SUNDATHELPHUSA PROSPERIDAD, SP. N. (DECAPODA: BRACHYURA: GECARCINUCIDAE), A NEW CAVE-OBLIGATE FRESHWATER CRAB FROM MINDANAO ISLAND, THE PHILIPPINES, WITH NOTES ON THE CONSERVATION STATUS OF PHILIPPINE CAVE SPECIES
Daniel Edison M. Husana
Abstract
A new species of cave-obligate freshwater crab of the genus Sundathelphusa Bott, 1969 (Gecarcinucidae) from Agusan del Sur, Philippines is described. The new species is morphologically close to S. hades Takeda and Ng, 2001 but
distinctly differs in the shape of carapace and gonopods. Although the new species is found close to the type locality of
S. hades, the morphological features are distinct and their habitats are separated by an extension of the Philippine faultline and Oligocene-Miocene volcanic deposits. Six Sundathelphusa species having true troglobiomorphic characters
are now recorded from caves in the Philippine archipelago.
INTRODUCTION
A significant number of cavernicolous crab species have been recorded from the Philippines. Eight species of freshwater crabs with various degrees of cave adaptations, all belonging to the genus Sundathelphusa Bott, 1969 of the family Gecarcinucidae Rathbun, 1904, have been described from different caves in the Philippine archipelago. Two of these species were described from Bantakay Cave in the northern island of Luzon, i.e. S. holthuisi Ng, 2010 and S. danae Husana, Yamamuro and Ng, 2014, while S. niwangtiil Husana, Kase and Mendoza, 2015, was described from Mabinay Cave in Negros Island. These three species exhibit partial cave adaptations, i.e. elongated slender ambulatory legs in proportion to their body size. Five species exhibit more advanced troglomorphism, with reduced eyes, elongated legs and loss of pigment. These are S. cavernicola Takeda, 1983 and S. sottoae Ng and Sket, 1996 from Bohol Island; S. hades Takeda and Ng, 2001 from Mindanao Island; S. waray Husana, Naruse and Kase, 2009 and S. lobo
Husana, Naruse and Kase, 2009, from Samar Island.
The new species, Sundathelphusa prosperidad, described here is the ninth species in the genus and also exhibits advanced troglomorphism. It is the second cave-obligate crab recorded from the island of Mindanao. Although other species of Sundathelphusa such as S. philippina (von Martens, 1868), S. boex Ng and Sket, 1996, S. vedeniki Ng and Sket, 1996, S. urichi Ng and Sket, 1996, S. vienae Husana, Yamamuro and Ng, 2014, and S. quirino Husana and Ng, 2019 were recorded from caves in various islands of the Philippines, these species do not exhibit any troglomorphic features. However, S. vedeniki and S. urichi have slightly reduced eyes and shortened eyestalks with noticeable reduction in the body pigmentation in the latter species (Ng and Sket, 1996). Sundathelphusa spelaeophila Stasolla, Abbarchi and Innocenti, 2015, was described from a cave but has no cave-adapted characters and is a junior synonym of S. philippina sensu stricto (Husana and Ng, 2019). All these species are just surface organisms
that regularly enter and stay inside, near the entrance of the cave, for shelter during the day. It is important to note that Sundathelphusa species in the Philippines evolved rapidly as Klaus et al. (2013) demonstrated on the character change following the transition from surface to subterranean life of the five species of this freshwater crab in Bohol Island based on molecular genetic analyses.
Other species of cave crabs from the Philippines have been described and recorded from anchialine caves in various islands of the archipelago. These include species of Varunidae family, i.e. Orcovita tabiacoud Stasolla and Innocenti, 2014, from Pukaway Cave, Coron Island; O. holthuisi Ng and Ng, 2009, from Pukaway Cave, Coron Island; O. angulata Ng, Guinot and Iliffe, 1996 from Pukaway Cave, Coron Island; O. fictilia Ng, Guinot and Iliffe, 1996, Hinagdanan Cave, Panglao Island; Hymenosomatidae family, i.e. Samarplax principe Husana, Tan and Kase, 2011, Principe Cave, Guiuan Island; Sesarmidae family, i.e. Karstarma philippinarum Husana, Naruse and Kase, 2010, Bat Cave, Boracay Island and Tagbaobo Cave, Samal Island; K. boholano Ng, 2002, Tawala Cave, Panglao Island; K. sulu Ng, 2002, St. Paul N. P. Cave, Palawan Island; Gecarcinidae, i.e. Discoplax gracilipes Ng and Guinot, 2001, Virata Cave, Panglao Island, but my extensive field research shows that this latter species is widespread in many caves in karstic
islands in the Philippines. Of these species, only S. principe has the complete troglomorphic features, while others have just elongated legs and/or slight eye reduction as the only cave adaptations.
MATERIALS AND METHODS
Materials were collected using opportunistic sampling methods from a cave on Mindanao Island. A minimal number of samples were hand-picked to avoid high impact that might cause population decline. They were treated with 10% formalin for a week after anesthetizing them in the freezer for about an hour. Specimens were transferred to 70% ethanol after rinsing in fresh flowing water for a few hours. Photographs of live individuals were taken in the field. Photographs of important parts for the description of the specimen were taken from the preserved holotype at the lab using a Canon 70D camera. Figures were made using a Nikon camera lucida. Measurements provided are the maximum carapace width (CW) by carapace length (CL). The terminology follows that by Ng and Sket (1996) with modifications as recommended by Davie et al. (2015). Specimens were deposited at the National Museum of the Philippines, Manila (NMCR) and Zoological Reference Collection (ZRC) Lee Kong Chian Natural History Museum, National University of Singapore. The abbreviations G1 and G2 are used for male first and
second gonopods, respectively.
SYSTEMATICS
Family Gecarcinucidae Rathbun, 1904
Genus Sundathelphusa Bott, 1969
Sundathelphusa prosperidad, new species
Figs. 1–4
Material examined. – Holotype: Male (30.68 × 22.3 mm), NMCR 50776, Ognop Cave, Prosperidad, Agusan del Sur, Philippines, 345mASL. D.E. Husana and A. Pasilan, 14 May 2014. Paratypes: female (28.04 21.38 mm), NMCR 50777, same data as holotype; male (20.58 16.67 mm), female (25.77 20.19 mm), NMCR 50778, Lorenzo Cave, Prosperidad, Agusan del Sur, Philippines. A. Pasilan, January 2014; Male (25.74 19.33 mm), Females (26.16 19.91 mm; 22.69 × 18.02 mm) NMCR 57081, Ognop Cave, Prosperidad, Agusan del Sur, Philippines, 345mASL. D.E. Husana and A. Pasilan, 14 May 2014; male (25.33 20.2 mm), female (28.33 22.62 mm), NMCR 50779, Ognop cave, Prosperidad, Agusan del Sur, Philippines, 345mASL. D.E. Husana and A. Pasilan, 1 May 2012; male (25.29 19.79 mm), ZRC 2019.0876, Ognop cave, Prosperidad, Agusan del Sur, Philippines, 345mASL. D.E. Husana and A. Pasilan, 1 May 2012; female (24.68 19.61 mm), ZRC 2019.0877, males (25.92 × 21.1 mm; 24.4 20.62 mm; 26.54 20.89 mm), NMCR 50780, Ognop cave, Prosperidad, Agusan del Sur, Philippines, 345mASL. A. Pasilan, 20 Nov. 2011.
Comparative materials. – Sundathelphusa cavernicola Takeda 1983: holotype female (25.7 21.0 mm), NSMT-Cr 8937, Quinapon-an Cave, Antequera, Bohol, Philippines, 9º49’38”N, 123º54’10”E, coll. S. I. Ueno, 4 March 1983; 1 male (18 15.4 mm), 1 female (29.2 24 mm), NSMT-Cr 14130, Bongkawi Cave, Antequera, Villa Aurora, Bohol, Philippines, coll. P. K. L. Ng, 16 December 2000; 1 male (26.5 21.6 mm), 2 females (23.1 18.1, 26.5 21.8 mm), ZRC 2000.2079, Bongkawi Cave, Antequera, Villa Aurora, Bohol, Philippines, coll. B. Sket, 23 February 1999; 1 female (22.2 17.8 mm), ZRC 2001.0335, Bongkawi Cave, Antequera, Villa Aurora, Bohol, Philippines, coll. P. K. L. Ng, December 2000; 3 males (13.0 15.10.8 24.1 mm), Canantong Uno cave, Quinapon-an, Antequera, Villa Aurora, Bohol, Philippines, coll. B. Sket, 25 February 1999. Sundathelphusa sottoae Ng and Sket, 1996: 1 female (26.2 21.1 mm), ZRC 1996.1553, paratype, Bonugan, Batuan, Bohol, Philippines, coll. B. Sket, February 1995; 1 (17.5 14.4 mm), ZRC 1996.1548, open well, Batuan, Bohol, Philippines, coll. B. Sket, February 1995; 1 male (18.0 14.9 mm),
ZRC 2001.0343, Bongkawi Cave, Antequerra, Villa Aurora, Bohol, Philippines, coll. P. K. L. Ng, 16 December 2000. Sundathelphusa hades Takeda and Ng, 2001: holotype male (19.7 16.4 mm) NSMT-Cr 14274, Latay Cave, Agusan del Sur, Mindanao, Philippines 8º23’N, 126º05’E, Cave Research Group of Meiji University, 15 Nov. 1981; paratype female (24.9 20.8 mm) ZRC- 2001.1000, Sta. Rita Thinking Cave, Surigao del Sur, Mindanao, Cave Research Group of Meiji University, 27 Nov. 1998. Sundathelphusa waray Husana, Naruse and Kase 2009: holotype male (33.4 25.8 mm), NMCR 27059, Langun Cave, Calbiga, Western Samar, Philippines, 11º39.022’N, 125º02.991’E, coll. D. E. Husana, 28 October 2006. Sundathelphusa lobo Husana, Naruse and Kase 2009: holotype male (31.5 24.3 mm), NMCR
27061, Lobo Cave, Jiabong, Western Samar, Philippines 11º46.786’N, 124º55.732’E, coll. D. E. Husana, 1 August 2006.
Description. – Carapace quadrate to trapezoidal in shape, widest breadth at anterior quarter, dorsal surface convex longitudinally (Figs. 1A, 1M). Frontal region sloping antero-ventrally; branchial regions moderately inflated, with oblique rows of granules of various shapes and lengths; cervical grooves deep; H-shaped median groove deep; epigastric and postorbital with cristae, not confluent; epigastric cristae separated from each other by deep cleft. Frontal margin broadly protruded, two lobes clearly separated with deep broad median concavity; external orbital tooth low, outer margin slightly longer than inner margin, margins granulated; epibranchial tooth small, low, separated from external orbital
tooth by deep notch, inner margin extended dorsally, lined with large granules; anterolateral margin gently convex, lined with large granules, not clearly demarcated from posterolateral margin; posterolateral margin gently concave, converging gradually towards posterior margin of carapace (Figs. 1A, 1B, 1C, 1D, 1M). Frontal medial triangle complete; dorsal and lateral margins distinct, granulose, not fused; dorsal margin concave, lateral margins protruded distally over lateral ends of dorsal margin; orbit well developed; supraorbital margin granulated, sinuous; infraorbital margin beaded with distinct granules; outer edge reaching and fused with anterolateral margin; suborbital and subbranchial regions covered with scattered oblique long and short striae as well as small granules; pterygostomial region smooth with oblique ridges on upper outer region (Figs. 1C, 1D). Epistome divided into three lobes; median lobe large, circular, shallow notch present ventrally; lateral lobes wider and less protruded, sinuous, placed more anteriorly than median lobe (Figs. 1C, 1D).
Eyes reduced, tapering, cornea with traces of pigment, occupy two-thirds of orbit (Figs. 1C, 1D). Basal antennular segment large, subquadrate, flagellum long; antenna with long flagellum, distal end reaching beyond tip of eye when stretched laterally. Ischium of third maxilliped rectangular, bearing distinct oblique submedian sulcus; merus quadrate with shallow median depression; tip of exopod reaching to midpoint of outer margin of merus, with long flagellum (Fig. 1E).
Chelipeds noticeably elongated, subequal, stronger in males; all margins of merus serrated, ventral outer and inner margins more distinct, dorsal margin without distinct subdistal tooth, carpus armed with strong distal sharply-pointed inner angle, flattened dorso-ventrally, laterally fringed with proximal spines; palm minutely granulated on ventral surface, longer than finger; finger robust, cutting edges armed with many sharp teeth of various sizes (Figs. 1M, 1N, 1O). Ambulatory legs long, slender, third leg longest, merus of third leg 0.89–0.95 times CL (n 2); dorsal margins of meri indistinctly serrated, with subdistal tooth or spine, ventral margins serrated on first leg, second to fourth smooth; carpi short, with longitudinal submedian ridge on the dorsal surface except fourth leg, widened distally, dorsal margins
indistinctly serrated; propodi armed with rows of spines on margins, longer on ventral than dorsal margins; dactyliarmed with rows of spines on both margins, spines at ventral margins longer than on dorsal margins (Figs. 1K, 1L, 1M). Male pleonal cavity reaching to level of proximal quarter of coxae of male chelipeds. Male pleon narrow, T-shaped; first somite very short, proximal and distal margins sinuous; second somite transversely subrectangular; third to fifth somites narrows abruptly; lateral margins of third somite convex, lateral margins of fourth somite straight, fifth somite strongly concave; sixth somite rectangular, longer than broad, lateral margins concave; telson subtriangular, longer than broad, lateral margins slightly concave, rounded distally (Figs. 1F, 2A, 2H)
G1 relatively slender; subterminal segment curved outward by distal half, outer margin distinctly concave; terminal segment, bended outward by almost 40-45º, straight, cylindrical, slightly setose, tapering towards distal end (Figs. G1, 1H, 2B, 2C, 2D, 2E, 2I, 2J, 2K, 2L). G2 straight, longer than G1, flagellum short (Figs. 1L, 1J, 2F, 2G, 2M).
Notes on the paratypes. All the paratypes agree well with almost all the major non-sexual characters of the holotype except for varied degree of pigmentation in the eyes (Figs. 1C, 1D, 3A, 3B, 4A). This new species exhibits sexual dimorphism. Oblique granules of striae in the branchial region of the carapace are stronger in males than females. The female possesses large semi-circular vulvae covered by the abdomen at the submedian level of fifth somite, abdomen is rounded with triangular telson (Figs. 3C, 3D). Right and left chelipeds (Fig. 3E) of the females are sub-equal in size but the larger one appeared weaker than that of the males. Granules on the ventral surface of the palm of the cheliped are more prominent in males, with the surface almost smooth in females.
Coloration. Pigmentless, dorsal surface white to pale yellow, ventral surface white (Fig. 4).
Etymology. Named after the Prosperidad town, the species type locality, also a Spanish/Filipino word that means prosperity or success, alluding to the species’ successful colonization of the subterranean ecosystem. Used as a noun in apposition.
Habitat and Distribution. Sundathelphusa prosperidad, new species, is known only from Ognop Cave, the type locality of the new species, and Lorenzo Cave, both located within the karst system of Prosperidad, Agusan del Sur. The caves are part of an Oligocene-Miocene limestone formation (MGB, 2010) in Agusan del Sur, Mindanao Island, the Philippines
This new species occurs in small numbers near the vertical entrance of Ognop Cave (Fig. 4). Two samples of S. prosperidad, new species, were collected from Lorenzo Cave (NMCR 50778, male 20.58 16.67mm; female 25.77 20.19mm). This distribution clearly suggests that Lorenzo Cave and Ognop Cave are interconnected and the possibility that other colonies could be present in other unexplored areas of the cave system.
Ognop Cave is a long cave system with fragments of sharp, brittle rock boulders along its shallow subterranean river and deep pools. Lorenzo Cave is just a few meters long with a subterranean stream that flows towards its entrance. The water originates from a sump that makes it impassable and cannot be explored further without the use of diving equipment. This cave is located southeast of the Ognop Cave entrance.
Co-inhabitants of the groundwater of Ognop Cave are species of cave goby Caecogobius personatus Larson and Husana, 2017, unidentified cyprinid fish (manuscript in preparation), and atyid shrimps. A colony of bats, a large population of crickets and other invertebrates are also present inside the cave.
The spring that comes out from the rubble of the collapsed portion of the entrance of Ognop Cave is the headwater of one of the major tributaries of the Bega River traversing Bega Falls
Remarks. Sundathelphusa prosperidad, new species, closely resembles Sundathelphusa hades Takeda and Ng, 2001. However, S. prosperidad possesses the following characters that differentiate it from S. hades: 1) quadrate to trape Journal of Cave and Karst Studies, June 2020 • 217 Husana zoidal carapace with proportionately wider breadth at about its one-third level (vs. squarish and narrower breadth in S.
hades) (Figs. 1A, 1M, 3E vs. Takeda and Ng 2001, figs. 1a, 1b, 1e); 2) presence of a deep notch between the external orbital tooth and epibranchial tooth of the antero-lateral margin (vs. small or shallow in S. hades) (Figs. 1A, 1B, 1C, 1D, 1M, 3A, 3B, 3E vs. Takeda and Ng 2001, figs. 1a, 1b, 1c, 1e, 2a); 3) presence of a granulated crest formed as dorsal extension of the inner margin of the epibranchial tooth (vs. absent in S. hades) (Figs. 1A, 1B, 1C, 1D, 1M, 3A, 3B, 3E vs. Takeda and Ng 2001, figs. 1a, 1b, 1c, 1e, 2a); and 4) the distal part of the subterminal segment of the G1 is strongly curved outwards (vs. relatively straighter in S. hades) (Figs. 1G, 1H, 2B, 2C, 2D, 2E, 2I, 2J, 2K, 2L vs. Takeda and Ng 2001, figs. 3c,3d).
Both S. prosperidad and S. hades inhabit caves hence possessing strongly reduced eyes, with a small trace of pigmentation at the tip of the cornea (see Figs. 1C, 1D, 3A, 3B; Takeda and Ng 2001, figs. 1c, 2a, 2b). Such a degree of troglomorphism has also been observed in other freshwater crabs described from caves in the Philippines such as S. cavernicola Ng and Sket, 1996, S. sottoae Ng and Sket, 1996, S. lobo Husana, Naruse and Kase 2009, and S. waray Husana, Naruse and Kase 2009.
Sundathelphusa prosperidad, new species, and S. hades are both located in Agusan del Sur in the eastern part of Mindanao Island, and their type localities are close to each other. But unlike the overlapping habitat range of S. sottoae and S. cavernicola in Bohol Island, the habitats of these two cave species from Mindanao Island are separated by the extension of the Philippine fault-line and Oligocene-Miocene volcanic deposits (MGB, 2010). The type locality of S. prosperidad, new species, is a cave in an Oligocene-Miocene limestone formation, north of the type locality of S. hades, a cave in a younger Pliocene Pliestocene limestone formation (MGB, 2010). Attempts to obtain fresh samples of S. hades from the type locality were in vain due to the security situation in the area.
About 98 percent of freshwater crabs in the Philippines are endemic to the archipelago and most of them are data deficient (Cumberlidge et al, 2009). Although there is a possibility that colonies of S. prosperidad are present in some unexplored areas of Ognop Cave, the population estimate of this new species may not go beyond 1,000 individuals, it has a small geographic range, and with a very small and restricted area of occupancy.
Under IUCN Red List, this new species can be categorized between endangered to critically endangered species under Criterion B1 (< 100 km2 extent of occurrence), Criterion B2 (< 10 km2 area of occupancy), Criterion C (< 2,500 mature individuals), and Criterion D (< x 250 mature individuals per area inside the cave system).
Cave-obligate species in the Philippines are strictly endemic to the cave system they inhabit and cannot be found anywhere else. Similar to the Sundathelphusa prosperidad, new species, other cave crabs such as S. cavernicola Takeda, 1983, S. sottoae Ng and Sket, 1996, S. hades Takeda and Ng, 2001, S. waray Husana, Naruse and Kase, 2009, S. lobo Husana, Naruse and Kase, 2009, and Samarplax principe Husana, Tan and Kase, 2011; cave fishes such as Caecogobius cryptophthalmus Berti and Ercolini, 1991, and C. personatus Larson and Husana, 2019, and other cave-obligate species can fall into the same category. The limited distributional range, the restricted confinement in the cave habitat and small population size of cave-obligate species made them extremely vulnerable to human disturbance. Forest logging, slash and burn farming, and land conversion are common practice that will seriously threaten the cave and its inhabitants and should be strictly prohibited in the surrounding areas above the cave system. The increasing popularity of tourism in the country also poses a serious threat in this stenotopic species. Hence, it is strongly recommended that Ognop Cave and all other caves with cave-obligate species, as well as its surface vegetation, should be strictly protected to preserve the natural habitat of these species and other unique cave organisms.
Acknowledgements
I express my heartfelt gratitude to my friends in Prosperidad for their unwavering support for my field research in Agusan del Sur. There are no exact words to utter how thankful I am for their hospitality, generosity, and field assistance during my many research trips, as well as for their enthusiasm in protecting and preserving the local natural resources: the Honorable Mayor Albin Magdamit and his staff, especially Noradel Martinez and Marigyn Kamita who facilitated the activities every time I visited the site; the PMC outdoor group, especially Arnel Pasilan who originally discovered the new species, Almar Lambaco, Joelito Dumdum, Winsome Berdida and Joseph Mortiz for their assistance in my many
biological expeditions in the region; and the barangay chairman, Benecio Manliguez, for providing security and a local guide during field research trips. My many thanks to Prof. P.K.L. Ng for his guidance in crab taxonomy and hosting me during my research fellowships at NUS. His constructive comments and suggestions were so valuable for the improvement of this manuscript. I also appreciate the assistance of M. Manuel-Santos of the Philippine National Museum and J.C.E. Mendoza of the Lee Kong Chian Museum of Natural History for facilitating the storage of the specimens. This work was funded by the UP System Enhanced Creative Work and Research Grant (ECWRG 2017-2-008). This research is permitted by the Department of Environment and Natural Resources (Wildlife Gratuitous Permit No. R13- 2014-004).
References
Berti, R. and Ercolini, A., 1991, Caecogobius cryptophthalmus n. gen. n. sp. (Gobiidae Gobiinae), the first stygobic fish from Philippines: Tropical Zoology, v. 4, no. 1, p. 129–138. DOI: 10.1080/03946975.1991.10539482
Bott, R., 1969, Flußkrabben aus Asien und ihre Klassifikation (Crustacea, Decapoda): Senckenbergiana Biologica, v. 50, p. 359–366.
Cumberlidge, N., Ng, P.K.L., Yeo, D.C.J., Magalhães, C., Campos, M.R., Alvarez, F., Naruse, T., Daniels, S.R., Esser, L.J., Attipoe, F.Y.K., Clotilde-Ba, F.-L., Darwall, W., McIvor, A., Baillie, J.E.M., Collen, B., and Ram, M., 2009, Freshwater crabs and the biodiversity crisis: importance, threats, status, and conservation challenges: Biological Conservation, v. 142, p. 1665–1673. https://doi.org/10.1016/j.biocon.2009.02.038
Davie, P.J.F., Guinot, D. and Ng, P.K.L., 2015, Phylogeny of Brachyura: in Castro, P., Davie, P.J.F., Guinot, D., Schram, F., and Von Vaupel Klein, C., eds., Treatise on Zoology – Anatomy, Taxonomy, Biology: The Crustacea, complementary to the volumes translated from the French of the Traité de Zoologie, v. 9(C) (I), Decapoda: Brachyura (Part 2), p. 922–979.
Husana, D.E.M., Kase, T., and Mendoza, J.C.E., 2015, Two new species of the freshwater crab genus Sundathelphusa Bott, 1969 (Crustacea:
Brachyura: Gecarcinucidae) from Negros Island, Philippines: Raffles Bulletin of Zoology, v. 63, p. 226–236. http://zoobank.org/urn:lsid:zoobank.org:pub:549829D6-65A9-4D97-B15E-361755F7577B
Husana, D.E.M., Naruse, T., and Kase, T., 2009, Two new cavernicolous species of the genus Sundathelphusa from Western Samar, Philippines
(Decapoda: Brachyura: Parathelphusidae): Journal of Crustacean Biology, v. 29, no. 3, p. 419–427. https://doi.org/10.1651/08-3081.1
Husana, D.E.M., Naruse, T., and Kase, T., 2010, A new species of the genus Karstarma (Crustacea: Decapoda: Brachyura: Sesarmidae) from
Anchialine Caves in the Philippines: Raffles Bulletin of Zoology, v.58, no. 1, p. 65–69.
Husana, D.E.M., and Ng, P.K.L., 2019, On the identity of Sundathelphusa philippina (von Martens, 1868) (Decapoda: Brachyura: Gecarcinucidae) from the Philippines, with descriptions of two new species: Zootaxa, v. 4585, no. 2, p. 315–331. https://doi.org/10.11646/zootaxa.4585.2.5
Husana, D.E.M., Tan, S.H., and Kase, T., 2011, A new genus and species of anchialine Hymeosomatidae (Crustacea: Decapoda: Brachyura) from Samar, Philippines: Zootaxa, v. 3109, p. 49–59. https://doi.org/10.11646/zootaxa.3109.1.3 Husana, D.E.M., Yamamuro, M., and Ng, P.K.L., 2014, Two new species of freshwater crabs of the genus Sundathelphusa Bott, 1969 (Decapoda: Brachyura: Gecarcinucidae) from caves in Luzon, Philippines: Zootaxa, v. 3815, no. 4., p. 565–574. https://doi.org/10.11646/zootaxa.3815.4.6 Klaus, S., Mendoza, J.C.E., Liew, J.H., Plath, M., Meier, R., and Yeo, D.C.J., 2013, Rapid evolution of troglomorphic characters suggests selection rather than neutral mutation as a driver of eye reduction in cave crabs: Biology Letters, v. 9, 20121098. https://doi.org/10.1098/rsbl.2012.1098 Larson, H.K., and Husana, D.E.M., 2019, A new species of the blind goby Caecogobius (Govioidei, Gobiidae, Gobinellinae) from a cave system in Mindanao, Philippines: Ichthyological Research, v. 66, no. 1, p. 97–103. Published online: 6 October 2018. https://doi.org/10.1007/s10228-018-0659-y Martens, E. von, 1868, Ueber einige neue crustacean: Monatsberichte der Königlichen Preussische Akademie der Akademie der Wissenschaften zu Berlin: Sitzung der Physikalisch-mathematische Klasse, 1868:.in Mines and Geosciences Bureau, 2010, Geology of the Philippines, 2nd edition: p. 608–615, Department of Environment and Natural Resources, 532 pages. Ng, N.K., and Ng, P.K.L., 2009, Orcovita holthuisi, a new species of anchialine crab (Brachyura, Varunidae) from Coron Island, Palawan, Philippines: Crustaceana, v. 82, no. 9, p. 1097–1108. https://doi.org/10.1163/156854009X407678 Ng, P.K.L., 2002, New species of cavernicolous crabs of the genus Sesarmoides from the western Pacific, with a key to the genus (Crustacea: Decapoda: Brachyura: Sesarmidae): Raffles Bulletin of Zoology, v. 50, no. 2, p. 419–435. Ng, P.K.L., 2010, On the identity of Para-Bary-Thelphusa grapsoides longipes Balss, 1937, with description of a new species from the Philippines (Brachyura, Gecarcinucidae): in Fransen, C.H.J.M., De Grave S., and Ng, P.K.L., eds., Studies on Malacostraca: Lipke Bijdeley Holthuis Memorial Volume: Crustaceana Monographs, v. 14, p. 561–571. Ng, P.K.L., and Guinot, D., 2001, On the land crabs of the genus Discoplax A. Milne Edwards, 1867 (Crustacea: Decapoda: Brachyura: Gecarcinidae), with description of a new cavernicolous species from the Philippines: Raffles Bulletin of Zoology, v. 49, no. 2, p. 331–338. Ng, P.K.L., and Sket, B., 1996, The freshwater crab fauna (Crustacea: Decapoda: Brachyura) of the Philippines. IV. On the collection of Parathelphusidae from Bohol: Proceeding of the Biological Society of Washington, v. 109, p. 695–706. Ng, P.K.L., Guinot, D., and Iliffe, T.M., 1996, Revision of the anchialine varunine crabs of the genus Orcovita Ng and Tomascik, 1994 (Crustacea: Decapoda: Brachyura: Grapsidae), with descriptions of four new species: Raffles Bulletin of Zoology, v. 44, no. 1, p. 109–134. Rathbun, M.J., 1904, Les crabes d’eau douce (Potamonidae): Nouvelles Archives du Muséum d’Histoire Naturelle, 4e ser., v. 6, p. 225–311, pls. 9–18. Stasolla, G., Abbarchi, A., and Innocenti, G., 2015, Sundathelphusa spelaeophila, a new species of cavernicolous crab from Samar, Philippines (Decapoda: Brachyura: Gecarcinucidae): Raffles Bulletin of Zoology, v. 63, p. 448–453. Stasolla, G. and Innocenti, G., 2014, A new species of cavernicolous crab from Coron Island, Palawan, the Philippines (Decapoda: Brachyura: Varunidae): Raffles Bulletin of Zoology, v. 62, p. 591–599. Takeda, M., 1983, A new cavernicolous crab from Bohol, the Philippines: Bulletin of the National Science Museum, Tokyo, Series A, v. 9, p.169–173. Takeda, M., and Ng, P.K.L., 2001, The freshwater crab fauna (Crustacea, Brachyura) of the Philippines: VI. A new cavernicolous crab from Mindanao: Zoological Science, v. 18, p. 1123–1127. https://doi.org/10.2108/zsj.18.1123
A NEW SPECIES OF THE BLIND GOBY CAECOGOBIUS (GOBIOIDEI,
GOBIIDAE, GOBIONELLINAE) FROM A CAVE SYSTEM ON MINDANAO ISLAND,
THE PHILIPPINES
Helen K. Larson1,2 · Daniel E. M. Husana3
Received: 29 April 2018 / Revised: 23 August 2018 / Accepted: 23 August 2018 / Published online: 6 October 2018
© The Ichthyological Society of Japan 2018
Abstract
A new species of the eyeless goby genus Caecogobius is described from a cave system on Mindanao Island, the Philippines. Caecogobius personatus sp. nov. is the second cave-obligate fsh ever discovered from the Philippine archipelago. The frst species, Caecogobius cryptophthalmus Berti and Ercolini 1991 was recorded from Samar Island, an adjacent island north of Mindanao. The new species difers from its only congener, C. cryptophthalmus, in having a fnely ridged feshy area over the orbit and feshy fap-like sensory papillae on feshy raised ridges (the sensory papillae in C. cryptophthalmus are all small and
evenly sized, not feshy or fap-like) and having all elements of the second dorsal fn segmented (frst element unsegmented in C. cryptophthalmus). The relationship of these two Caecogobius to each other and to other gobionellines is not known.
Keywords Gobiidae · Caecogobius · New species · Cave systems · Philippines
Introduction
The goby genus Caecogobius Berti and Ercolini 1991 is
the only blind cave-dwelling gobioid known from the Philippines, represented by one known species, Caecogobius
cryptophthalmus Berti and Ercolini 1991 (Larson 2001;
Romero and Paulson 2001). It has been reported only from
This article was registered in the Ofcial Register of Zoological Nomenclature (ZooBank) as 8EA76D50-374B-4838-808C-79473 43C9735. This article was published as an Online First article on the online
publication date shown on this page. The article should be cited by using the doi number.
- Helen K. Larson
helen.larson@magnt.net.au
Daniel E. M. Husana
dehusana@gmail.com
1 Museum and Art Gallery of the Northern Territory, PO Box 4646, Darwin, NT 0801, Australia
2 Museum of Tropical Queensland, 70-102 Flinders Street, Townsville, QLD 4810, Australia
3 Environmental Biology Division, Institute of Biological Sciences, College of Arts and Sciences, University of the Philippines Los Baños, 4031 Los Baños, Laguna, Philippines
the Calbiga Cave system on Samar Island (Berti and Ercolini 1991). The type locality of C. cryptophthalmus is more than 300 kilometers to the north of Mindanao Island and separated by the Surigao Strait. The fsh, which we describe here as a new species, is the second stygobitic goby from the Philippines to be reported so far. This new species was found with the help of a local guide who frst spotted the fsh
inside the cave during the second author’s (D. E. M. Husana) biological cave expedition in Mindanao (Fig. 1).
When the genus Caecogobius was frst described from the Philippines, Berti and Ercolini (1991) recognized its similarity to Glossogobius and Mugilogobius. Larson (2001) accepted it as a good genus and gave characters separating it from the other two genera. Additionally, the characters defning Glossogobius given in Hoese et al. (2015) do not agree with Caecogobius nor the new species. Diferences between C. cryptophthalmus and the new species are given below under Comparisons.
The only other externally eyeless gobiid species known, apart from C. cryptophthalmus, is Glossogobius ankaranensis Bannister 1994 from Madagascar, which difers from Caecogobius in possessing the bilobed tongue characteristic of the genus Glossogobius. The new species does difer from most species of Glossogobius, however, in lacking all sensory pores and canals on the head (vs. sensory pores present
in all species but for one in Glossogobius), in having a blunt
Fig. 1 Photograph of the subterranean pool inside the cave where Caecogobius personatus sp. nov. was collected
tongue with small central notch (vs. tongue always bilobed), having 25–26 vertebrae (vs. usually 27–30) and in having less than fve rows of sensory papillae on the cheek (vs. having fve or more rows of papillae on cheek). However, the complete absence of sensory pores is shared with Glossogobius favipinnis (Aurich 1938), endemic to Lake Towuti in central Sulawesi (Hoese et al. 2015).
The other eyeless gobioids known are Caecieleotris Walsh and Chakrabarty 2016 (one species), Milyeringa
Whitley 1945 (two species), Oxyeleotris Bleeker 1874 (two species) and Typhleotris Petit 1933 (three species). Others, such as Bostrychus microphthalmus Hoese and Kottelat 2005, Luciogobius albus Regan 1940 and Luciogobius pallidus Regan 1940, live in caves but have greatly reduced eyes, i.e., are not completely eyeless.
We have deliberately withheld details of locality due to concerns for the fsh’s safety (fsh smugglers; aquarium trade). The local government, however, has created a program to help manage its natural habitat to protect and preserve the species.
Materials and methods
Measurements were taken using electronic callipers and dissecting microscope. Counts and methods generally follow Hubbs and Lagler (1970), except as indicated below. Transverse scale counts backward (TRB) are taken by counting the number of scale rows from just before the anal fn origin diagonally upward and back toward the second dorsal fn base. Head length is taken to the upper attachment of the
opercular membrane. Interorbital width was determined from the bony frontal margins. As the genus has no external eyes, one additional head measurement was taken, from the snout tip to the upper edge of the preopercular margin (POP). The total segmented caudal ray pattern (e.g., 9/8) is the number of segmented caudal rays on either side of the gap between the two parts of the hypural plate (hypurals 3–4
and 1–2). Pectoral ray counts are based on those from the left side only, as the right fn was removed from all specimens for later genetic analyses (a separate project). Vertebral counts and other osteological information were obtained by X-ray (Fig. 2). Pterygiophore formula follows Birdsong et al. (1988). Type specimens are deposited in the National Museum of the Philippines (PNM), Australian Museum,
Sydney (AMS) and Zoological Reference Collection, Singapore (ZRC). Museum acronyms follow those used in Sabaj (2016). Standard length and head length are abbreviated as SL and HL, respectively.
Caecogobius personatus sp. nov.
Holotype. PNM 15353, ex ZRC 56329, 49 mm SL male, Ugnop Cave system, Mindanao, Philippines, coll. D.E. Husana, 14 May 2012.
Paratypes. ZRC 56329, 1 (49 mm SL), male; PNM 15354, 1 (42), female; AMS I.47860-001, 1 (39), male, same collecting data as holotype; all paratypes with same data as holotype.
Diagnosis. A species of Caecogobius with frst dorsal fn with VI spines; second dorsal fn with 7 soft rays, all elements segmented; anal fn rays I, 6; pectoral fn rays 14–15; pelvic fn rays I, 5; 17 segmented caudal fn rays with 13–16 rays branched; 25–26 weakly ctenoid lateral scales; 10–12 cycloid predorsal scales; feshy rounded to fap-like sensory papillae on the head and body; scale margins on upper part of body narrowly edged with pale brown, body otherwise mostly without pigment; vertebrae 10 + 15–16 (25–26),
pterygiophore formula 3-12210; 2 pre-anal pterygiophores, 2 epurals, may be partly fused; 5/5 to 6/6 procurrent rays. Found in a cave in Mindanao, Philippines
Description. Based on four specimens, 39–49 mm SL. Counts of the holotype (Fig. 3) indicated by asterisk.
First dorsal spines VI; second dorsal rays 7; anal rays I, 6; pectoral rays 14–15; pelvic rays I, 5; segmented caudal rays 17, in 9/8* pattern, with 13–16 (14 in holotype) fn rays branched; lateral scale count 25–26; transverse scales backward 8–10 (9 in holotype); predorsal scale count 10–12. Vertebrae 10 + 15–16 including urostyle (25–26), pterygiophore formula 3-12210; 2 pre-anal pterygiophores, 2 epurals, may be partly fused; 5/5 to 6/6 procurrent rays.
Body moderately robust in males, slender in female, somewhat rounded anteriorly, compressed posteriorly; body depth at anal fn origin 16.0–19.0% of SL. Caudal peduncle slender, length 25.0–27.8% of SL. Caudal peduncle depth 10.0–11.8% of SL. Head depressed anteriorly, head much wider than deep at preopercular margin, head length 32.2–36.0% of SL; head depth at posterior preopercular margin 44.4–52.9% of HL; width at posterior preopercular margin 53.0–67.6% of HL (female with narrowest head).
Fig. 2 X-ray illustration of all four type specimens
Fig. 3 Photograph of holotype of Caecogobius personatus sp. nov. showing (a) dorsal, (b) lateral and (c) ventral view, PNM 15353, 49 mm SL male, Ugnop Cave, Mindanao. Photograph by Heok Hui Tan
Mouth large, terminal and oblique, jaws forming an angle of 30–35° with body axis. Upper jaw length 36.4–44.9% of HL; inner margin of lips smooth to very fnely fmbriate; lower lip fused to chin anteriorly, side of lip free; chin rounded with no mental frenum. Anterior naris in wide-based short tube overhanging edge of upper lip; posterior naris rounded with raised rim that is split to base anteriorly (Fig. 4). Eyes
absent; orbital region with slightly raised thickened skin forming slight fold above cheek. Snout broad, rounded anteriorly in dorsal view; snout with hump in female; length of snout tip to upper edge of the preopercular margin 68.9–75.3% of HL. Gill opening moderate, reaching forward under opercle, ending close behind preopercular rear margin. Tongue large, tip blunt with small central notch. Teeth in both jaws curved, sharp and pointed; in two to three rows in upper jaw and three to four in lower; largest teeth
Fig. 4 Illustration of sensory papilla pattern in holotype of Caecogobius personatus sp. nov., PNM 15353, 49 mm SL, lateral view
Fig. 5 Illustration of sensory papilla pattern in holotype of Caecogobius personatus sp. nov., PNM 15353, 49 mm SL, ventral view
across front of jaws; teeth in female all smaller and evenly sized than in males. Head pores absent. Sensory papillae rounded and feshy, in reduced transverse pattern; papillae may form small pointed lobes or faps; papillae in the few transverse rows short pointed faps joined together basally by skin (Figs. 4, 5). Sensory papillae on lower half of body short feshy faps, in widely spaced irregular vertical rows; two longitudinal rows of papillae on caudal fn.
Body with weakly ctenoid scales, reaching forward onto head to just above or slightly before rear preopercular margin. Side of head naked but for small cycloid scale on anterodorsal part of opercle. Prepelvic region with scattered cycloid scales close to pelvic fn bases. Pectoral fn base naked. Belly with few cycloid scales especially on posterior half; midline usually naked.
First dorsal fn triangular, with third or fourth spine just reaching base of second dorsal fin spine; depressed fin 17.1–20.0% of SL; holotype with tips of third and fourth spines bifurcate. Second dorsal and anal fns short based, rays taller than frst dorsal fn; posteriormost rays slightly longer than anterior rays but not greatly so, posterior rays falling well short of caudal fn base. Second dorsal fn with all elements segmented. Anal fn with spine and segmented rays. Pectoral fn slender, pointed, central rays longest, fn
reaching back to above anus, length 24.3–27.4% of SL; only upper and lowermost rays unbranched. Pelvic fns oval, ffth rays longest, length 18.8–22.1% of SL; fns oval, pointed, fn tips not quite reaching anus; frenum complete, about 20% length of fins. Caudal fin oval, pointed, fin length 26.3–28.5% of SL.
Fresh coloration. From photograph of two fresh dead specimens by D. E. M. Husana (Fig. 6). Head and body white, with scale margins on nape and upper half of body narrowly edged with brown, predorsal scales with darkest margins especially anteriorly; opercle with faint pale brown fine speckling; interorbital finely speckled with brown, with some scattered brown speckling extending onto dorsal surface of snout. First dorsal fn without visible pigment in photo. Second dorsal fn with brown pigmentation along bases of rays and extending about halfway up each ray. Pectoral fn with brown pigment along base of each ray, extending about a quarter length of each ray. No pigment visible from photo on anal, pelvic or caudal fns; fn rays translucent and membranes transparent.
Coloration in alcohol. Head and body whitish, with scale margins on nape and upper half of body narrowly edged with pale brown, predorsal scales with darkest margins; opercle with indistinct pale brown fne speckling and vermiculation. First dorsal fn with variable amount of pale brown pigment
Fig. 6 Freshly dead type specimens of Caecogobius personatus sp. nov. showing (a) dorsal and (b) lateral views (pinkish cast to edges is a result of fsh being photographed on red background)
on outer membranes, most pronounced in 42 mm SL male. Second dorsal fn with indistinct pale brown speckling along bases of rays at least; may extend halfway up each ray. No pigment on anal, pectoral, pelvic or caudal fns; fn membranes transparent.
Distribution. Known only from a karstic cave system in Mindanao Island, the Philippines.
Ecology. The cave where this new species was discovered is in a forested area close to a tribal village. Access to the cave is through the surface stream that springs out from the rubble of its collapsed entrance. The temperature of the outfowing water from the cave is much colder than the surface water, suggesting a long confnement as groundwater. Together with this new goby species is a large population
of eyed cyprinid species. Stygobitic crabs and shrimps were also observed in the cave stream. Cave crickets were abundant in the cave as well as other small terrestrial invertebrates and bats.
Only about six individuals of the goby were observed at the time of collection, of which four were collected. It is believed however, that the population stock is present upstream or in the deeper part of the cave, because this species had not been observed during several cave expeditions before and after the discovery of the goby. It is possible that the larger co-inhabitant cyprinid fsh preys upon the smaller
goby.
Comparisons. The features on this species’ head difer from those of Caecogobius cryptophthalmus, which does not possess the feshy fnely ridged area over the orbit, the feshy fap-like papillae or the few short transverse papilla rows of C. personatus. The sensory papillae in C. cryptophthalmus are all small and evenly sized, not feshy or fap-like and there do not appear to be any transverse rows of papillae,
based on the senior author’s (H. K. Larson) drawing of a paratype (Larson 2001: fg. 45). Figure 5 in Berti and Ercolini (1991) is a “reconstruction” of the head of the type specimens and does appear to contain several transverse rows, but the diagrammatic nature of the reconstruction gives
some uncertainty (and difers from the paratype observed by H. K. Larson). The eyes in C. cryptophthalmus appear to be present but greatly reduced and buried in the fesh of the head (i.e., not visible externally), unlike the eyes of C. personatus, which cannot be seen at all. In addition, C. personatus has all segmented rays in the second dorsal fn, unlike C. cryptophthalmus; but similar to the pattern found in Milyeringa veritas (Larson et al. 2013). There are other minor morphological and meristic diferences (in pectoral
ray counts, lateral scale counts, body proportions). It is possible that each species actually represents a diferent genus, but without additional specimens (four each known for C. cryptophthalmus and C. personatus), it is not possible to pursue further osteological, morphological and genetic analyses until these are found. Work remains to be done on the possible relationships of these two Caecogobius to each other and to other gobionellines.
Etymology. The Latin personatus (masked) refers to the feshy area covering the orbits, masking where the eyes should be.
Remarks. There are very few eyeless cave-dwelling gobioids worldwide already described, with most of these stygobitic species being eleotrids (e.g., Walsh and Chakrabarty 2016; Chakrabarty et al. 2012; Chakrabarty 2010). In the Philippines, the new species described here is the second so far. Considering the geologic history and the archipelagic setting of the region, there is a possibility that more cavefsh
species could be discovered in the future. Many cave aquatic invertebrate species have been recorded in the past few years, from D. E. M. Husana’s biological cave expeditions. To date, many karst areas are still unexplored and remain a challenge because of the difculty of access. The growing interest in tourism activities will provide new information with regard to the location of caves. However, this will also
pose a problem to the safety of the cave organisms.
Comparative material. Caecogobius cryptophthalmus paratype, ZSM 27189, 58.5 mm SL female, Calbiga Cave system, Samar, Philippines, coll. Samar 87 Expedition, Federazione Speleologica Veneta, January–February 1987 (Table 1).
Table 1 Measurements of the four specimens of Caecogobius personatus sp. nov.
Acknowledgments. We ofer our many thanks to Heok Hui Tan of ZRC, who facilitated the loan of the specimens and provided beautiful X-rays of them. Thanks also are due to Gavin Dally of MAGNT, who made sure the fsh arrived safely. We also appreciate the assistance of Marivene Manuel-Santos of the Philippine National Museum for facilitating the storage of the specimens. D. E. M. Husana would like to express his great appreciation to his friends in Mindanao. There are no exact words to describe how thankful he is for their hospitality, generosity and feld assistance during his many research trips to the region: the Honorable Mayor Albin Magdamit and his staf, especially Noradel Martinez and Marigyn Kamita who showed their eagerness to protect the natural environment in their town; the PMC outdoor group, especially Arnel Pasilan, Almar Lambaco, Joelito Dumdum, Winsome Berdida and Joseph Mortiz and all the other members for their assistance in D. E. M. Husana’s many biological expeditions in the region; and the barangay chairman, Benecio Manliguez, for providing security and a local guide. This research is permitted by the Department of Environment and Natural Resources (Wildlife Gratuitous Permit No. R13-2014-004).
References
Aurich HJ (1938) Mitteilung XXVIII der Wallacea-Expedition Woltereck. Die Gobiiden. (Ordnung: Gobioidea). Int Revue ges
Hydrobiol Hydrogr 38:125–183
Banister K (1994) Glossogobius ankaranensis, a new species of blind cave goby from Madagascar (Pisces: Gobioidei: Gobiidae). Aqua 1:25–28
Berti R, Ercolini A (1991) Caecogobius cryptophthalmus n. gen. n. sp. (Gobiidae, Gobiinae), the frst stygobitic fsh from Philippines. Trop Zool 4:129–138
Birdsong RS, Murdy EO, Pezold FL (1988) A study of the vertebral column and median fn osteology in gobioid fshes with comments on gobioid relationships. Bull Mar Sci 42:174–214
Bleeker P (1874) Esquisse d’un système naturel des Gobioïdes. Arch Néerl Sci Exactes Nat 9:289–331
Chakrabarty P (2010) Status and phylogeny of Milyeringidae
(Teleostei: Gobiiformes), with the description of a new blind cave-fsh from Australia, Milyeringa brooksi, n. sp. Zootaxa 2557:19–28
Chakrabarty P, Davis MP, Sparks JS (2012) The frst record of a trans-oceanic sister-group relationship between obligate vertebrate troglobites. PLoS One 7 (8):e44083
Hoese DF, Kottelat M (2005) Bostrychus microphthalmus, a new microphthalmic cavefsh from Sulawesi (Teleostei: Gobiidae).
Ichthyol Explor Freshw 16:183–191
Hoese DF, Hadiaty RK, Herder F (2015) Review of the dwarf Glossogobius lacking head pores from the Malili lakes, Sulawesi, with a discussion of the defnition of the genus. Rafes Bull
Zool 63:14–26
Hubbs CL, Lagler KF (1970) Fishes of the Great Lakes Region.
Third edn. University of Michigan Press, Ann Arbor Larson HK (2001) A revision of the gobiid fsh genus Mugilogobius
(Teleostei: Gobioidei), and its systematic placement. Rec West Aust Mus Suppl (62):i–iv + 1–233
Larson HK, Foster R, Humphreys WF, Stevens MI (2013) A new species of the blind cave gudgeon Milyeringa (Pisces: Gobioidei,
Eleotridae) from Barrow Island, Western Australia, with a redescription M. veritas Whitley. Zootaxa 3616:135–150
Petit G (1933) Un poisson cavernicole aveugle des eaux douces de Madagascar: Typhleotris madagascariensis gen. et sp. nov. C R Seances Acad Sci 197:347–348
Regan CT (1940) The fshes of the gobiid genus Luciogobius Gill. Ann Mag Nat Hist Ser 11 5:462–465
Romero A, Paulson KM (2001) It’s a wonderful hypogean life: a guide to the troglomorphic fshes of the world. Environ Biol Fishes 62:13–41
New species of the blind goby Caecogobius
Sabaj MH (2016) Standard symbolic codes for institutional resource collections in herpetology and ichthyology: an Online Reference. Electronic version version 6.5 (16 Aug 2016). American Society
of Ichthyologists and Herpetologists, Washington, DC. http://www.asih.org/. Accessed 30 August 2017
Walsh SJ, Chakrabarty P (2016) A new genus and species of blind sleeper (Teleostei: Eleotridae) from Oaxaca, Mexico: frst obligate cave gobiiform in the Western Hemisphere. Copeia 104:506–517 Whitley GP (1945) New sharks and fshes from Western Australia. Pt 2 Aust Zool 11:1–42
BARBODES PYRPHOLEOS, NEW SPECIES, THE FIRST CAVE-DWELLING CYPRINID FISH IN THE PHILIPPINES, WITH REDESCRIPTION OF B. MONTANOI (TELEOSTEI: CYPRINIDAE)
Tan Heok Hui1* & Daniel Edison M. Husana2
Abstract. Barbodes pyrpholeos, new species, is the first cave-dwelling cyprinid fish reported from the Philippines. It is described from karst systems in Mindanao. It is distinguished from other congeners by having a poorly pigmented body with reddish fins in combination with a smooth dorsal-fin spine without serrations, and several additional morphological characters. It differs from the Indonesian troglobitic congener Barbodes microps by the presence of eyes, and a narrower body amongst other characters. Barbodes montanoi, a putative close relative of the new species, is redescribed based on recently collected material.
Key words. troglobite, Cyprinidae, biodiversity, new species, Southeast Asia
INTRODUCTION
The freshwater fishes of Mindanao are not well documented, except for the endemic species flock of cyprinids in Lake Lanao (Herre, 1933). This flock comprises five genera and 18 species (Herre, 1924; Myers, 1960), for which there is no recent update, and most are apparently in danger of extinction or have become extinct (Ismail et al., 2014). Herre (1953) provided a checklist of fishes from the Philippines
and listed more than 2,000 species, but this list included both marine and freshwater taxa. At present, around 290 species of fishes are recorded from the inland waters of the Philippines by some sources (e.g., see Fishbase, 2019), but such lists are outdated and in need of revision.
Recently, cyprinids normally placed collectively under Systomus have been split up and revalidated with older available names, and some also given new generic names (see Kottelat, 2013: 481–483), including Barbodes, Desmopuntius, Oliotius, Pethia, Puntigrus, Striuntius, and Systomus. Many of the species previously identified as Puntius binotatus or its species complex are now reassigned to the genus Barbodes (Kottelat, 2013: 482).
Accepted by: Kevin W. Conway
1 Lee Kong Chian Natural History Museum, National University of Singapore, 2 Conservatory Drive, Singapore 117377; Email: heokhui@nus.edu.sg (*corresponding author)
2 Environmental Biology Division, Institute of Biological Science, College of Arts and Sciences, University of the Philippines Los Baños, 4031 Los Baños, Laguna, Philippines; Email: dmhusana@up.edu.ph
© National University of Singapore
ISSN 2345-7600 (electronic) | ISSN 0217-2445 (print)
Amongst the Sundaic populations of Barbodes, there is one cave-dwelling (troglobitic) species known from Java—B. microps. This poorly known species was described by Günther (1868) from the Gunung Sewu cave system, Central Java (according to Weber & de Beaufort, 1916: 186). Barbodes microps apparently exhibits a complete lack of pigmentation (see Kottelat et al., 1993: pl. 16) and variation in eye size and eye presence (eyes absent in some individuals). Haryono (2006) reported on the morphometry and meristics of 10 specimens of B. microps, and demonstrated morphometric differences between B. microps and B. binotatus (based on individuals from Sumatra, Kalimantan, and Java).
Exploration of aquatic habitats in cave systems of the Philippines by the second author has resulted in the discovery of two cave-dwelling fish species to date. This includes the gobiid fish Caecogobius personatus (described by Larson & Husana, 2018) and an undescribed cyprinid of the genus Barbodes.
The present paper serves to describe this new species of Barbodes, which represents the first record of a cavedwelling cyprinid fish from the Philippines. We also take this opportunity to redescribe the poorly known B. montanoi, a putative close relative of the new species described by Sauvage in 1881.
MATERIAL AND METHODS
Specimens were visually targeted and caught with a hand net (around 15 × 15 cm opening, mesh size 5 mm) while snorkelling in the cave waters. Specimens were fixed in formalin and subsequently stored in 75 % ethanol. Specimens were measured from the left side using dial calipers (accuracy to 0.5 mm). Meristics and measurements were taken according to Kottelat (2001) and Kottelat & Freyhof (2007). The last two branched dorsal and anal rays supported by a single pterygiophore (appearing as a single ray branched at the base) are noted as ‘1½’. Vertebral and fin-ray counts were obtained from digital radiographs using a Faxitron LX-60 digital x-ray machine.
Specimens examined are deposited at the Muséum national d’Histoire naturelle (MNHN), Paris, France; National Museum of the Philippines (PNM), Manila, Philippines; and the Zoological Reference Collection (ZRC), Lee Kong Chian Natural History Museum, Singapore. Abbreviations used: SL – standard length, length measured from tip of upper jaw to base of caudal fin; BL – trunk length, length measured from posterior edge of operculum to base of caudal fin; HL – head length, length measured from tip of upper
jaw to posterior edge of opercle.
TAXONOMY
Barbodes pyrpholeos, new species (Figs. 1–8)
Unidentified cyprinid fish – Husana, 2020: 216.
Material examined. Holotype — PNM 15649, 104.1 mm SL; Philippines: Mindanao, Agusan drainage; Ugnop Cave system; coll. D. E. Husana, 14 May 2014.
Paratypes — PNM 15650, 2 ex., ZRC 61230, 3 ex., 69.6–93.1 mm SL; same locality data as holotype. — PNM 15651, 3 ex., ZRC 61231, 3 ex., 68.2–103.4 mm SL; Philippines: Mindanao, Agusan drainage; Ugnop Cave system; coll. Prosperidad Mountaineering Club, 1 May 2012. — ZRC 61232, 2 ex., 59.7–76.1 mm SL; Philippines: Mindanao, Agusan drainage; Ugnop Cave system; coll. D. E. Husana and local residents, 14 May 2014.
Diagnosis. Barbodes pyrpholeos can be differentiated from all congeners by the following unique combination of characters: body with little brown pigment, appearing white or pinkish in life; unpaired fins with posterior half bright orangey-red in life, anterior half of unpaired fins and paired fins hyaline; eyes present and pigmented, possibly still functional. All other congeners (except the cave-dwelling B.
microps) having body with black blotches, bars, stripes, dots, and triangular markings; body and fins appear pigmentless in B. microps (information on colours in life not available). Barbodes pyrpholeos can be further differentiated from B. microps (some data obtained from Haryono, 2006) in having the following characters: eye present, though variable in size (based on available material only) vs. eye absent or
represented by a small, possibly non-functional eye in some individuals of B. microps; more dorsal-fin rays (8–9½, vs. 8); greater mean head length (32.3% SL, vs. 30.8%); lower mean predorsal length (55.1% SL, vs. 57.5%); lower mean body depth at anus (20.6% SL, vs. 36.5%); lower mean caudal peduncle depth (12.4% SL, vs. 14.7%); larger eye
From the geographically close congener Barbodes montanoi, the new species can be further distinguished by having a smaller eye (eye diameter 14.9–22.3% HL, vs. 21.9–29.4%), longer head (head length 30.7–34.1% SL, vs. 27.4–29.5%), slimmer body (body depth 19.1–22.2% SL, vs. 23.6–25.5%), slimmer caudal peduncle (caudal peduncle depth 11.6–12.9% SL, vs. 13.8–15.3%); last unbranched dorsal-fin ray spinous, but without serrations (see Fig. 8; vs. serrations present on last unbranched dorsal-fin ray); lateral series scales 23–25 (mode 23) (vs. 24–27, mode 24); predorsal scales 8–9 (mode 9) (vs. 8).
Description. See Figs. 1–7 for general impression, and Table 1 for meristic and morphometric data.
Body slim, deepest at dorsal-fin origin (27.9–31.7% SL), tapering to its narrowest at caudal peduncle (11.6–12.9% SL). Head blunt (head depth 56.3–68.5% HL, head width 54.1–63.9% HL), relatively long about ⅓ of standard length (head length 30.7–34.1% SL). Mouth sub-terminal, two pairs of maxillary barbels, barbels longer than eye diameter (up to three times), posterior pair longer than anterior, reaching past eye posterior margin. Eye relatively small (eye diameter
14.9–22.3% HL). Mouth large, gape height 9.0–15.1% SL, 26.6–43.3% HL; mouth width 9.2–15.1% SL, 29.8–46.9% HL. Dorsal-fin origin and pelvic-fin origin at roughly midbody (predorsal-fin length 51.2–56.7% SL; pre-pelvic fin length 53.4–61.9% SL), anal-fin origin at ¾ length of body (preanal-fin length 72.3–79.2% SL). Dorsal and anal fins triangular in shape, with a smooth and straight anterior margin, straight posterior margin. Caudal fin symmetrically forked (upper caudal-fin lobe length 25.5–33.3% SL; lower caudal-fin lobe length 25.5–33.0% SL). Pelvic fins triangular-shaped with straight margins, pectoral fin rounded.
Lateral series with 23–25 scales (mode 23), 8–9 predorsal scales (mode 9), 4½.1.2½–3½ transverse scales, 11–12 circumpeduncular scales (mode 11), 4½ scales between lateral series and pelvic-fin origin. Vertebral count 17–18
14–15 = 32 (mode = 32; n = 8).
RAFFLES BULLETIN OF ZOOLOGY 2021
Live colouration. See Figs. 1–3. Head and rest of body white or pinkish, with some body scales silvery. Eyes pigmented. Posterior half of unpaired fins orange-red, anterior half hyaline. Paired fins hyaline; posterior margin of pelvic fin with slight orange tint (observations based on photographs of 1–2 freshly caught specimens).
Preserved colouration. See Figs. 4–7. Head and rest of body cream, with yellowish overtone. Dorsum of head and anterior part of body with extremely faint light brown pigment, most obvious around posterior margin of dorsal scales and forming weak reticulate pattern. An extremely faint light brown rounded blotch on caudal peduncle anterior to caudal-fin base. All fins hyaline.
Tan & Husana: A new cave-dwelling cyprinid fish from the Philippines
Distribution. Known only from karstic cave systems in Mindanao Island, the Philippines.
Field notes. See Larson & Husana (2018: 98, fig. 1) and Husana (2020) for view of the habitat and syntopic species. Barbodes pyrpholeos was originally discovered by Arnel Pasilan (Prosperidad Mountaineering Club) during their earlier exploration, and brought to the attention of the second author.
Etymology. The species name is a combination of the Greek words pyr, meaning fire, and pholeos, meaning cave, in reference to the fiery red fins of this cave-dwelling species. Used as a noun in apposition.
Remarks. To date only three species of cave fish are recorded in the Philippines, viz. Caecogobius crypthophthalmus Berti & Ercolini, 1991, Caecogobius personatus Larson & Husana, 2018, and this present new species, Barbodes pyrpholeos. The majority of Philippine aquatic cave species recorded
so far are invertebrates. Husana (2020) reviewed various species of cavernicolous crabs in the Philippine archipelago, belonging to the families Gecarcinucidae, Gecarcinidae, Hymenosomatidae, Sesarmidae, and Varunidae. Shrimps of the families Alpheidae, Atyidae, and Palaemonidae were also recorded from various caves in different parts of the archipelago (Cai & Anker, 2004; Cai & Husana, 2009). There are also other smaller invertebrates present in the same cave systems, including amphipods (Melitidae), copepods
(Boholiniidae), isopods (Cirolanidae), and gastropods (Neritiliidae) (Fosshagen & Iliffe, 1989; Bruce & Iliffe,
1992; Kano & Kase, 2004; Sawicki, Holsinger & Iliffe, 2005). Still, many undescribed species from various caves in different parts of the Philippines were observed and collected by the second author during speleological expeditions, and this material awaits further study.
Until now, no cave-dwelling Barbodes has been documented from the Philippines. Barbodes pyrpholeos is not only the first known cave-dwelling cyprinid described from the Philippines, but is also only the second species of cave-dwelling cyprinid reported from the Sundaic islands. Barbodes microps, the
first species of cave-dwelling cyprinid reported from the Sundaic islands, was described by Günther in 1868 from material collected in Central Java. Little information is available for B. microps, but it appears to be pigmentless (see Kottelat et al., 1993: pl. 16).
Along with the collection of Barbodes pyrpholeos, pigmented and eyed Barbodes were obtained from surface waters in close proximity to the Ugnop Cave system. Based on morphological characters and geographic location, these individuals were identified as Barbodes montanoi. Based on geographic proximity, B. montanoi may be a close relative of B. pyrpholeos, but this subject requires further investigation with morphological and molecular characters and is beyond the scope of this study. As B. montanoi is poorly known, we take this opportunity to redescribe this species.
Barbodes montanoi (Sauvage, 1881)
(Figs. 8–11)
Puntius montanoi Sauvage, 1881: 103; Bertin & Estève, 1948: 29.
Barbodes montanoi (Sauvage) – Herre, 1924: 292; 1953: 125;
Kottelat, 2013: 79.
Material examined. Syntypes — MNHN 3398, 1 ex., ca. 90 mm TL; Philippines: Mindanao, Simulao River; Montano, 1880 [low resolution image only; https://science.mnhn.fr/institution/mnhn/collection/ic/item/list?scientificName=puntius+montanoi]. — MNHN 3399, 4 ex. (of 12); Philippines: Mindanao [low resolution images and digital radiographs only; https://science.mnhn.fr/institution/mnhn/collection/ic/item/a-3399?listIndex=2&listCount=2].
Non-type material — PNM 15652, 6 ex., ZRC 61233, 6 ex., 17.5–87.2 mm SL; Philippines: Mindanao, Agusan drainage; Enchanted Falls; coll. D. E. Husana, 14 May 2014. — ZRC 61234, 2 ex., 50.0–67.2 mm SL; Philippines: Mindanao, Agusan drainage; pools at Ugnop; coll. Prosperidad Mountaineering Club, 1 May 2012.
Diagnosis. Entire body yellowish-brown dorsally and cream ventrally, with faint brown reticulate pattern corresponding to anterior margin of exposed part of body scales; body pattern consisting of four to six black dots or dashes (dependent on ontogenetic stage), two positioned at base of dorsal fin and
anal fin (anal-fin spot missing or faint in adults), one at dorsal part of opercular opening (missing or faint in adults), one at mid-body below dorsal-fin origin, one at mid-body above anal-fin origin, one at middle of caudal peduncle anterior to caudal fin; unpaired fins anterior half golden-yellow, posterior half reddish-orange; paired fins yellowish or hyaline; eyes present and pigmented; last unbranched dorsal-fin ray spinous, with 8–12 weak serrations on specimens smaller than 62 mm SL (see Fig. 8); lateral scale series 24–27 (mode 24); predorsal scales 8.
Barbodes montanoi is chiefly distinguished from other selected Philippine and Sundaic congeners as follows: from B. amarus, B. lateristriga, and B. kuchingensis by having a pattern of black spots on the body (vs. body without black markings in B. amarus; pattern of two black bars on anterior half of body with central black stripe on posterior half of body
in B. lateristriga and B. kuchingensis); from B. manguaoensis and B. palavanensis by having larger black spots, covering 2–3 scales (vs. smaller spots, restricted to single scale); from B. banksi, B. bunau, and B. rhombeus by having a small round black spot below dorsal-fin base (vs. black triangular marking in B. banksi and B. bunau; short black bar in B. rhombeus); from B. binotatus by having fewer black spots
on body when young (ca. 4 vs. ca. 9); from B. dunckeri by the absence (vs. presence) of orange pigment on the paired fins in life; from B. everetti by having distinct black spots on body in sub-adults and adults (vs. black spots on body connected by black lateral stripe in sub-adults and adults); and from B. sealei by having only 8–12 weak serrations on last unbranched dorsal-fin ray in specimens smaller than 62 mm SL (vs. last unbranched dorsal-fin ray with 13–21 welldeveloped serrations in specimens larger than 60 mm SL).
Description. See Figs. 9–11 for general impression, and Table 1 for meristic and morphometric data.
Body slim, deepest at dorsal-fin origin (31.8–35.7% SL), tapering to its narrowest at caudal peduncle (13.8–15.3% SL). Head pointed (head depth 68.9–73.9% HL, head width 54.5–60.7% HL), relatively short, less than ⅓ of standard length (head length 27.4–29.5% SL). Mouth sub-terminal, two pairs of maxillary barbels, barbel not longer than eye diameter, posterior pair longer than anterior, reaching past middle of eye. Eye relatively large (eye diameter 21.9–29.4% HL). Dorsal-fin origin and pelvic-fin origin at mid-body
(predorsal-fin length 53.1–56.1% SL; pre-pelvic fin length 51.8–54.5% SL), anal-fin origin at ¾ length of body (preanalfin length 74.7–76.9% SL). Dorsal and anal fins triangular in shape, with a smooth and straight anterior margin, straight posterior margin. Caudal fin forked with upper lobe slightly longer (upper caudal-fin lobe length 30.7–33.2% SL; lower caudal-fin lobe length 29.1–30.4% SL). Pelvic fin triangular with straight margin, pectoral fin rounded. Lateral series with 24–27 scales (mode 24), 8 predorsal scales, 4½.1.3 transverse scales, 12 circumpeduncular scales, 4½ scales between lateral series and pelvic-fin origin. Vertebral count 17–19 + 13–14 = 31–32 (mode = 32; n = 9).
RAFFLES BULLETIN OF ZOOLOGY 2021
Live colouration. See Fig. 9 for fresh colouration. Head and body dorsum brownish, sides golden, venter silverish to cream. Body scales with anterior portion with narrow, dark brown edge, giving a reticulation pattern. Body with distinct black to dark brown dots or dashes (number of dots variable dependent on maturation stage), one dot just above dorsal part of opercle opening, one dot at dorsal-fin base, one
dot along mid-body below dorsal-fin origin, one dot along mid-flank above anal-fin origin, one dot at anal-fin base, dot spot along middle of caudal peduncle before caudal-fin base. Unpaired fins with anterior portions yellowish and middle to posterior portions orange to red. Paired fins yellowish-brown.
Preserved colouration. See Figs. 10, 11 for preserved colouration. Head and body brownish, darker on dorsum and cream on ventrum. Four to six distinct dark brown/black dots or dashes along flank, all larger or equal to eye diameter. Faint brown blotch on body just posterior to edge of opercle. First distinct dark brown spot at anterior base of dorsal fin, second dark brown spot on mid-flank below dorsal-fin origin, third dark brown tiny blotch along mid-flank above anal-fin origin, fourth dark brown spot on middle of
caudal peduncle before caudal-fin base. A faint brown spot can sometimes be visible above the anal-fin base. Some individuals (50–60 mm SL) with interrupted dark brown lateral stripe, running from opercle edge to caudal-fin base. All fins hyaline.
In a juvenile (Fig. 11; 32.2 mm SL), six distinct black to dark brown spots can be observed. The locations of the spots as above, except the spot on body just posterior to opercle edge and above the anal-fin origin are very distinct. All spots equivalent to or slightly larger than eye diameter.
The ontogenic change in body pattern is exhibited where the number of body spots decreases with age, as noted by Kottelat (2013: 482).
Tan & Husana: A new cave-dwelling cyprinid fish from the Philippines
Distribution. Reported from Mindanao only. This species may be restricted to the Agusan River basin in Mindanao, Philippines. Further surveys are necessary to clarify the true distribution of this species.
Field notes. Syntopic fish species from Enchanted Falls locality include: Nomorhamphus cf. bakeri (Zenarchopteridae), Gulaphallus cf. panayensis (Phallostethidae), and multiple species of goby (Gobiidae).
Remarks. The type locality for B. montanoi is Simulao River, in central Mindanao (Sauvage, 1881; Kottelat, 2013); and not Simulac River as stated by Fricke et al. (2021). The specimens of B. montanoi examined herein are from the water pools at Ugnop and Enchanted Falls, and likely represent true B. montanoi.
This species was named after the celebrated French traveller and collector Joseph Montano (1844–1914), who passed through Mindanao in 1880 (Herre, 1924: 293). The original description of Puntius montanoi (Sauvage, 1881: 103, 104) is based on 13 individuals (Kottelat, 2013). The MNHN currently contains specimens labelled as both holotype (MNHN 3398) and paratypes (MNHN 3399, 12 individuals) of Puntius montanoi, likely following Bertin & Estève (1948). Following ICZN article 72.1, these 13 specimens must be referred to collectively as syntypes for the following reasons: 1) Sauvage (1881) did not explicitly designate a holotype for Puntius montanoi; and 2) no lectotype designation has taken place in the years subsequent to the original description.
Sauvage (1881) stated that the third bony dorsal ray is smooth (presumably without serrations) and nearly the
length of the head. Based on our examination of the recently collected specimens from Enchanted Falls and radiographs of nine additional specimens (ZRC 61233 and PNM 15652), specimens smaller than 62 mm SL have 8–12 weak serrations on the spinous last unbranched dorsal-fin ray, and specimens larger than 65 mm SL have no visible serrations. This could possibly be attributed to ontogenetic changes with size. The radiograph of four specimens listed as MNHN 3399 shows no signs of serrations on the spinous last unbranched dorsalfin ray, either indicating that they are mature individuals or the digital radiograph is of a resolution grade insufficient to show such fine details. Herre (1924: 293) noted that the absence of dorsal-fin ray serrations would make this species unique among lowland cyprinids found in Mindanao Island.
General notes on Barbodes. There are at least 27 other Barbodes species recorded from the Philippines, most of them poorly known and either not depicted with figures when originally described or badly illustrated. Within Mindanao Island in the Philippines, six other Barbodes have been recorded from riverine habitats (fide Kottelat, 2013—B. cataractae, B. joaquinae, B. montanoi, B. quinquemaculatus,
B. resimus, and B. umalii). There are 17 endemic species of Barbodes that occur only from within Lake Lanao and the single outflow river—B. amarus, B. baoulan, B. clemensi, B. disa, B. flavifuscus, B. herrei, B. katolo, B, lanaoensis, B. lindog, B. manalak, B. pachycheilus, B. palaemophagus, B. palata, B. sirang, B. tras, B. truncatulus, and B. tumba (fide Herre, 1924; Myers, 1960; Kottelat, 2013). From Mindoro, B. hemictenus is recorded; from Balabac, B. ivis is known; from Palawan, B. manguaoensis and B. palavanensis are
listed (see Kottelat, 2013).
From Borneo, B. bunau is described from Sesayap basin in North Kalimantan; B. banksi, B. everetti, B. kuchingensis, and B. lateristriga are recorded from the southern half of Borneo; B. xouthos is known only from Lake Merimbun in Tutong District, Brunei Darussalam, northwestern Borneo; and B. sealei has been collected from throughout Borneo.
From Peninsular Malaysia, B. banksi, B. dunckeri, B. lateristriga, and B. rhombeus are found. From Java, B.
binotatus sensu stricto is now assumed to be restricted to western Java; B. microps is known only from the Gunung Sewu cave system, Central Java (according to Weber & de Beaufort, 1916: 186).
Amongst all these species of Barbodes, B. montanoi looks superficially most similar to B. sealei (only known from Borneo; see Fig. 12), but differs in the following characters: body spots tend to be stretched longitudinally thus appearing ovoid (vs. taller and rounder spots for B. sealei); both species with faint dark brown reticulate pattern on body, but with different extent of pigmentation—B. montanoi with only
anterior portion of non-embedded body scales with brown pigments, vs. B. sealei with crescentic anterior margin of non-embedded body scales with brown pigments; dorsal and anal fins hyaline (vs. presence of narrow dusky black posterior margins for B. sealei); slimmer upper and lower caudal-fin lobes (vs. broad caudal-fin lobes for B. sealei); fewer vertebral count than B. sealei (31–32 [mode = 32, n = 9], vs. 33 [n = 4]); fewer and weak serrations on last unbranched dorsal-fin ray (8–12, vs. 13–21 stronger serrations
for B. sealei).
There are five Barbodes species from the main Sundaic landmass which may look similar to B. montanoi in terms of having a spotted body pattern. They include B. banksi (Fig. 13), B. binotatus (Fig. 14), B. rhombeus (Fig. 15), B. dunckeri (Fig. 16), and B. everetti (Fig. 17). The common feature of these five taxa is that at the juvenile stage, the body pattern consists of numerous black spots and blotches (see Kottelat, 2013: 482). For B. banksi, B. binotatus, and B. rhombeus, the small spots are lost upon maturity, the adult
only retaining the black spot or blotch below the dorsal-fin base, supra-anal region, and caudal peduncle (see Figs. 13–15). For B. dunckeri and B everetti, these spots and blotches enlarge with age (see Figs. 16, 17). Another common feature for all five taxa is the presence of serrations on the spinous last unbranched dorsal-fin ray at both juvenile and mature stages. Barbodes montanoi also exhibits a slenderer body when compared to B. banksi, B. rhombeus, B. dunckeri, and B. everetti.
Herre (1924, 1935) and Myers (1960) suggested that the ancestral stock of the Barbodes species flock in Lake Lanao is Barbodes binotatus. They also indicated that B. binotatus is found throughout the island of Mindanao except within Lake Lanao. At that juncture, the species of origin for the Lake Lanao species flock was not doubted. In today’s context, B. binotatus sensu stricto is believed to be restricted to the island of Java (M. Kottelat, pers. comm.). All other populations of B. binotatus sensu lato are believed to be other named taxa (currently in the synonymy of B. binotatus) or undescribed taxa (M. Kottelat, ongoing research).
Comparative material examined
Philippines.
Barbodes amarus — ZRC 51648, 2 ex., 79.5–125.6 mm SL; Mindanao: Lake Lanao; April 2007.
Barbodes manguaoensis — ZRC 60530, 10 ex., 25.2–54.8 mm SL; Palawan: Taytay, Lake Manguao; 13 October 1988.
Barbodes palavanensis — ZRC 60529, 10 ex., 41.2–57.6 mm SL; Palawan, Irawan; 18 November 1988.
Sundaic area.
Barbodes banksi — ZRC 43643, 10 ex., 23.1–49.7 mm SL; Sarawak: Lundu, Sungai Sebiris, 8.7 km to Sematan on Lundu-Sematan road; 2 October 1998. — ZRC 39387, 5 ex., 58.5–72.5 mm SL; Sarawak: Kampung Matang, 1.3 km to Sungai Cina Matang; 4 September 1995. — ZRC 60155, 9 ex., 35.5–91.6 mm SL; Sarawak: Song District: Rejang River basin: Katibas River: Ulu Katibas, Sungei Merating, draining into Sungei Bloh, 01°38.045′N, 112°17.350′E, 121m asl; 19 May 2018. — ZRC 60076, 18 ex., 14.8–96.0 mm
SL; Sarawak: Song District: Rejang River basin: Katibas River: Ulu Katibas, Sungei Satap, ca. 25 min upriver of Nanga Bloh Field Station, 01°39.240′N, 112°15.108′E, 117 m asl; 24 May 2018.
Barbodes binotatus — ZRC 40127, 13 ex., 21.2–72.2 mm SL; Java: Bogor, tributary of Cipinang Gading; 10 July — ZRC 40141, 8 ex., 33.6–61.0 mm SL; Java: Desa Cinangueng, Kecamatan Ciampea; 10 July 1996.
Barbodes dunckeri — ZRC 60671, 1 ex., 79.6 mm SL; Malaysia: Johoe, Kahang, Gunung Belumut Recreational Forest; 11 June 2018. — ZRC 37602, 1 ex., 58.4 mm SL; Malaysia: Johoe, near Kota Tinggi falls; 1993. Barbodes everetti — ZRC 54289, 13 ex., 12.6–71.6 mm SL; Sarawak: Sematan outskirts, Kampung Poeh, hill stream at base of Gunung Poeh; 5 November 2013. Barbodes rhombeus — ZRC 55401, 7 ex., 36.6–60.7 mm SL; Singapore: Mandai Track 15 stream; 18 June 2015. — ZRC 54686, 20 ex., 25.6–87.2 mm SL; Singapore: Mandai Track 15 stream; 28 July 2015. Barbodes sealei — ZRC 40411, 3 ex., 46.6–70.1 mm SL; Malaysia: Sabah: Danum Valley, Sungei Bilong; 3 October — ZRC 61238, 5 ex., 37.6–94.0 mm SL; Malaysia: Sabah: Kalabakan basin, un-named stream en route to SAFE camp; 21 April 2017. — ZRC 56188, 1 ex., 65.4 mm SL; Sabah: Sandakan, Kabili-Sepilok; 27 April 2017. — ZRC 60536, 5 ex., 59.6–90.5 mm SL; Sabah: Kalabakan Forest Reserve, Brantian basin, 5 m buffer stream; 4 May 2015. — ZRC 60359, 18 ex., 29.0–80.0 mm SL; Sarawak: Sarawak Kiri basin, Annah Rais, Sungai Timouh; 28 September 2018.
ACKNOWLEDGEMENTS
The authors would like to thank the following: Peter Ng and Jose C. E. Mendoza (LKCNHM), for providing the opportunity to work with Philippine cave fish through research fellowship to DEMH; Kelvin Lim, for discussions on fishes; Kevin W. Conway, for handling the manuscript and his patience and helpful comments that vastly improved the paper; two anonymous reviewers for constructive comments
that improved the manuscript substantially; and funding and use of facilities from the Lee Kong Chian Natural History Museum.
The second author would like to thank the following: the Honorable Mayor Albin Magdamit and his staff, especially Noradel Martinez and Marigyn Kamita who demonstrated their enthusiasm to protect the natural environment of their town; the PMC outdoor group, in particular Arnel Pasilan, Almar Lambaco, Joelito Dumdum, Winsome Berdida, and Joseph Mortiz, along with many others, for their assistance
in field and cave explorations; and the barangay chairman, Benecio Manliquez, for providing security and local guides. This research was conducted under auspices of the Department of Environment and Natural Resources (Wildlife Gratuitous Permit no. R13-2014-004).
LITERATURE CITED
Berti R & Ercolini A (1991) Caecogobius cryptophthalmus n. gen. n. sp. (Gobiidae Gobiinae), the first stygobic fish from Philippines. Tropical Zoology, 4(1): 129–138.
Bertin L & Estève R (1948) Catalogue des types de poisons du Muséum national d’Histoire naturelle. 4e partie. Ostariophysaires (Cypriniformes). Muséum National d’Histoire Naturelle, Paris, 117 pp.
Bruce NL & Iliffe TM (1992) Anopsilana conditoria, a new species of anchialine troglobitic cirolanid isopod (Crustacea) from the Philippines. Stygologia, 7(4): 225–230.
Cai Y & Anker A (2004) On a collection of freshwater shrimps (Crustacea Decapoda Caridea) from the Philippines, with descriptions of five new species. Tropical Zoology, 17: 233–266.
Cai Y & Husana DEM (2009) Cave shrimps of the genus Edoneus Holthuisi, 1978, from Luzon, the Philippines, with descriptions of three new species (Crustacea: Decapoda: Atyidae). Raffles
Bulletin of Zoology, 57(1): 51–63.
Fishbase (2019) List of Freshwater Fishes Reported from Philippines. Version 12/2019. https://www.fishbase.se/country/CountryChecklist.php?showAll=yes&what=list&trp
p=50&c_code=608&cpresence=Reported&sortby=alpha2&ext_CL=on&ext_pic=on&vhabitat=fresh (Accessed 20 June 2020). [List includes non-native species] Fosshagen A & Iliffe TM (1989) Boholina, a new genus (Copepoda: Calanoida) with two new species from an anchialine cave in the Philippines. Sarsia, 74: 201–208.
Fricke R, Eschmeyer WN & Van der Laan R (eds.) (2021) Eschmeyer’s Catalog of Fishes: Genera, Species. http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp (Accessed 8 June 2021).
Günther A (1868) Catalogue of the Fishes in the British Museum.
Volume 7. British Museum, London, xx + 512 pp. Haryono (2006) Studi morformetri Ikan Wader Goa (Puntius microps Gunther, 1868) yang unik dan dilingungi undangundang. Berkala Penelitian Hayati, 12: 51–55. [In Bahasa Indonesia] Herre AWCT (1924) Distribution of the true fresh-water fishes in
the Philippines. I. The Philippine Cyprinidae. The Philippines Journal of Science, 24(3): 249–307.
Herre AWCT (1935) The fishes of Lake Lanao: A problem in evolution. The American Society of Naturalists, 67(709): 154–162.
Herre AWCT (1953) A Checklist of Philippine Fishes. Research Report Vol. 20. Fish and Wildlife Service, United States Department of Interior, Government Publishing Office, Washington, D.C., 977 pp.
Husana DEM (2020) Sundathelphusa prosperidad, sp. n. (Decapoda: Brachyura: Gecarcinucidae), a new cave-obligate freshwater crab from Mindanao Island, the Philippines, with notes on the conservation status of Philippine cave species. Journal of Cave and Karst Studies, 82(3): 210–218. ICZN (1999) International Code of Zoological Nomenclature, 4th Edition. The International Trust for Zoological Nomenclature, London, xxix + 306 pp. Ismail GB, Sampson DB & Noakes DLG (2014) The status of
Lake Lanao endemic cyprinids (Puntius species) and their conservation. Environmental Biology of Fishes (2014), 97: 425–434.
Kano Y & Kase T (2004) Genetic exchange between anchialine cave populations by means of larval dispersal: The case of a new gastropod species Neritilia cavernicola. Zoologica Scripta, 33: 423–437.
Kottelat M (2001) Fishes of Laos. Wildlife Heritage Trust, Colombo, 198 pp. Kottelat M (2013) The fishes of the inland waters of Southeast Asia: A catalogue and core bibliography of the fishes known to
occur in freshwaters, mangroves and estuaries. Raffles Bulletin of Zoology, Supplement 27: 1–663.
Kottelat M & Freyhof J (2007) Handbook of European Freshwater Fishes. Kottelat, Cornol & Freyhof, Berlin, xiv + 646 pp. Kottelat M, Whitten AJ, Kartikasari SN & Wirjoatmodjo S (1993) Freshwater Fishes of Western Indonesia and Sulawesi. Periplus Editions, Hong Kong, 221 pp., 84 pls. Larson HK & Husana DEM (2018) A new species of the blind goby Caecogobius (Gobioidei, Gobiidae, Gobionellinae) from a cave system on Mindanao Island, Philippines. Ichthyological Research, 66: 97–103.
Myers GS (1960) The endemic fish fauna of Lake Lanao, and the evolution of higher taxonomic categories. Evolution, 14(3): 323–333.
Sauvage H-E (1881) Description de quelques poissons de la collection du Muséum d’histoire naturelle. Bulletin de la Société Philomathique de Paris, Série 7, 5: 101–104.
Sawicki TR, Holsinger JR & Iliffe TM (2005) New species of amphipod crustaceans in the genera Tegano and Melita (Hadzioidea: Melitidae) from subterranean groundwaters in Guam, Palau, and the Philippines. Journal of Crustacean Biology, 25(1): 49–74.
Weber M & de Beaufort LF (1916) The Fishes of the IndoAustralian Archipelago. III. Ostariophysi: II. Cyprinoidea, Apodes, Sunbranchii. Brill, Leiden, 455 pp.