A new species of Schindleria (Teleostei: Gobiiformes: Gobiidae) from the Red Sea (Saudi Arabia) with a specialized caudal-fin complex

specialized


Introduction
Species of the gobiid genus Schindleria are among the "most extreme example of progenetic developmental truncation known among fishes" (Johnson and Brothers 1993).Some species already mature at a size of 10 mm total body length (TL) or less and are the smallest vertebrates of the oceans (Watson and Walker 2004).They are also among the fastest reproducing vertebrates in the world with an extremely short generation time (of up to nine generations per year) reaching maturity at 23 to 60 days of age (Kon and Yoshino 2002).So far, very little research has been undertaken on the biology and ecology of this taxon (Robitzch et al. 2021(Robitzch et al. , 2022)), likely because species of Schindleria are tiny, translucent, and resemble larval stages for which they are easily mistaken (Bogorodsky and Randall 2019;Robitzch et al. 2021).
Progenetic, developmentally truncated fishes resemble the larval stages of their ancestors with the gonadal development distinctly exceeding the somatic development (Rüber et al. 2007;Britz and Conway 2009;Britz et al. 2014).Characteristic for the larvae of most teleost species are three stages in the development of the notochord (chorda dorsalis): the "preflexion" stage with a straight notochord, the "flexion" stage during which a dorsal flexion of the caudal-most part of the notochord starts, and the "postflexion" stage at which the caudal-most part of the notochord is fully bent dorsally (Kendall et al. 1984).During the preflexion stage, the hypurals, the skeletal elements that carry the principal caudal fin rays, start to develop on the ventral side of the caudal end of the notochord and are thus pointing ventrally in most teleost species.During the dorsal flexion of the caudal end of the notochord, the hypurals and finally also the caudal fin gradually moves into a final, horizontal position (e.g., Ott et al., 2012;Desvignes et al., 2018;Thieme et al., 2021).With the transformation of the notochord into the vertebral column, this gradual up-turning of the chorda dorsalis becomes less distinct, and once ossified as the urostyle (or terminal compound centrum) is barely recognizable (Schultze and Arratia, 1989;Thieme et al., 2021).
Generally, in Gobiidae, the urostyle is relatively small, of about half the size of a regular caudal centrum, and is fused with the upper half of the hypural plate (= hypural 3+4) (e.g., Murdy 1985;Scsepka et al. 1999;Kindermann et al. 2007;Ghanbarifardi et al. 2020).As a synapomorphy of the genus, the urostyle in Schindleria is exceptionally elongated and of about the same length as preural vertebrae 2-5 (Schindler 1932;Johnson and Brothers 1993).The two hypural plates are tightly fused to each other and form a roughly triangular cartilaginous plate (hypural 1-4; hypural 5 is missing in Schindleria) (Johnson and Brothers 1993).The upturned tip of the urostyle is hook-like and firmly attached to the edge of the upper half of this plate, dorsally.This arrangement of the caudal skeleton is typical for Schindleria (Johnson and Brothers 1993;Ahnelt and Sauberer 2018) and independent of the species and its size.It is present in large species such as S. praematura (22 mm TL) (Schindler 1930) or small species such as S. brevipinguis (8.6 mm TL) (Watson and Walker 2004).
Because species of Schindleria reach maturity within a few weeks and at an extremely early somatic developmental stage (Kon et al. 2007), the skeleton, but also the entire bauplan of adult Schindleria leaves the impression of overall morphological simplification.Such a simplification by undeveloped or incompletely developed characters in relation to close relatives make it challenging to separate Schindleria species at a morphological level (Kon et al. 2007;Ahnelt and Sauberer 2018;Ahnelt 2019).This is possibly the major reason why only nine species have been nominally described so far: S. praematura (Schindler, 1930), S. pietschmanni (Schindler, 1931), S. brevipinguis Watson & Walker, 2004, S. nigropunctata Fricke & Abu El-Regal, 2017, S. elongata Fricke & Abu El-Regal, 2017, S. macrodentata Ahnelt & Sauberer, 2018, S. multidentata Ahnelt, 2020, S. parva Abu El-Regal, El-Sherbiny, Gabr & Fricke, 2021, and S. edentata Ahnelt, Robitzch & Abu El-Regal, 2022.Nevertheless, it can be assumed that a number of undescribed species still remain unrecognized given the huge distributional range of this genus, which spans the entirety of the tropical and subtropical Indo-Pacific, from Central and South America in the East, to South Africa and the Red Sea in the West (Ahnelt and Sauberer 2020).So far, based on just two genetic studies in the Western Pacific, as many as 25 genetic species-level lineages have been identified (Kon et al. 2007(Kon et al. , 2010)).Because many of these lineages were restricted to single islands, generally a high level of endemism is expected in Schindleria.The Red Sea is known as a hotspot for marine endemism (e.g., DiBattista et al. 2015) and may also harbor high levels of endemism in Schindleria.Just from a single locality in the northern Red Sea, close to Hurghada, Egypt, four species have been documented, from which three have been new (Fricke andAbu El-Regal 2017a, 2017b;Abu El-Regal and Kon 2019;Ahnelt et al. 2022) (Fig. 1).(Robitzch et al., 2021).The map is from https:// www.landkartenindex.de/kostenlos/cliparts/cliparts_gruppe_1/saudiarabien.gif.
Herein, we describe a new species of Schindleria, based on three females from the Red Sea, Saudi Arabia, which is characterized by two peculiar characters: (1) a straight unflexed urostyle, which is not fused to but inserted into the hypural cartilage and (2) very few but very large eggs.

Material and methods
The three type specimens of Schindleria qizma are deposited in the Naturhistorisches Museum in Wien (NMW), Vienna, Austria and registered as NMW 99999 (holotype) and as NMW 100000 and NMW 100001 (paratypes).
The three adult (i.e., females with visibly developed eggs) specimens of Schindleria qizma were collected at the mid-shelf reef Al Fahal (Arabic for "the great/ mighty", due to its large size) off of the coast of Thuwal, Red Sea, Saudi Arabia, using three Bellamare collapsible LED battery-powered light traps (of 500-micron mesh), set at ~ 2 m below the surface, fixed to moorings at the wave-protected, northern-end of the reef (22°18'24.54"N,38°57'47.25"E),with a bottom depth of approx.10 m to 12 m.LED lights are efficient in attracting fish larvae as well as Schindleria during the night time (see e.g., Robitzch et al. 2020Robitzch et al. , 2021)).The light traps were deployed during the day around new moon for a period of ~ 24 h for collections to take place during the entire night.The specimens of S. qizma were collected on 19 and 22 of February 2015 and on 17 of June 2015.Sampling was in accordance with the policies and procedures of the King Abdullah University of Science and Technology (KAUST, Saudi Arabia) and permits for sampling were obtained from the relevant Saudi Arabian authorities.The collection did not involve endangered species.
We follow the distinction into species groups in Schindleria based on the two dorsal-fin types as defined by Ahnelt (2019).
Because the three females of our new species have their very large eggs arranged in a double row anteriorly, we provide the total number of eggs and compare these with the total number of eggs in other species.This is in contrast to previous counts of the number of eggs in female Schindleria, which has been given for one of the two ovaries only and counted in a single row (e.g., Fricke and Abu El-Regal 2017a; Ahnelt and Sauberer 2018;Ahnelt 2020;Abu El-Regal et al. 2021).
Pictures of the specimens preserved in 70% EtOH were taken with a Nikon DSRi-2 camera mounted on a Nikon SMZ25 stereo microscope using NIS-Elements Microscope Imaging Software (BR V.5.02) with a Real Time Extended Depth of Focus patch.The images were processed with Adobe Photoshop CS5 for the final figure plates.
Measurements were made with the aid of a stereo-microscope and a micrometer eyepiece to the nearest 0.1 mm by H.A.
Diagnosis.A member of the SDF group of Schindleria, which can be distinguished from all members of the LDF group by a combination of following characters: (i) the dorsal fin about the same or nearly the same length of the anal fin (vs.dorsal fin distinctly longer than anal fin), (ii) a relatively short (5.8 % of SL vs. 8.7% of SL) and deep (2.2% of SL vs. 1.5% of SL) caudal peduncle, (iii) a straight (vs.flexed) urostyle, fewer procurrent rays (0-2 vs. 5-8), and absence of teeth in both jaws (vs.both jaws with teeth).

Coloration in life. Unknown.
Coloration preserved.The entire body, including the head, is uniformly whitish.The iris of the eye is black and capped dorsally with an iridescent silvery layer spotted with numerous melanophores (Fig. 3).The black pigment cap on the swim bladder is visible through the body wall (Fig. 2).The fins are translucent.

Discussion
The new species Schindleria qizma is characterized by a unique caudal complex with a modified urostyle.The tip of the urostyle is not flexed, nor is it tightly attached to the anterior, upper margin of the hypural plate, as is characteristic for Schindleria (e.g., Johnson and Brothers 1993;Ahnelt and Sauberer 2018) but it is straight and deeply inserted into the cartilage of the hypural plate.Generally, the caudal complex of Schindleria is a unique propulsion system.It comprises modified preural vertebrae 2 and 3, an extremely elongate urostyle, a relatively large, triangular hypural plate, a system of modified muscles with an elongated pair on each side of the urostyle, and a caudal fin with segmented and partly branched principal caudal fin rays (Ahnelt and Sauberer 2018;Robitzch et al. 2022).
Despite overall progenesis in this genus, the advanced developmental stage of the caudal complex in S. qizma is outstanding.Possibly the straight urostyle is the result of the reduction of notochord flexion and may represent a derived state and an apomorphy for S. qizma among the species of Schindleria.
In general, the dentition of the genus Schindleria is variable (Ahnelt 2020).Five different dentition patterns are known from just nine nominally described species (as the dentition of S. elongata is not known in detail): (i) no teeth on upper and lower jaws in S. brevipinguis, S. edentata, and S. qizma (Watson and Walker 2004;Ahnelt et al. 2022; this study); (ii) minute teeth on the upper jaw but no teeth on the lower jaw in S. parva (Abu El-Regal et al. 2022); (iii) minute and densely positioned teeth along the entire length of the premaxilla, but only anteriorly positioned teeth on the dentary close to the symphysis in S. nigropunctata, S. pietschmanni, and S. praematura (Johnson and Brothers, 1993;Fricke and Abu El-Regal 2017a;Ahnelt 2019); (iv) minute and densely positioned teeth along the entire length of the premaxilla and along the dentary up to its coronoid process in S. multidentata (Ahnelt 2021); and (v) few, very large, and widely spaced teeth on both jaws in S. macrodentata (Ahnelt and Sauberer 2018).It is yet unclear how and on what these tiny fishes are feeding and the functional relevance of the various dentition patterns of Schindleria remains unknown (Ahnelt 2020).Nevertheless, specimens of Schindleria are active feeders, as all investigated specimens have had guts full with amorphous, unidentifiable material (authors' personal observations during numerous collections), similar to the anguilliform leptocephalus larvae, which feed on "marine snow" or particulate organic matter (POM) (Tsukamoto and Miller, 2020, see Fig. 5c, d).
The mode of reproduction in Schindleria is also unknown.Some authors assume a demersal egg deposition (Watson and Leis 1974;Whittle 2003;Thacker and Grier 2005), but documentation of Schindleria among benthic and environmental studies is very rare (Robitzch et al. 2022) and evidence of such a spawning strategy is missing (Whittle 2003;Thacker and Grier 2005).Addi-tionally, adult and juvenile specimens were collected far offshore, some between 200-360 km distance from the next shoreline (Ahnelt and Sauberer 2020).Nonetheless, data show that the total egg number and egg size differs distinctly among species of Schindleria, comprising ~200 eggs (0.4% of SL) in S. macrodentata, ~90 (1% -1.1% of SL) in S. multidentata, ~50-60 (1.3% -1.8% in SL) in S. nigropunctata, S. parva, S. pietschmanni, and S. praematura, and ~11 (2.5% -5% of SL) in S. brevipinguis and S. qizma.These differences in egg numbers and sizes suggest differences in spawning strategies.Some species of Schindleria reproduce multiple times as more than one size class of eggs have been found in the ovaries of S. pietschmanni and S. praematura (Schindler 1930(Schindler , 1931;;Whittle 2003;Thacker and Grier 2005).
Generally, reproductive isolation is often accompanied by genital diversity (Langerhans et al. 2016).For males of Schindleria a high diversity in the shapes of the urogenital papillae hs been documented.Kon et al. (2007) describe 10 different morphotypes of such papillae.Seemingly less variable are the urogenital papillae of female Schindleria (e.g., Robitzch et al. 2021a).Just two general types have so far been reported: (i) a plain urogenital opening (Ahnelt and Sauberer 2018;Ahnelt 2020) and (ii) a roundish, bulbous papilla with two short horn-like projections lateral to the urogenital opening (e.g., Bruun 1940;Sardou 1974;Johnson and Borthers 1993;Ahnelt 2019) (Fig. 7C).A third and very conspicuous type of urogenital papilla is now described for S. qizma.here, the urogenital opening of females is flanked by two long, flat, and bifurcated projections (Fig. 7A, B).
Although some recent studies investigated sexual dimorphism (Robitzch et al. 2021a), lunar migration cycles (Robitzch et al. 2021b), and swimming mode (Robitzch et al. 2022) of Schindleria, the entire lifecycle, habitat, and basic biology and ecology of these enigmatic fishes are virtually unknown and still need detailed exploration.Nonetheless, the collection in which this new species was found may allow for the inference of a few more details on the habitat or distribution of S. qizma.The specimens come from a year-long study and a collection of over 2000 Schindleria specimens, collected monthly using the same method at three different reef sites along a cross-shelf gradient during the same time period (Robitzch et al. 2021a).The collection sites included a reef at the shelf-edge, one mid-shelf reef, and one inshore reef.However, S. qizma could be found only at the mid-shelf reef and in very low numbers.The rest of the collection is thought to mainly be comprised of one to three LDF species (unpublished data).This mid-shelf reef is known to be particularly large (about 10 km long) and has some of the regionally lowest average current speeds, wave action and visibility at its sheltered side, where S. qizma has been collected (Robitzch and Berumen 2020).Altogether, the uniqueness of S. qizma and the parameters of its habitat may hold evidence of an extreme example of endemism, with a relatively narrow distribution range and the specialization to a very specific habitat within the Red Sea.