Gastrotheca turnerorum, Carvajal-Endara & Coloma & Morales-Mite & Guayasamin & Székely & Duellman, 2019

Carvajal-Endara, Sofía, Coloma, Luis A., Morales-Mite, Manuel A., Guayasamin, Juan M., Székely, Paul & Duellman, William E., 2019, Phylogenetic systematics, ecology, and conservation of marsupial frogs (Anura: Hemiphractidae) from the Andes of southern Ecuador, with descriptions of four new biphasic species, Zootaxa 4562 (1), pp. 1-102 : 48-56

Gastrotheca turnerorum sp. nov.

urn:lsid:zoobank.org:act:B72F71A3-671F-4F89-91D5-2410C1D0B6DF

Holotype. CJ 393 ( Fig. 18 ), an adult female (collected as tadpole and raised in captivity), from Laguna Negra de Jimbura , Parque Nacional Yacuri, Amaluza, 3406 m (04° 42' 44.24" S, 79° 25' 42.38" W), Loja Province, Ecuador, one of a series collected on 12 June 2011 by Elicio E. Tapia, Sofía Carvajal-Endara and Henry Grefa.

Paratypes. (Total 9: 6 males, 2 females, 1 juvenile). Ecuador: Loja: CJ 394–5 (female, male), 415–7 (males, juvenile), 1386 (female), and KU 335390 (male), collected with the holotype. CJ 7823 (male, collected as tadpole and captive raised), from Parque Nacional Yacuri, Amaluza, 3331 m (04° 43' 25.22" S, 79° 26' 15.47" W), Loja Province , Ecuador, one of a series collected on 7 July 2016 by Dan Cogǎlniceanu, Diana Székely and Paul Székely. Zamora Chinchipe : MUTPL 221 , male from Reserva Tapichalaca , 3073 m (04° 28' 55.58" S, 79° 09' 29.76" W), collected on 9 December 2014 by Diego Armijos-Ojeda .

Referred specimens. Ecuador: Zamora Chinchipe : QCAZ 9575 (captive raised tadpoles and juveniles) from Parque Nacional Podocarpus, Lagunas del Compadre, 3205 m (04° 10' 29.24" S, 79° 06' 59.54" W), on 1 December 1994 by Jenny Rudston ; QCAZ 47299 (tadpole) , QCAZ (sc 29154) (female) from Parque Nacional Podocarpus, Lagunas del Compadre, 3205 m (04° 10' 29.24" S, 79° 06' 59.54" W), on 20 October 2009 by Elicio E. Tapia .

Diagnosis. Included in the genus Gastrotheca by having a closed brood pouch on dorsum of female. A moderately large species (54.0– 58.2 mm SVL in females, n = 3; 50.0– 55.6 mm SVL in males, n = 4), with tibia length 37¯42% SVL, shorter than foot; (2) interorbital distance slightly greater than width of upper eyelid; (3) skin on dorsum areolate, not co-ossified with skull, lacking transverse ridges; (4) supraciliary processes absent; (5) heel lacking calcar or tubercle; (6) tympanic annulus smooth; (7) Finger I slightly shorter than Finger II, width of discs much wider than digits; (8) fingers unwebbed; (9) foot webbing between external toes extending to antepenultimate subarticular tubercle on Toe IV, to penultimate subarticular tubercle on Toe V; (10) in life, dorsum uniform green without dark paravertebral marks; (11) head markings consisting of pale labial and canthal stripes formed by a series of small bronze dotes; (12) dorsolateral stripe present, also consisting in a series of small bronze dotes; (13) flanks brown and groin green both with or without a few cream spots; anterior surfaces of thighs dark brown, posterior surfaces of thighs bluish brown with numerous cream tubercles proximal to the vent; (14) venter dark brown with uniformly distributed cream spots; gular region dark brown; (15) brood pouch single, dorsal.

Gastrotheca turnerorum most closely resembles three other species in southern Ecuador, G. pseustes , G. elicioi , and G. litonedis . Gastrotheca turnerorum differs from all of them by having a different skin texture on the dorsum, and a distinctive color pattern (compare Figs. 10J , 19–20 vs 10A–I, K, L). The dorsal skin is areolate in G. turnerorum , whereas it is weakly areolate or smooth in G. pseustes , finely granular in G. elicioi , and smooth in G. litonedis . In G. turnerorum the venter is dark brown with uniformly distributed cream spots, whereas it is cream with dark marks in G. pseustes and G. elicioi and pale brown-gray in G. litonedis . The labial stripe consists of a series of small bronze dots in G. turnerorum , and mostly uniform cream in G. pseustes , G. elicioi , and G. litonedis . Gastrotheca pseustes and G. elicioi have a dark brown canthal stripe, whereas G. turnerorum has a canthal stripe formed by a series of small bronze dots.

Gastrotheca turnerorum is the sister species of G. aguaruna + G. yacuri , with a genetic distance of at least 2.85 % (in a DNA dataset of 438 bp, 16S gene). The Peruvian G. aguaruna differs from G. turnerorum by having a weakly granular to smooth dorsal skin (areolate in G. turnerorum ), Fingers I and II equal in length (Finger I shorter in G. turnerorum ), and a cream venter with dark fleck or spots (venter dark brown with uniformly distributed cream spots in G. turnerorum ).

Description of the holotype. An adult female ( Fig. 18 ) that was collected as a tadpole and raised in the laboratory; body moderately robust; SVL 54.0 mm; head wider that long; snout rounded in dorsal view, bluntly rounded in profile; canthus rostralis round in section; loreal region concave; lips rounded; top of head flat; interorbital distance 89% of width of upper eyelid; internarial area flat; nostrils not protuberant, directed anterolaterally, posterior to level of anterior margin of lower jaw; diameter of eye greater than its distance from nostril; tympanum round, separated from the eye by distance about equal to diameter of tympanum; tympanic annulus barely evident;, supratympanic fold moderately weak, extending from behind the tympanum to the insertion of the forelimb. Dentigerous vomerine processes narrowly separated medially, each bearing five teeth.

Arm robust; ulnar tubercles absent; hand and fingers moderately large (TFL 34% of SVL); fingers unwebbed; discs large and rounded, width of disc of Finger III greater that diameter of tympanum; relative lengths of fingers I<II<IV<III; subarticular tubercles prominent, round, conical in profile, none bifid; supernumerary tubercles, conical; palmar tubercle bifid, prepollical tubercle large, elliptical. Hind limb robust; tibia length 38% of SVL; foot length 46% of SVL; calcar and tarsal tubercles absent; inner tarsal fold approximately ¼ the length of the tarsus; outer metatarsal tubercle rounded; inner metatarsal tubercle elliptical elevated; toes moderately long; relative length of toes I<II<III<V<IV; basal webbing between Toes I and II; webbing formula for other toes II1— 2III 1— 2.5IV2— 1V; subarticular tubercles moderately large, rounded; supernumerary tubercles, numerous, and rounded.

Skin on dorsum weakly areolate; skin on flanks coarsely areolate; skin on throat, venter surfaces of thighs, and arms heavily areolate; skin on belly areolate; skin on venter surface of shanks smooth; numerous white tubercles ventrolateral to cloacal opening. Tongue broad, suboval, not notched posteriorly, fully attached to mouth floor. Pouch opening V- shaped with anterior border at level of posterior edge of sacrum.

Coloration in life. The dorsal surfaces of the head, body, and limbs are green; the inner and outer surfaces of the forearm, thighs, and shanks are brown ( Fig. 18 ). Head markings are canthal and labial stripes that consist of a series of small bronze dots. The labial stripe continues to the insertion of the forelimb. The dorsolateral stripe also consists of a series of small bronze dots. The flanks are bronze-brown with some small white stippling; the groin is green. The anterior surfaces of the thighs are dark brown with some cream stippling; the posterior surfaces of the thighs are dark brown with cream tubercles lateral and below the vent. The ventral surfaces are dark brown with uniformly distributed cream spots. The iris is yellow-cream with brown reticulations and a brown horizontal bar across the eye.

Coloration in preservative. The dorsum is uniform bluish-gray. The pale labial, canthal, and dorsolateral stripes formed by a series of small bluish gray dots. The labial stripe continues to the insertion of the forelimb. The flanks, groin, and anterior surfaces of thighs are uniform dull gray; the posterior surfaces of thighs are dark gray with numerous white tubercles lateral to, and below, the cloacal opening. The ventral surfaces are uniform dark bluish-gray.

Measurements (in mm). SVL: 54.0, TIBL: 20.5, FL: 24.7, HL: 17.8, HW: 20.5, IOD: 4.9, EW: 5.6 IND: 3.4, ED: 5.6, EN: 4.3, TD: 2.3, FFL: 9.9, TFL: 18.5, TFD: 3.4.

Variation. Morphometric variation of three females and three males is summarized in Table 3. Females are larger than males (55.9± 2.1 mm; 52.7.± 2.5 mm). The skin on the dorsum varies from weakly to coarsely areolate. All adults have a supratympanic fold, which usually extends from the posterior edge of the tympanum to a point above the insertion of the forelimb.

Color variation in preservative. All preserved specimens have a uniformly bluish gray dorsum; labial, canthal, and dorsolateral stripes are formed by a series of small brown dots. The dorsal surfaces of hands and feet also have brown dots. The flanks, groin, and anterior surfaces of the thighs are uniform dull gray, but in some specimens the flanks are covered by small dark gray dots. The posterior surfaces of the thighs are dark gray with numerous white tubercles lateral to, and below the cloacal opening; a short, fragmented supracloacal stripe is present in some individuals. The ventral surfaces are uniform dark bluish-gray.

Color variation in life. ( Figs. 10J , 18–19 ). The dorsum is uniform green (e.g., CJ 1386) or brown (e.g., CJ 7823). In CJ 1386, the dorsal surfaces of limbs are green, whereas the inner and outer surfaces of the forearms, thighs, and shanks are brown. Dorsal surfaces of hands and feet have a pattern of brown dots over a lighter background. Head markings are like those of the holotype; a dorsolateral stripe is present in all specimens. The flanks are bronze-brown with or without white stippling; the axillae and groin are green, with a bluish suffusion in some specimens. The anterior surfaces of thighs are dark brown with or without cream stippling and, and the posterior surfaces of thighs are dark brown with cream tubercles lateral to, and below, the vent. The ventral surfaces are dark brown with uniformly distributed cream dots, but some specimens have larger cream spots, thereby resulting in a paler venter.

Tadpoles. Tadpoles belong to Type IV tadpole of Orton (1953), and the exotroph, benthic ecomorphological guild. All measurements are expressed in millimeters. The following description is based on a specimen in Stage 39, from a series (CJ 1959) obtained from a pond at Laguna Negra de Jimbura, Parque Nacional Yacuri, 3406 m, Loja Province, Ecuador, by Elicio E. Tapia, Sofía Carvajal-Endara, and Henry Grefa on 12 June 2011 ( Fig. 5F ). Total length 61.3, body length 23.5 (38% of total length). Body robust, ovoid in dorsal and lateral views, slightly depressed; throat slightly concave in lateral profile; body width at level of spiracle 14.7, and height at same position 11.9; head width at level of eyes 12.9. Lateral-line system not evident. Nostril medium sized (in proportion to body length), ovoid, protruding, with a fleshy annulus, its opening directed anterolaterally. Snout–nostril distance 3.7. Eyes positioned and directed dorsally, eye length 2.4, eye width 2.2. Spiracle sinistral, located at midbody level; spiracular opening oriented posteriorly; distance from tip of snout to spiracle opening 15.9; spiracle end rounded, not free, attached to body wall, inner wall of spiracle not evident; tube length 3.4, tube transverse width 1.4. Vent tube dextral, the opening oriented posteriorly, tube length 4.0, tube transverse width 2.6. Tail length 38.8, caudal musculature robust in the two-thirds proximal to body, narrowing gradually until tail terminus; tail muscle height 5.4, tail muscle width 4.8; caudal fins thin at proximal half of tail, getting higher on distal half and raising near tail–body junction, dorsal fin height 3.5, ventral fin height 3.7; maximum height of tail 12.7; tail tip rounded, tail musculature not reaching fin terminus.

Oral disc small, ventral, located near tip of snout, not protruding laterally beyond body, not visible dorsally; transverse width 5.6. It is surrounded by an uniserial row of marginal papillae, interrupted medially in upper lip; lower lip papillae alternating in and out, giving the appearance of two series; upper lip with 18 papillae on right side and 17 papillae on left side; lower lip with 42 marginal papillae; upper jaw sheath medium-sized, forming a finely serrated, smooth arch, height 0.4, transverse width 3.3 (59% of oral disc width); lower jaw sheath V- shaped, open and finely serrated, width 2.4, height 0.7. Labial tooth row formula 2/3(1), tooth rows lengths: A1: 4.7, A2: 4.0, P1 right row 1.9, P1 left row 2.1, P1 gap 0.1, P2: 3.6, P3: 3.5. ( Fig. 6E ).

Color in preservative. Dorsum dull gray, with darker areas on flanks, above the eyes and on the throat; body contour and snout translucent. Caudal musculature and fins with scattered, white spots, densely arranged near tailbody junction; fins otherwise translucent. Venter dark gray; eyes lavender gray, oral apparatus translucent.

Color in life. (CJ 1957, Stage 36). Fig. 5F . In dorsal and lateral views, body tan, speckled with black; areas around the snout are lighter. Venter cream with black markings, semi-translucent; guts visible as a darker area; throat translucent with small cream flecks; gills evident as a red hue. Caudal musculature reddish-pink in proximal half, decreasing its intensity towards distal half; myomeres and nerves barely visible; caudal musculature and fins with cream marks, clustered in dorsal line of caudal musculature, otherwise caudal fins translucent. Legs cream. Oral apparatus light cream. Iris copper-yellow, with small black reticulations.

Variation. Variation of 26 meristic characters of tadpoles in Stages 35–39 (CJ 1959) are shown in Table 7. Total length varies between 61.3 (Stage 39) and 75.0 (Stage 35); tail length proportion varied from 63.2 to 67.0 until Stage 39; labial tooth row formula was 2/3(1). Number of marginal papillae varied among specimens and Gosner stages, variation in lower lip papillae is high (42–57).

We documented changes in coloration during ontogenetic development of CJ 1958–9 ( Fig. 20 ). At Stage 36, the dorsum and flanks are pale brown with dark brown areas on posterior body and flanks. By Stage 42, dorsal surfaces of body and limbs are uniform green; fine, cream, dorsolateral stripes are present, extending to midbody. Cream stripes border the outer dorsal margins of the limbs. At Stage 46, dorsal surfaces of body and limbs have more well-defined cream stripes, and a cream labial stripe; the canthus rostralis is green, and remaining flanks are mostly dark brown with an upper diffuse black-stripe. Dorsal surfaces of fingers and toes are brown except on finger and toe discs, which are yellowish-cream. The iris is copper-yellow, lacking the brown horizontal band that is observed in adults.

Comparisons. Tadpoles of Gastrotheca turnerorum may occur in sympatry with those of G. elicioi , G. lojana , G. psychrophila , and G. pseustes , in the Loja-Abra de Zamora region. Gastrotheca turnerorum differs from G. elicioi by lacking a dorsal gray-pigmented fin that abruptly arises from the body; from G. lojana by having a more rounded tail terminus and having bold cream marks in a dorsal line of caudal musculature, and from G. pseustes by having a more rounded tail terminus (compare in Fig. 5 ). For G. psychrophila , see remarks under G. elicioi tadpole account.

Distribution and ecology. Gastrotheca turnerorum only is known from three localities in the Cordillera Oriental of the Andes in southern Ecuador. These localities are in Parque Nacional Yacuri, Parque Nacional Podocarpus, and Reserva Tapichalaca in Zamora Chinchipe and Loja provinces. Its elevational range is 3073–3406 m in an area of extent of occurrence of about 450 km 2.

This mostly nocturnal, semiarboreal species inhabits mainly paramos and a few forests in the Evergreen Shrub and Herbazal of Paramo, and the Evergreen Montane Forest of Catamayo-Alamor (Ministerio de Ambiente del Ecuador 2012), where the average annual rainfall is 895–1278 mm and the average annual temperature is 10.4– 13.5 °C ( Fick & Hijmans 2017).

At the Lagunas del Compadre in the Parque Nacional Podocarpus, a gravid female was collected on 1 December 1994. It deposited tadpoles on 12 December in the laboratory, some of them were raised, and others were preserved. On 20 September 2009, another female with eggs in her pouch was found at the same locality. It was sitting on moss at approximately 2 m from the Río Sabanilla, which is about 1.5 km from Lagunas del Compadre. The holotype, from Laguna Negra de Jimbura in the Parque Nacional Yacuri ( Fig. 11C ), was found at the edge of a pond about 3 x 2 m at the edge of a lagoon, at 14:00 h. The water temperature was 16.4° C, and water pH was 5.3. Eighteen tadpoles were collected at this pond. Another group of tadpoles was found at 18:00 h; at the same locality in another lagoon, the water temperature was 7.4 ° C. Strong winds blow across the lagoon, and only a small patch of forest remained at one border (Elicio E. Tapia field notes, 12 June 2011). A brooding female is depicted in Figure 10J .

Conservation status. We suggest that Gastrotheca turnerorum should be considered as an Endangered species according to criteria B2ab(i,ii,iii) of the IUCN Red List. Although this species occurs at the Yacuri and Podocarpus National Parks, we suggest this conservation status because of its small known area of occurrence (159 km 2) that is vulnerable to improperly regulated tourism activities ( Aguirre 2001), introduced species such as trout, climate change, and pathogens. Laguna Negra de Jimbura has suffered the synergistic effects of agriculture, cattle and sheep raising, fires, introduced species, pesticide use, and unregulated tourism activitites.

Etymology. The specific name turnerorum is a latinized word that honors the Turner family. As unique as this marsupial frog is to the amphibian world, the Turner family stands out in their exceptional, unwavering and ever- growing commitment to conservation of the world natural resources. From Ted Turner’s pioneering efforts to protect very large land areas and restore them to their original and natural states of clean water and abundant fauna and flora to granddaughter Elizabeth’s awareness-raising book “Our friends the frogs,” there are multiple generations of active conservationists with a true appreciation for the value of all of our natural resources. In 1991, Laura Turner Seydel (with father Ted) co-founded the Captain Planet Foundation and continues to work diligently to inspire the same appreciation for conservation and sustainable living in the next generation of young people who will surely be making big decisions that will affect the health of our planet for themselves and their own grandchildren. Through the camera’s eye, Rhett Turner has managed to put conservation issues such as the pollinator perils and amphibian crisis in front of millions of people. Through the Turner Endangered Species Fund, there is hope for dozens of threatened species of plants and animals in the US and abroad that was not there before. Together, the Turner family has put their hearts, souls, and personal resources into helping make the planet a better place for the next generation.

Comments. Gastrotheca turnerorum belongs to the subgenus Gastrotheca as reported as species C in Duellman (2015: Fig 12.1).

Figures

FIGURE 5. Live tadpoles of: (A) Gastrotheca cuencana (CJ 1945, Stage 37), from Cuenca, Azuay Province, (B) Gastrotheca litonedis (CJ 6813, Stage 37), from Laguna de Busa, San Fernando, Azuay Province, (C) Gastrotheca lojana (CJ 1948, Stage 35), from Oña, Azuay Province, (D) Gastrotheca elicioi (CJ 4312a, Stage 37), from Loja, Loja Province, (E) Gastrotheca turnerorum (CJ 1957, Stage 36), from Laguna Negra de Jimbura, Parque Nacional Yacuri, Loja Province, and (F) Gastrotheca pseustes 1 (CJ 1949, Stage 37), from Chillacocha, El Oro Province. Scales = 3 mm (A–D, F) (E). Photos by LAC (A, C, E) and MAM (B, D).

FIGURE 6. Oral discs of: (A) Gastrotheca cuencana (CJ 1945, Stage 38), from Cuenca (south control), Azuay Province, (B) Gastrotheca litonedis (CJ 5292, Stage 35), from from Laguna de Busa, San Fernando, Azuay Province, (C) Gastrotheca lojana (CJ 4309, Stage 37), from El Tablón, Loja Province, (D) Gastrotheca elicioi (CJ 4311, Stage 36), from Barrio Puntzará Grande, Loja, Loja Province, (E) Gastrotheca turnerorum (CJ 1959, Stage 39), from Laguna Negra de Jimbura, Parque Nacional Yacuri, Loja Province, and (F) Gastrotheca pseustes (CJ 1949, Stage 37), from Chillacocha, El Oro Province. Not to scale. Photos by LAC.

FIGURE 10. Live adults and brooding females of (A) holotype of Gastrotheca litonedis (KU 202690, SVL = 62.4 mm), of (B– C) G. litonedis (D–G) G. pseustes, G is the holotype (KU 203443, SVL = 55.2 mm) from 7.1 km N San Lucas, 2940 m, (H–I) G. elicioi, (J) G. turnerorum, (K) G. cuencana, (L) G. lojana, (M) female G. psycrophila (KU 164233, SVL = 63.5 mm) from 15 km E of Loja, 2850 m, and (N–O) G. yacuri, N is the holotype (CJ 5822, SVL = 57.4 mm). Not to scale. Photos A, G, M by WED; B–F, H–L by LAC, and N–O by PS.

FIGURE 11. (A) Habitat of Gastrotheca elicioi, G. lojana, G. pseustes, G. psychrophila, and G. turnerorum at the Abra de Zamora, Loja Province, (B) habitat at the type locality of G. cuencana in Cuenca, Azuay Province, (C) habitat of G. turnerorum and G. yacuri at Lagunas Negras, Parque Nacional Yacuri, Loja Province, (D) habitat of G. litonedis, G. lojana, and G. pseustes at Laguna de Busa, Azuay Province, (E) habitat of Gastrotheca lojana at El Tablón, Loja Province, (F) habitat of G. pseustes and (G–H) habitats of G. elicioi at Loja and 15 Km N of Loja, Loja Province. Photos A–B, E, G, H by LAC, C by PS, D by MMM, and F by Jan Verkade.

FIGURE 18. Live holotype of Gastrotheca turnerorum (CJ 393, female, SVL = 54.0): A) dorsal, ventral and lateral views, (B) ventral view of left hand, enlarged 1.9X of A, and (C) ventral view of left foot, enlarged 2.1X of A. Photos by LAC.

FIGURE 19. Live adults of Gastrotheca turnerorum showing variation in dorsaleral lateral, dorsal, ventral, groin, thighs and eye color pattern: (A) CJ 1386, female, SVL = 58.2 mm, and (B) CJ 7823, male, SVL = 46.7 mm. Not to scale. Photos by LAC.

FIGURE 20. Ontogenetic changes in live Gastrotheca turnerorum (CJ 1958), from Laguna Negra de Jimbura, Loja Province, Ecuador. Stages of Gosner: (A) Stage 36, (B) Stage 42, (C) Stage 46 (CJ 1959), and (D) adult. Scale = 10 mm. Photos by LAC.