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(Figs. 1, 2)
Holotype - ZMA 123.714 male, 61.8 mm: Surinam , Upper Marowijne system, Tapanahony River, 5 km downriver from Palumeu on the right bank, a hunting trail leads to a creek 15 minutes walk from the river; 03° 22’ 43”N055° 24’ 41”W , coll. F.B.M. Vermeulen, 14 July 2003 . Station number SU 2003-02.
Allotype - ZMA 123.715 female, 65.1 mm. Surinam , Upper Marowijne system, Palumeu River 20 km upstream from the confluence of the Palumeu and Tapanahony Rivers, small creek 20 minute walk from riverbank, 03° 13’ 51”N055° 23’ 46” W coll. F.B.M. Vermeulen, 16 July 2003 . Station number SU 2003-06.
Paratypes - ZMA 123.716, 2 juveniles, 32.9-36.3 mm specimens collected by S. Sladkowsky and F.B.M. Vermeulen, 20 August 2000 . Station number SVS 2000-02 (same collection locality as holotype). ZMA 123.717, 6 juvenile 31.5-38.1 mm specimens collected by F.B.M. Vermeulen, same collection data as holotype. NZCS F6418, (originally identified as Rivulus cf. lanceolatus Eigenmann, 1909 ZBK ); Ulemari tributary, 13 km upstream of confluence with Litani River, 03° 13’ 23”N054° 15’ 38”W , collected by P. E. Ouboter, S. Sahdew and S. Ramanand, 3- 5 April 1998 . NZCS F7063-F7066, 4 juvenile specimens, same collection data as holotype. MNHN 2004-3096, 1 specimen, same collection data as holotype.
Diagnosis -Distinguished from other Kryptolebias ZBK and Rivulus ZBK species by a combination of characters including low number of LL scales, high number of anal rays, short predorsal length and a robust body (Table 1), and unique mitochondrial DNA gene sequences. Kryptolebias sepia ZBK is further distinguished by remarkably strong melanistic pigmentation and the ability to change this coloration into several distinct patterns, lack of obvious sexual dimorphism, strong dichromatism between juveniles and adults, and absence of the “ Rivulus ” spot in females and juveniles.
Description -A medium sized Kryptolebias ZBK , robust shape, with a non-annual lifecycle. Morphometric data of holotype , allotype and eight paratypes from different localities are given in Table 2 in millimeters and in Table 3 as percent of standard length. Meristic data are in Table 4. Males differ little from females in their body coloration, shape and fins. In adult males yellow marking on the gill cover is slightly more prominent and some but not all males show a few yellow markings along the lateral line. Frontal scalation pattern is in general E-type, but one individual showed mixed E-D-type (Hoedeman 1958). The strong melanism observed in K. sepia ZBK is also observed in at least three other species of Kryptolebias ZBK - K. caudomarginatus , K. brasiliensis and K. marmoratus - and in R. atratus ZBK . However, K. sepia ZBK is differentiated from these species by morphometric data, lower dorsal fin ray count (7.8 vs. 8.6 to 9.0), high anal fin ray count (15.1 vs. 11.2 to 12.6), by the absence of clear sexual dimorphism, by a network of dark markings beginning behind the eye and continuing just posterior of gill cover, by an oblique pattern on the lateral sides, and by their extraordinary capability to change color pattern within seconds. Diagnostic differences are given in Table 1. Kryptolebias sepia ZBK also differs by a strong orange body coloration of juveniles, which otherwise is only known in juvenile R. amphoreus ZBK . With the co-occurring R. urophthalmus ZBK / R. stagnatus ZBK group they share the lower number of dorsal rays and low number of LL scales but differ by a higher number of anal rays (15.1 vs. 12.3), by slightly shorter predorsal length to SL (76.6 % vs. 78.0 %), the absence of red spots forming lateral rows, and other diagnostic characters.
Adult males -See Figures 1 and 2. Body grayish, dark brown near the dorsum, pale white near the belly. Scales on lateral sides show dark pigments forming a network pattern, scale centers are brighter forming five to six light rows from post operculum to the end of peduncle. Eight to 10 oblique bars are shown in subadults and adults depending on their mood. These oblique markings become more permanent and intense after reaching full maturity. Some scales along the lateral line on the anterior part of body show bright yellow color in sexually active males. Head dark brown to reddish brown, in the suprapectoral region a bluish shine is only visible with striking light, cheek pale white without markings. On the operculum, posterior to the eye, a network of deep black blotches start on partly yellow background forming two to three bands. On the lateral sides posterior to the gill opening the black blotches continue in an irregular branched pattern. All fins rounded without any filaments or extensions. Caudal fin shows a wine-red hue that is more intense near the caudal base. Around the caudal fin base a large number of small speckles, mostly situated along the rays, form a reticulated pattern. These reticulations become more intense with age. A dark wine-red margin is often present. Dorsal transparent with reddish hue and irregular wine-red dots, some speckles near the base form a reticulated pattern as in caudal but more subdued. Anal iridescent green, near the base fading to bluish white with numerous fine wine-red speckles forming five to six diagonal lines, more compact towards the fin tip. A wine-red band is weakly visible near the anal fin margin. Ventral fins iridescent pale blue, no markings. Pectorals clear but orange towards the base; color becomes more intense with age. Eyes with a golden-brown iris, more golden when sexually active.
Adult females -See Figures 3 and 4. Same coloration as in adult males. Body graybrown toward the dorsum and whitish gray to white toward the ventrum. Depending on the mood of the female, eight to 10 dark melanistic oblique bars may appear or disappear. Also depending on mood, head black to grayish black, dorsal portion being reddish brown. Chin whitish, operculum black or with black markings on a not very distinct yellow background. All fins rounded without any filaments and with the same colors and patterns as adult males. Eyes same as in males. The so-called “ Rivulus ” spot is normally present on the dorsal portion of the caudal peduncle at its junction with the caudal fin, and is a major identifying feature of Rivulus ZBK females; however, it is not present in this species at any lifestage.
Juveniles -Head and body same as in adults, but the pale white color of the belly is replaced by orange white. Lateral pattern depends on the mood of the individual; see Figures5, 6 and 7. During the night and when frightened, a fine oblique barred pattern appears following the lines of the scales. However, this pattern is also sometimes exhibited in other situations. Often pale golden blotches form an irregular pattern on the sides.
Color in alcohol -Males and females: body brown to yellow brown with barred pattern subdued but visible; chin, lower half of gill cover, and abdomen whitish; operculum with dark markings; unpaired fins with fine brown spots and markings.
Reproduction -Eggs are 2 mm in diameter and have no major filaments on the cambium membrane, but are covered with an elastic and sticky substance. They are placed one by one between roots at the waters edge, or just above it. Under aquarium conditions, K. sepia ZBK deposits more than 50% of its eggs above the waterline. This behavior is occasionally observed in rivuline species of the genus Rivulus ZBK (FBMV pers. obs.). Very low water levels stimulate this species to mate, with males aggressively driving females. Decreasing water level to less than 3 cm instantly result in spawning activity. Color of eggs is dark amber matching the color of the spawning substrate. No differences in egg development time were observed under the three incubation conditions. In fully aquatic environment, eggs develop and hatch in 14 to 16 days at 24°C. On both wet and moist peat moss, eggs develop normally within the 14 to 16 day period, but do not hatch. If not allowed to hatch by immersing them in water, the embryos die within the following next seven days. This species is therefore unlikely to lay eggs capable of undergoing a developmental diapause (Wourms 1972), and the three week period potentially sets the upper time limit for temporary habitat desiccation. Kryptolebias sepia ZBK is also a good jumper and will, as many of its family members do ( Lüling 1971, Huber 1992), seek new water bodies by moving overland through leaf litter if its habitat becomes unsuitable.
Habitat -See Figure 8. Kryptolebias sepia ZBK appears to live only in extremely shallow parts of small creeks in hilly areas, and is restricted to primary forests with a very dense canopy cover. The actual habitat of K. sepia ZBK is found outside the main stream in swampy areas directly adjacent to the creeks themselves. The layer of leaf litter is often thick, sometimes over 50 cm, and is especially thick in the lower parts of creeks and adjacent flooded areas. Kryptolebias sepia ZBK is found in only a few centimeters of water which stands above this leaf layer, and over 95% of the population appears to consist of juveniles. In case of disturbance of the biotope, K. sepia seeks ZBK shelter in the soft bottom layer or jumps out of the water. The creeks proper had permanent running water. The water was clear, mineral poor, but with high concentrations of tannic acid, the so called black water type (Sioli 1984). No aquatic vegetation was present. Water temperatures were not always taken but likely never exceed 23ºC; pH values varied between 4.1 and 5.4, and GH and KH hardness were both <0.5 DH.
Kryptolebias sepia ZBK is found syntopically with Rivulus aff. urophthalmus ZBK and frequently with Rivulus aff. geayi ZBK . On two occasions a third species of Rivulus ZBK was found together with K. sepia ZBK . This species was identified as R. holmiae ZBK by Hoedeman (1961) but moved to R. igneus ZBK by Huber (1991). This species, however, does not fit well with original descriptions of either species, thus its true identity needs further study. The only non-rivulid fish fauna included the rare Pyrrhulina laeta and on one occasion Tatia aff. creutzbergi . Besides these species, no other fish were found in the creek or surrounding leaf litter.
It is likely Kryptolebias sepia ZBK is a predator of small fishes and invertebrates. However, aquarium observations suggest they are not cannibalistic. The authors’ field observations suggest that in general all large and medium sized rivulids feed on tadpoles, ants and mosquito larvae and in many areas they probably contribute to controlling malaria outbreaks.
Distribution - Kryptolebias sepia ZBK was found only in creeks emptying into the Tapanahony and Palumeu Rivers and in the Ulemari River area ( NZCS F 6418-fish collected by P. E. Ouboter, S. Sahdew and S. Ramanand in April 1998 ). Additional collections are needed, including the upper Litani and Marowini River basins, to confirm the authors hypothesis that K. sepia ZBK is wide spread in southeastern Surinam and southwestern French Guiana.
Etymology -The name sepia alludes to the family Sepiidae, the cuttlefish, whose chromatophores also can cause rapid changes in color.
Phylogenetic relationships -The maximum likelihood and the Bayesian likelihood analysis yielded identical topologies. Due to the size of the data set, it was not practical to estimate nodal support of the maximum likelihood topology via bootstrapping. Therefore, we report the maximum likelihood topology, conveying information on branch lengths, and indicate support for individual nodes with Bayesian posterior probability values (Fig. 9). Kryptolebias sepia ZBK shows a statistically well supported sister taxon relationship to K. brasiliensis (Figs. 9, 10). The monophyly of Kryptolebias ZBK whose members in addition to K. sepia ZBK are K. marmoratus , K. caudomarginatus , and K. brasiliensis , is also strongly supported (Figs. 9, 10). These relationships are recovered in all analyses, and strongly support the hypothesis that K. sepia ZBK is indeed a phylogenetic member of the genus Kryptolebias ZBK . Costa (2004b) also placed R. campelloi ZBK into Kryptolebias ZBK , although this species was not included in the analysis on which this taxonomic revision was based; it was reassigned without being listed as examined. The maximum parsimony topology (Fig. 10) suggests that Kryptolebias ZBK is sister to all other Rivulidae as hypothesized by Hrbek & Larson (1999), while the maximum likelihood topology (Fig. 9) suggests that Kryptolebias ZBK is sister to Rivulinae as hypothesized by Hrbek et al. (2004). The phylogenetic placement of Kryptolebias ZBK observed in the maximum likelihood hypothesis (Fig. 9) is also supported by Costa’s (2004b) recent maximum parsimony analysis of morphological data. Thus the most likely phylogenetic hypothesis for Kryptolebias ZBK will need further investigation, but its monophyly and differentiation from Rivulus ZBK is undisputed. The two species ( Rivulus aff. geayi ZBK and Rivulus aff. urophthalmus ZBK ) with which K. sepia ZBK co-occurs, are members of a phylogenetically very distinct Amazonian clade of Rivulus ZBK (Hrbek & Larson 1999), and are not closely related to K. sepia ZBK (Figs. 9, 10).
In the Tapanahony and Palumeu River drainages, as well as in other areas of northern South America there is a pattern of co-appearance of robust and small Rivulus ZBK species. The robust and the small species form reciprocally monophyletic groups which were labeled as the Guyana Coast and Guyana Shield clades, respectively (Hrbek & Larson 1999). Cooccurrence of robust and small species of Rivulus ZBK is usually observed in shaded primary forest of the mountainous highland plateau. These biotopes are characterized by very shallow, slowly running or stagnant water, low pH (3.5-5.1), low mineral concentrations (hardness <0.5 DH), and thick canopy with diffuse light. These marginal habitats are unoccupied by other fish species except for occasional Pyrrhulina ZBK spp.
Typical community compositions include R. igneus ZBK with R. cladophorus ZBK or R. geayi ZBK ; Rivulus aff. igneus ZBK with Rivulus aff. geayi ZBK ; R. waimacui ZBK with R. breviceps ZBK or R. sp. Mahdia ; and R. immaculatus ZBK with R. gransabanae ZBK or R. torrenticola ZBK . Sister clade to the Guyana Coast is the Amazon basin clade (Hrbek & Larson 1999) whose members form similar associations with the eastern Guyana Shield subclade (Hrbek et al. 2004). These associations include R. ophiomimus ZBK with R. rectocaudatus ZBK and R. compressus ZBK with R. duckensis ZBK . However, even within these communities, the robust species tends to be found in flooded swampy parts of the creek, while the smaller species tends to be found in the creek proper. Naturally some species within these clades do not fit this ecological pattern. These species include, for example, R. agilae ZBK which prefers open savannah and secondary forest habitats, and usually occurs alone, or R. hartii which is found in a wide variety of habitats but seem to usually co-occur with poeciliids for which they are a major predator (Reznick 1982). The R. urophthalmus species complex ZBK , which includes R. urophthalmus ZBK , R. stagnatus ZBK , R. deltaphilus ZBK and R. lungi ZBK among others, occurs with rivulids as well as poeciliids.
The newly described Kryptolebias sepia ZBK also fits within this pattern of co-occurrence. Although it superficially resembles robust Rivulus ZBK species, it is a member of a phylogenetically distinct clade, and appears to be ecologically differentiated as well. Formal taxonomic recognition of this clade did not occur until recently when Costa (2004b) described the genus Kryptolebias ZBK . Costa (2004b) reanalyzed Rivulus brasiliensis and its close relatives -all species analyzed in Costa (1998) as well -and no longer found R. brasiliensis and its relatives to have synapomorphies which previously placed it within a monophyletic Rivulus ZBK (Costa 1998). This made Rivulus ZBK non-monophyletic, a hypothesis that has been put forth by molecular phylogenetic analyses (Hrbek & Larson 1999, Murphy et al. 1999), and by an unpublished molecular study reviewed by and cited in Costa (1998). Costa (2004b) therefore proposed the new generic name Cryptolebias ZBK which, however, is preoccupied by a fossil cyprinodont fish (Gaudant 1978). As first reviser, Costa (2004a) substituted the name Kryptolebias ZBK for Cryptolebias ZBK . In spite of a somewhat complicated morphological history, all lines of evidence now clearly show that Kryptolebias ZBK is a clade distinct from the remaining Rivulus ZBK species. Whether the remaining Rivulus ZBK species form a clade (Costa 1998, 2004b) or are non-monophyletic (Hrbek & Larson 1999, Murphy et al. 1999, Hrbek et al. 2004) remains to be resolved, but the taxonomic validity of Kryptolebias ZBK is upheld by this study.
Kryptolebias sepia ZBK is a distinct taxon that is morphologically, ecologically and phylogenetically differentiated from sympatrically occurring robust ( Rivulus aff. igneus ZBK or R. urophthalmus ZBK ) and small ( Rivulus aff. geayi ZBK ) species. It occurs in low densities in a rarely collected primary forest habitat of the central mountains of Surinam, and is easily overlooked in usual surveys. This study clearly shows that a better understanding of rivuline biodiversity, and of the genera Rivulus ZBK and Kryptolebias ZBK specifically, will require a focused collecting effort in appropriate habitats, as well as the combined use of molecular and morphological data in taxonomic and phylogenetic studies.