Abstract

We describe a new, tiny species of Schindleria from a reef lagoon in the Red Sea off the coast of Hurghada, Egypt. Schindleria edentata, new species, belongs to the short dorsal-fin type of Schindleria, with the dorsal and anal fins of about equal length. Schindleria edentata is characterized by an elongated but relatively deep body (body depth at anal-fin origin 10.8% of SL and at 4^th anal-fin ray 10.9 % of SL); a short dorsal fin originating just slightly anterior to the anal fin (predorsal-fin length 60.9% of SL, pre-anal fin length 64.8% of SL); a stubby head with a steep frontal profile, a short snout (i.e., 23.1% of head length), and large eye (i.e., 27.7% of the head’s length); a long pectoral radial plate (length 7.6% of SL); four dorsal and four ventral procurrent caudal-fin rays increasing in length posteriorly; last procurrent ray simple without additional spine and, although the longest, not distinctly elongate; 15 dorsal-fin rays; 13 anal-fin rays; the base of the first anal-fin ray positioned below the base of the third dorsal-fin ray; upper and lower jaws toothless; in vivo with translucent body; eye black; swim bladder capped by a melanophore blotch; no pigmentation externally on body after preservation.

Gobiiformes, morphology, new species, paedomorphosis, progenesis

The genus Schindleria (Giltay, 1934) (Schindler’s fishes or infant fishes) has a large biogeographic range spanning the entire Indo-Pacific from remote South American islands to East and South African coasts, and from the Red Sea to Japan (summarized in Ahnelt and Sauberer 2020). Often found in and close to coral reef lagoons (Leis 1994; Watson 2000; Robitzch et al. 2021a), also offshore and deep-water records have been documented (Belyanina 1989; Parin 1991; Ahnelt and Sauberer 2020). Schindleria are not only among the smallest vertebrates (8 mm– 22 mm, average ca. 17 mm) but also mature rapidly. Some species reach maturity at an average of 37 days and may produce up to nine generations per year (Kon and Yoshino 2002).

Although individuals of Schindleria are likely among the most numerous fishes associated with coral reefs (Gosline and Brock 1960; Whittle 2003; Robitzch et al. 2021) these tiny gobioids are easily overlooked and frequently mistaken for larval fishes (Bogorodsky and Randall 2019; Robitzch et al. 2021a). Numerous records are based on a few specimens only (Ahnelt and Sauberer 2019, 2020; Robitzch et al. 2021b) and these were often collected as by-catch of other research surveys. Therefore, almost nothing is known about the biology and ecology of Schindleria (Robitzch et al. 2021a). To date, the sister group of Schindleria is still unknown and its position among gobioid fishes is still under debate (e.g., Ahnelt 2020; Abu El-Regal et al., 2021). Originally described as species of Hemirhamphus (Schindler 1930, 1931, 1932), these tiny fishes were reclassified as a new genus, Schindleria, and placed in a new family, Schindleriidae, by Giltay (1934) and demonstrated to belong to the Gobioidei by Johnson & Brothers (1993). However, in two molecular phylogenetic studies Schindleria was resolved within the family Gobiidae (Thacker 2009; Agorreta et al. 2013).

Eight nominal species of Schindleria have been described so far: S. brevipinguis Watson and Walker 2004, S. elongata Fricke and Abu El-Regal 2017, S. macrodentata Ahnelt and Sauberer 2018, S. multidentata Ahnelt 2020, S. nigropunctata Fricke and Abu El-Regal 2017, S. parva Abu El-Regal et al. 2021, S. pietschmanni (Schindler 1931), and S. praematura (Schindler 1930). Yet, this number of species underestimates their true diversity as over 25 unrecognized species of Schindleria were documented during two surveys on the Ryukyu, Ogasawara, and Palau Islands (Western Pacific), where nearly all of them are endemic to one of these islands (Kon et al., 2007, 2011). Based on short generation time and high levels of endemism Kon et al. (2007) suggested that large numbers of species throughout the entire range of the genus have remained undescribed.

Schindleria are extremely progenetic (Johnson and Brothers 1993) and are among the most short-lived vertebrates (Kon and Yoshino 2002, Zák et al. 2021). Adult Schindleria have a reduced larva-like, elongate, translucent, and scaleless body with a straight gut and a characteristic caudal complex (comprising two modified last vertebrae, an extremely elongate urostyle, and fused hypurals forming a triangular plate (Johnson & Brothers 1993) and a pair of elongated muscles on each side of the urostyle) (Ahnelt and Sauberer 2018). Many morphological characteristics important for species-level diagnoses in gobioid fishes, mainly involving features of the pelvic and first dorsal fins, are missing in Schindleria (Schindler 1932; Johnson and Brothers 1993). However, Schindleria species are morphologically more diverse than often assumed, having relatively few but distinct characters, which allow the identification of species (Watson and Walker 2004; Kon et al., 2010; Ahnelt and Sauberer 2018, Ahnelt 2020; Abu El-Regal et al. 2021; Robitzch et al. 2021b). For instance, the relative position of the dorsal and anal fins to each other, the number of their fin rays, the number of myomeres and vertebrae (Schindler 1930, 1931; Kon et al. 2007; Fricke and Abu El-Regal 2017a, b), the shape of the pectoral radial plate, the shape of the last procurrent caudal-fin rays, the shape of the lower jaw arch, and details of the dentition of the oral jaws (Ahnelt and Sauberer 2018; Ahnelt 2019, 2020) are helpful in diagnosing species.

In an attempt to group Schindleria specimens morphologically (Ahnelt 2019; Abu El-Regal et al. 2021), two characters seem most useful: (1) relative length of dorsal and anal fins (Ahnelt 2019, 2020) and (2) dentition (Watson and Walker 2004; Ahnelt 2020). The dentition of the jaws allows distinction of two main groups: species with jaw teeth and species that lack teeth in one or both jaws. In six out of the eight described species of Schindleria, teeth are present on both, the premaxilla and the dentary (Ahnelt 2020). Among the remaining two species of Schindleria, S. parva has a toothless dentary but a toothed premaxilla (Abu El-Regal et al. 2021) and S. brevipinguis lacks teeth in both jaws (Watson and Walker 2004). These two species share a very small size (<12 mm SL and <9 mm, respectively). In the present study we describe another tiny species of Schindleria with toothless jaws.

The holotype of Schindleria edentata is deposited in the Natural History Museum in London, Great Britain, and registered as BMNH 2007.5.20.1 (Abu El-Regal and Kon 2008). The specimen was collected with a plankton net (500 mm mouth diameter, 0.5 mm mesh size). Already dead when the net was emptied, it was preserved in 10% buffered formalin and later stored in 70% ethanol (Abu El-Regal and Kon 2008). Counts were taken and measurements were made with a stereomicroscope and a micrometer eyepiece to the nearest of 0.1 mm by HA. The length of the urogenital papilla was measured from the anterior point of the ventral attachment of the papilla to its most distal tip.

Morphometric and meristic differences between S. edentata, S. brevipinguis and S. parva, the only three species lacking teeth in one or both jaws, are highlighted in grey in Table 1 and Table 2.

Due to its subsequent preservation, the specimen has now a dark brown to blackish color (Fig. 1A). Hence, the exact position of the swim-bladder was determined using a photograph taken by MAE-R of the holotype shortly after its collection (Fig. 1B). The caudal fin is now partly damaged and its shape has been described from the same original photograph.

Figure 1. 

A Holotype of Schindleria edentata (BMNH 2007.5.20.1), male, SL 9.0 mm; Egypt, Hurghada. Arrows indicate position of broken-off first and second dorsal fin rays. Scale bar = 1 mm. Photo H. Ahnelt. B Same specimen, but photo taken shortly after initial collection. Grey arrow indicates position of last dorsal fin ray, black arrow indicates position of swim bladder. Scale = 1 mm. Photo M. Abu El-Regal.

We follow Thacker (2009) and Agorreta et al. (2013) who considered Schindleriidae as junior synonym of Gobiidae, a view also adopted by Gill and Mooi (2010), Nelson et al. (2016), Betancur-R et al. (2017) and Parenti (2021). Other authors have continued to classify Schindleria in its own family Schindleriidae (e.g., Fricke and Abu El-Regal 2017; Abu El-Regal et al. 2021).

The new species Schindleria edentata from the Red Sea is the ninth in the genus and the fourth species endemic to the Red Sea. Six of nine species of Schindleria are known from the margins of the distributional range of the genus: S. edentata, S. elongata, S. nigropunctata, and S. parva from the Red Sea and S. pietschmanni and S. praematura from the Hawaiian Islands (Northern Central Pacific). The three other species are known from the Society Islands (S. multidentata), from Queensland, Australia (S. brevipinguis) and from the Malayan Archipelago (S. macrodentata) (Ahnelt, 2020). The recent discoveries of three new species endemic to a relatively small area in the extreme north of the Red Sea (Fricke and Abu El-Regal 2017a, b; this study) support Kon et al.’s (2011) view that there are high levels of endemism and potentially unrecognized species in the genus Schindleria.

Adults of Schindleria are characterized in life by a translucent body with blackish eyes and a black-capped swim bladder, features otherwise common among many larval fishes (Johnson and Brothers 1993). Life coloration of S. nigropunctata (Fricke and Abu El-Regal 2017b) and S. praematura (Whittle 2003), has been described as including orange blotches extending along the ventral surface of the body. Some studies have reported dark spots or dots on the body in S. nigropunctata (Fricke and Abu El-Regal 2017b) and S. praematura and S. pietschmanni (Watson 2000). But such a type of pigmentation is likely to disappear after preservation (S. nigropunctata) and is not species specific (Ahnelt 2019) as it is shared by S. praematura and S. pietschmanni. Schindler (1930, 1931) mentioned that individuals of the latter two species were not pigmented except for the swim bladder and the eyes, an observation confirmed by Johnson and Brothers (1993). In some species identified as S. praematura, juveniles and larvae had black melanophores in the ventral midline but no such pigment was reported in adults (Sardou 1974; Ozawa and Mazui 1978). Based on our current state of knowledge, preserved adult specimens have no pigmentation on the body.

A reliable character to group species of Schindleria is the relative length of their dorsal and anal fins. Already the first two described species, S. praematura and S. pietschmanni, are easily distinguished by this feature (Schindler 1932). In S. praematura, the dorsal fin is distinctly longer than the anal fin; while in S. pietschmanni both fins are of about equal length (Schindler 1932). This character is, however, not diagnostic at the species level but rather serves the initial separation into two groups, the LDF and SDF groups. There is evidence for various unrecognized species within both groups (Kon et al. 2007) and samples from the Indo-Pacific Ocean (Ahnelt and Sauberer 2018, 2019) match either the LDF type of S. praematura or the SDF type of S. pietschmanni (Kon et al. 2007; summarized in Ahnelt and Sauberer 2020). All currently valid species of Schindleria can be assigned into one of these two groups. The new species S. edentata is a SDF species together with S. brevipinguis, S. parva, and S. pietschmanni (Ahnelt 2019, 2020; Abu El-Regal et al. 2021). Although three of the four SDF species are among the smallest Schindleria (<12 mm SL), this feature is likely not size related. With up to 20 mm, the SDF S. pietschmanni is among the larger Schindleria.

An important morphological character system to distinguish species is the diverse dentition pattern. Schindleria can be separated into species with jaw teeth and those that lack teeth in one or both jaws (Watson and Walker 2004; Ahnelt and Sauberer 2018; Ahnelt 2020; Abu El-Regal et al. 2021). In most species (S. elongata, S. macrodentata, S. multidentata, S. nigropunctata, S. praematura, and S. pietschmanni), teeth are developed on the premaxilla and the dentary (Ahnelt 2020). In the majority of these species, the teeth are tiny, numerous, and densely set. In general, there are differences in the dentition of both jaws. On the premaxilla teeth extend in a single row along the entire length of its ventral edge. On the dentary teeth are positioned in up to three rows on a bony ridge that extends from the symphysis posterolaterally (Johnson and Brothers 1993; Ahnelt 2020). Exceptions are S. macrodentata, with few, large and widely spaced teeth (Ahnelt and Sauberer 2018) and S. multidentata, with additional teeth on the dorsal edge of the posterior half of the dentary (Ahnelt 2020). In three species, teeth are missing either in one or both jaws. In S. parva the dentary is toothless but the premaxilla is toothed (Abu El-Regal et al. 2021). In S. brevipinguis (Watson and Walker 2004) and in S. edentata, teeth are missing in both jaws. These three species have in common that they are very small in size (8 mm –12 mm SL). We speculate that partial or complete reduction of the dentition in these latter three species may be linked to their small size with the two smallest species (S. edentata and S. brevipinguis) having completely toothless jaws. Specimens thought to be adult were actively feeding and had their guts filled with content that could not be further identified and it is still unclear on what and how Schindleria are feeding.

The generation time and the developmental time for the two toothless species are unknown but it is conceivable that the smaller species may have an even shorter lifespan and faster development. For instance, the specimens of the “S. praematura”–type (LDF) from Ogasawara (Japan) reach a size of 16 mm – 18 mm SL after an average of just 31 days (Kon and Yoshino 2002). During development of many gobiid fishes teeth appear first in larvae of 4 mm – 9 mm TL (e.g., Peters 1983; Daoulas et al. 1993; Strydom and Neira 2006; Kondo et al. 2012; Zanella et al. 2017; Hwang et al. 2018). In Schindleria sp., teeth were first found at a size of 4.2 mm – 4.5 mm SL (Watson 2000) and in S. pietschmanni at 4.5 mm – 5 mm SL (Watson &Walker 2004), with teeth first forming on the praemaxilla and subsequently on the dentary. Whether toothlessness in S. brevipinguis and S. edentata is the result of a more truncated development than that in S. parva, a species with a toothed premaxilla but a toothless dentary, needs to be confirmed in future studies.

H.A. and M.A.E-R. conceived the idea. M.A.E.-R. sampled the material. H.A., V.R. and M.A.E.-R. analyzed, interpreted, and discussed the data, contributing significantly to the final version of the manuscript.

The authors declare no competing interests.

For the loan of the material we are indebted to James Maclaine, Natural History Museum, London, GB. The constructive comments of one anonymous reviewer and the associate editor are gratefully acknowledged.