua: Región Autónoma de la Costa Caribe Sur: one female, Escondido River (12.1065°N, 84.0256°W, 10 m), 12.VII.1892, C.W. Richmond ( USNM) . Panama: Panama: one male, Pearls Island, San Jose (8.270219°N, - 79.112038°W, 30 m), 02.IV.1944, J.P. Morrinson ( USNM) ; Bocas del Toro: one female, Changinola , El Silencio (9.3845°N, 82.5356°W, 20 m), E. Marrango ( USNM) , one male and one female, Gamboa (9.1176°N. 79.6959°W, 50 m), 05.XIII.2018, N. Hazzi and S. Maneses ( MCZ IZ 162179 ) ; Chiriquí: one male, one female, Puerto Amuelles (8.2841°N, 82.8691°W, 10 m), 25.VII.2018, N. Hazzi, J. Bernal, T. Rios ( MCZ IZ 162180 ) . Costa Rica: Alajuela: one male and one female, San Ramón, Muelle San Carlos (10.4335°N, 84.5622°W, 990 m) ( MZUCR) ; one male, Canalete, Upala (10.8358°N, 85.0437°W, 950 m), 25.XI. 1979 ( MZUCR) , two females and two males, San Carlos, Peje Viejo (9.644°N, 82.7516°W), F. Garray ( MZUCR) , 00. X.1999; Limón: one female, Guapiles (10.2217°N, 83.7705°W, 450 m), 30.IX.1977 ( MZUCR) ; one female, Batan (10.0842°N, 83.3364°W), 12.VIII.1984, Federico Muñoz ( MZUCR) , Reserva Biológica Hitoy Cerere (9.647°N, 83.0709°W); one female, Talamanca, Amumbri de Bratsi (9.6501°N, 82.7542°W) ( MZUCR) ; Puntarenas: one female, Rincon de Osa (8.6986°N, 83.4876°W, 20 m), 00. III.1967, C. Valerio ( MZUCR) ; one male, Conte, Casa de la Guardia Rural (8.443°N, 83.0401°W, 990 m), 14.VII.1984; one female and one male Cirenas (9.7199°N, 85.2119°W, 10 m), 00. VI.2018, N. Hazzi ( MCZ IZ 162181 ) , Cartago: one female, Turrialba, Bajo Pacuare (9.862°N, 83.5203°W, 730 m), 25.IV.1983, F. Calderón ( MZUCR) ; Heredia: one juvenile, Sarapiqui, Reserva Tirimbina (10.4164°N, 84.1199°W, 160 m), 10. VI.2019, N. Hazzi; one male, San Isidro (10.0182°N, 84.0551°W, 1300 m) ( MCZ IZ 162183 ) . Ecuador: Esmeraldas: Esmeraldas, Caimito (0.7005°N, 80.0741°W, 10 m), 1.10.2019, N. Hazzi ( MCZ IZ 162184 ) . Colombia: Chocó: one female, Bahía Solano, Ciudad Mutis (6.2186°N, 77.4075°W, 5 m), 5. V.1973 ( ICN-AR) ; one juvenile, Acandí, Capurgana (8.6338°N, 77.3503°W, 15 m), 08.X.2007, C. Duran ( MPUJ) ; Cundinamarca: Fusagasugá (4.3439°N, 74.3678°W, 1600 m), 00. XII.2001 (ICN-AR-5258); Yacupi, vereda La Oscura (5.45°N, 74.35°W, 1190 m), 03.I.2000 (ICN-AR-907); Quipile, Vereda el Trigo (4.7455°N, 74.5341°W, 1300 m); 28.V.2000 (ICN-AR-908); Pandi, vereda El Caucho (4.1911°N, 74.4875°W, 910 m), 20.IX.2000 (ICN-AR-903); La Mesa (4.6333°N, 74.4666°W, 1080 m), 16.VI.1983 (ICN-AR-343); Nilo, Pueblo Nuevo (4.3166°N, 74.6333°W, 480 m), 12.I.1980 (ICN-AR-303) ; Santander: Chima, El Rodeo (6.3458°N, 73.3736°W, 113 m); 03.I.1970 (ICN-AR-315); one female, Suaita (6.10°N, 73.45°W, 1550 m), 10. V.1998 (ICN-AR-5261) ; Antioquia: one female, Urabá, Apartadó (7.8856°N, 76.6347°W, 20 m), 00. VII.2003 (ICN-AR-5259); one female, Urabá, Turbó (8.0981°N, 76.7317°W, 20 m) (ICN-AR-5260); one female, Urabá, Chigorodó (7.6769°N, 76.6864°W, 20 m), 00. IX.2003 (ICN-AR-5262) ; Cauca: one male, PNN. Gorgona Island (2.98°N, 78.1825°W, 5 m), 00. XII.2003 (ICN-AR-5263); one female and five males, Caloto, vereda Morales (3.0369°N, 76.4116°W, 1100 m), 00. X.2009, N. Muriel (MUSENUV) ; Valle del Cauca: one female and one male, Cali, El Aguacatal (3.4617°N, 76.5560°W, 1000 m), N.Hazzi (MUSENUV); one female, Cali (3.4616°N, 76.5560°W, 1000 m), 20.X.1982 (MUSENUV); one female , same locality 00. X.1986 (MUSENUV); one male, Cali, Barrio El Refugio (3.4372°N, 76.5225°W, 1000 m), 00. XI.1995 (MUSENUV) one female, Dagua , El Palmar (3.6033°N, 76.6463°W, 1300 m), 27.IX.1994 (MUSENUV); one female, Roldanillo (4.4147°N, 76.1547°W, 950 m) (MUSENUV); KM 30 , El Carmen (3.566°N, 76.6475°W, 1400 m); 10.XII.2008, N. Hazzi (MUSENUV); one male, Buga, Liceo de los Andes (3.8833°N, 76.2986°W, 950 m), 12.XII.2009, N. Hazzi (MUSENUV), one female, Buenaventura, Reserva Natural San Cipriano (3.8833°N, 76.9166°W, 180 m), 00. II.2012, N.Hazzi and J. Moreno (MUSENUV) ; Boyaca: Puerto Boyaca, Puerto Romero, vereda Los Quinchos (5.8375°N, 74.3408°W, 160 m) ; Risaralda: one female, Pereira (4.8133°N, 75.6961°W, 1400 m) (MUSENUV); one male, Balboa (4.9517°N, 75.9572°W, 1400 m); 10.XI.1998 (ICN-AR-5264) ; Quindío: one female, Montenegro, La Tebaida (4.5542°N, 75.7181°W, 1200 m), 27.I.2010, N. Hazzi (MUSENUV); one female, Montenegro , Pueblo Tapado (4.5178°N, 75.7847°W, 1250 m), 00. X.2004 (MUSENUV) ; Caldas: Samaná, Norcasia, Carrisa (5.5666°N, 74.8833°W, 600 m); 10.X.1992 ( ICN-AR342 ) .

Diagnosis.

Males of P. depilata resemble those of P. boliviensis by the truncated apex of the RTA (Fig. 9C, D ), but differ from this and the remaining Phoneutria species by the lateral pronounced projection of the locking lobes visible in ventral view (Fig. 9B ). In addition, males present an embolus with an internal bulge which is absent in P. boliviensis ; and a much larger tegulum (Figs 7B , 9B ). Females of P. boliviensis also resemble those of P. depilata by the general configuration of the epigynum but differ by the narrow area of the EMF (Fig. 8A ), copulatory ducts slightly sclerotized (Fig. 8A ), and large spermatheca heads (Figs 8B , 10D ). In addition, both males and females of P. depilata can be distinguished from P. boliviensis and the remaining Amazonian species ( P. perty and P. fera ) by the four conspicuous series of yellow dots in the ventral side of the abdomen (this character is also present in Phoneutria eickstedtae Martins & Bertani, 2007).

Description.

Male (from Puerto Amuelles, Chiriquí, Panama, MCZ IZ 162180 -1). Coloration (Figs 1B , 4C, D ): Carapace brown with a longitudinal black line. Ocular area with brown setae and back oblique band from PLE to anterior dorsal shield of prosoma edge. Chelicerae brown with reddish setae. Sternum, endites and labium yellowish-brown. Abdomen yellow-brown dorsally, with yellow dots; ventrally dark brown with four conspicuous series of yellow dots. Total length 23.21. Carapace 12.38 long and 9.94 wide, eye diameters: AME 0.46, ALE 0.34, PME 0.55, PLE 0.55. Clypeal height 0.45, sternum 5.03 long, 4.65 wide; labium 1.62 long, 1.62 wide. Sternum 2.58 long and 2.50 wide, labium 1.99 long and 2.15 wide, endites 2.93 long and 1.70 wide. Leg measurements: I: femur 14.65, patella 5.77, tibia 15.75, metatarsus 14.31, tarsus 3.93, total 54.41; II: 13.72, 5.19, 13.85, 12.63, 3.30, total 48.69; III, 11.12, 4.95, 10.21, 10.09, 3.17, total 39.54; IV 13.56, 4.86, 13.25, 16.35, 3.96, total 51.98. Leg spination: I tibia v2-2-2-2-2, d1-1-1, p0-1-0, r1-1-0, metatarsus v2-2-2, p1-0-0 r1-0-0, II tibia v-2-2-2-2-2, d1-1-1, p1-1-0, r1-1-0, metatarsus v2-2-2, p1-0-0 r1-0-0, III v2-2-2, d1-1-1, p1-0-1-0, r1-0-1-0, metatarsus v2-2-2-2, p1-1-2, r1-1-2, IV tibia v2-2-2, d1-1-1, p1-0-1-0, r1-0-1-0, metatarsus v2-2-2-2, d0-1-0, p1-1-2, r1-1-2. Palp: RTA small and truncated at the apex (Figs 7C , 9D ); embolus curve with internal bulge (Figs 7B , 9B ); cup-shaped median apophysis constrain at the base (Figs 7B , 9B ); conductor membranous, hyaline and C-shaped (Figs 7B , 9B ); tegulum large with probasal rounded projection (Figs 7B , 9B ).

Female (from Puerto Amuelles, Chiriquí, Panama, ( MCZ IZ 162180 -2). Coloration (Figs 1B , 4C, D ): Carapace brown with a longitudinal black line. Ocular area with brown setae and back oblique band from PLE to anterior dorsal shield of prosoma edge. Chelicerae brown with reddish setae. Sternum, endites and labium yellowish-brown. Abdomen yellow-brown dorsally, with yellow dots; ventrally dark brown with four conspicuous series of yellow dots. Total length 25.77. Carapace 12.56 long and 9.82 wide, eye diameter: AME 0.47, ALE 0.36, PME 0.60, PLE 0.65. Clypeal height 0.89, sternum long 5.15 and 4.76 wide, endites 3.89 long and 2.30 wide, labium 1.33 long and 1.59 wide. Leg measurements: I: femur 13.43, patella 5.09, tibia 12.78, metatarsus 9.99, tarsus 3.33, total 44.62; II, 11.22, 5.00, 11.57, 9.30, 3.00, total 40.09; III 7.83, 4.00, 7.89, 7.60, 2.50, total 29.83; IV 12.00, 4.62, 9.83, 12.72, 3.15, total 42.32. Leg spination: tibia I-II v2-2-2-2-2, metatarsus I-II v2-2-2-2-2; III tibia v2-2-2, d1-1-1, p1-0-1-0, r1-0-1-0; metatarsus v2-2-2-2, p1-1-2, r1-1-2; IV tibia v2-2-2, d1-1-1, p1-0-1-0, r1-0-1-0, metatarsus v2-2-2-2, d0-1-0, p1-1-2, r1-1-2. Epigynum (Figs 6A , 10C ): middle field convex with straight edges, anteriorly divergent and posteriorly convergent; lateral field with lateral apophysis. Vulva (Figs 6B , 10D ): copulatory ducts slightly sclerotized, enlarged spermatheca heads, fertilization ducts small and posteriorly located.

Variation.

Males (n = 5): Total length 21.00-26.37, carapace 11.26-13.75, femur I 13.27-15.84. Females (n = 8): Total length 25.77-34.00, carapace 12.56-15.00, femur I 13.43-14.36.

Distribution.

Trans-Andean region (0-1700 m) in Ecuador, Colombia, Panama, Costa Rica, Nicaragua, Honduras and Guatemala.

Natural history.

This species is found in disturbed habitats associated with both dry and humid tropical forests (0-1700 m), usually on the ground with sparse litter and low vegetation ( Hazzi 2014). The range of eggs per egg sac is 430-1300, and spiderlings emerge 28-34 days after the egg sacs are produced. Sexual maturity occurs after 14-17 molts, and spiders mature 300-465 days after emerging from the egg sac ( Hazzi 2014). Valenzuela-Rojas et al. (2020) reported that P. depilata is an euryphagous predator with a broad diet made up predominantly of arthropods and to a lesser extent of small vertebrates ( Gekkonidae , Hylidae , and Sphaerodactylidae ). There are human bite records of this species reported in Costa Rica and in banana plantations in Colombia ( Florez et al. 2003). All the cases reported have occurred with adults, and most of them have presented mild to moderate envenomation symptoms, with only one patient presenting severe symptoms such as renal failure ( Florez et al. 2003). Estrada-Gomez et al. (2015) partially characterized the venom of this species, detecting Ctenitoxin-Pb48 and Ctenitoxin-Pb53, which showed a high homology with other Ctenitoxins (family Tx3) from P. nigriventer , P. keyserlingi and P. reidyi affecting voltage-gated calcium receptors (Cav 1, 2.1, 2.2 and 2.3) and NMDA-glutamate receptors. Valenzuela-Rojas et al. (2019) found that the venom of P. depilata was significantly more effective on vertebrate (geckos) than invertebrate (spiders) prey in both LD50 and immobilization time. In addition, males had slightly more toxic venom (LD50) to geckos and much more toxic venom to spiders when compared to females ( Valenzuela-Rojas et al. 2019). For two periods, March to May and October to November, adult males and females with egg sacs are always found in homes in the Inter-Andean Cauca Valley of Colombia. This likely indicates two reproductive peaks that coincided with the two rainy seasons during those same periods (N. Hazzi, unpub. data).

Figures

Figure 1. A-D Habitus of Phoneutria spp. A female of P. depilata with eggs sac (from Chiriqui, Panama) B female of P. depilata (from Barro Colorado Island, Panama) C female of P. boliviensis (from Madre de Dios, Peru) D male of P. boliviensis (from Napo, Ecuador).

Figure 4. A, B dorsal view of the carapace and ventral view of the abdomen of P. boliviensis (male from from Finca Las Piedras, Madre de Dios, Peru) C, D dorsal view of the carapace and ventral view of the abdomen of P. depilata (male from Chiriqui, Panama). Scale bars: 2.00 mm.

Figure 6. Phoneutria boliviensis (Finca Las Piedras, Madre de Dios, Peru), female genitalia A epigynum, ventral view B vulva, dorsal view. CD = copulatory duct, ELA = epigynal lateral apophysis, ELF = epigynal lateral field, ELG = epigynal lateral guide, EMF = epigynal middle field, FD = fertilization duct, HS = head of spermatheca, PL = posterior lobe, S = spermatheca. Scale bar: 1.00 mm.

Figure 7. Phoneutria depilata (from Puerto Amuelles, Chiriqui, Panama), left male palp A prolateral view B ventral view C retrolateral view. Scale bar: 2.00 mm.

Figure 8. Phoneutria depilata (from Puerto Amuelles, Chiriqui, Panama), female genitalia A epigynum, ventral view B vulva, dorsal view. CD = copulatory duct, ELA = epigynal lateral apophysis, ELF = epigynal lateral field, ELG = epigynal lateral guide, EMF = epigynal middle field, FD = fertilization duct, HS = head of spermatheca, PL = posterior lobe, S = spermatheca. Scale bars: 1.00 mm.

Figure 9. A, B ventral view of the male palp of P. boliviensis (from Pucallpa, Peru) and P. depilata (from Gamboa, Panama), respectively C, D retrolateral tibia apophysis of P. boliviensis and P. depilata, respectively. Scales bars: 0.10 mm (A); 0.20 mm (B); 0.10 mm (C); 0.05 mm (D). C = conductor, E = embolus, IB = internal bulge, LL = locking lobes, MA = median apophysis, ST = subtegulum.

Figure 10. A, B epigynum and vulva (dorsal view) of Phoneutria boliviensis (from Pucallpa, Peru) C, D epigynum and vulva (dorsal view) of Phoneutria depilata (from Caimito, Esmeraldas, Ecuador). ELA = epigynal lateral apophysis, EMF = epigynal middle field, FD = fertilization duct, HS = head of spermatheca, PL = posterior lobe, S = spermatheca. Scales bars: 0.20 mm (A), 0.20 mm (B), 0.30 mm (C), 0.30 mm (D).