Introduction

During the last years, a series of studies on the ecology, faunistic, morphology, and taxonomy of Schindleria (infantfishes) have increased our current knowledge on this enigmatic gobiid genus (e.g. Ahnelt & Sauberer 2018, Robitzch et al. 2021a, b, Ahnelt et al. 2022). These tiny (10-23 mm TL) and extremely rapidly reproducing fishes (with up to nine generations per year; Kon et al. 2007) inhabit the entire tropical and sub-tropical Indo-Pacific, from Central and South America to East Africa and the Red Sea (Fig. 1). At its discovery, the first two described species, Schindleria praematura (Schindler, 1930) and S. pietschmanni (Schindler, 1931), were morphologically distinguished by a very conspicuous character in their dorsal and anal fins, where S. praematura featured a notably longer dorsal fin compared to its anal fin, while S. pietschmanni's dorsal and anal fins were approximately equal in length (Schindler 1930, 1931, 1932). Thus, subsequent studies started grouping new species of Schindleria in two species groups based on this character: the long dorsal fin type (LDF) as in S. praematura and the short dorsal fin type (SDF) as in S. pietschmanni (Ahnelt 2019). Virtually all reports of Schindleria across their Indo-Pacific distribution range resemble morphologically one of these two types (summarized in Ahnelt & Sauberer 2020). Nevertheless, the evolutionary history of this morphological trait is not known, nor whether these two fin types might have evolved convergently in allopatry multiple times.

Fig. 1.

Published records of Schindleria from 49 publications (black dots with numbers 1-49) and from the Dana Expedition 1928-1930 (black squares); for references and a detailed description of the Dana Expedition samples, see Ahnelt & Sauberer (2020). Type localities of all formally described species of Schindleria are encircled. These represent from west to east: S. edentata, S. elongata, and S. nigropunctata (black circle); S. parva and S. qizma (blue circle); S. macrodentata (light green circles); S. brevipinguis and S. nana sp. nov. (orange circle and red star for the latter); S. multidentata (pink circle); S. pietschmanni and S. praematura (red circle); and S. squirei (dark green circle). Map from Ahnelt & Sauberer (2020), modified.

More than 70 years after the first descriptions of the two Hawai'ian species of Schindleria, a third species, S. brevipinguis, was described from the Great Barrier Reef (Australia) close to Lizard Island. This species was morphologically clearly distinguishable from the two other species by a deeper body, toothless jaws, larger eyes, lower number of dorsal and anal fin rays, a non-pigmented swim bladder, and especially its much smaller size at maturity (< 10 mm TL) (Watson & Walker 2004). A further intriguing and distinctive character in the description of S. brevipinguis was the few but extremely large eggs of females. Among all described Schindleria species, females of the larger species S. nigropunctata, S. pietschmanni, S. praematura, and S. squirei have relatively numerous (in total 50-60) eggs of a size from 1.3-1.8% in SL, while the two smaller sized (< 11 mm SL) species, S. brevipinguis and S. qizma, have only a few (approx. 10) and distinctly large (2.5-5% of SL) eggs (Ahnelt et al. 2023).

Herein, we describe a new species of Schindleria of the LDF species group, two adult females and one juvenile, from Lizard Island (Queensland, Australia). This species is characterized by very small size, few and very large eggs, oral jaws with no or few teeth on the lower jaw, an inconspicuous urogenital papilla, de facto just a urogenital opening, and an unpigmented swim bladder.

Material and Methods

The three specimens of S. nana sp. nov. are deposited in the Australian Museum Sydney (AMS), Sydney, Australia, and are registered as AMS.I.23115-004 (holotype) and as AMS.I.23115-040 (paratypes). The sample was collected by J.M. Leis with a plankton tow at 6-10 m depth off of Lizard Island (Queensland, Australia), in the lagoon ‘Lizard Island Reef’, 14°41′ S, 145°27′ E (Fig. 2). The specimens were deposited at the Australian Museum, Sydney.

Based on three genetic studies in which Schindleria clustered within Gobiidae (Thacker 2009, Agorreta et al. 2013, Tornabene et al. 2018), we consider Schindleriidae a junior synonym of Gobiidae. We separate the species of Schindleria into two species groups, a long dorsal-fin type group (LDF) and a short dorsal-fin type group (SDF), as defined by Ahnelt (2019). The 12 formally described species of these two species groups are listed in Table 1.

Pictures of the specimens 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. Measurements were made with a stereo-microscope and a micrometer eyepiece to the nearest 0.1 mm by H. Ahnelt.

Abbreviations of collections: AMS – Australian Museum, Sydney, Australia; BMNH – Natural History Museum, London, UK; CAS – California Academy of Sciences, San Francisco, USA; NMW – Naturhistorisches Museum Wien, Vienna, Austria; SMF – Senckenberg Museum Frankfurt, Frankfurt, Germany; ZMUC – Statens Naturhistoriske Museum, Zoologisk Museum København, Kopenhagen, Denmark.

Comparative materials

Schindleria brevipinguis: Paratype (AMS.I.2632-003), 6.6 mm standard length (SL), Australia, Queensland, Carter Reef. Photographs of the holotype (AMS.I.23552-006).

Schindleria edentata: Holotype (BMNH 2007.5.20.1), 9.0 mm SL, Red Sea, Egypt, Hurghada, reef lagoon.

Schindleria elongata: Photographs of the holotype (SMF 35780) and paratype (SMF 35781).

Schindleria macrodentata: Holotype (ZMUC 77624), 16.5 mm SL, female, Molucca Sea, Indonesia, between Sulawesi and Halmahera, March 1929. Paratype (ZMUC 77617), 18.7 mm SL, female, Sulu Sea, Philippines, northwest of the northern tip of the Island Panaya.

Schindleria multidentata: Holotype (ZMUC P77177), 20.0 mm SL, female and paratype (ZMUC P771800), Society Islands, Tahiti, harbour of Papeete.

Fig. 2.

The sampling sites of Schindleria nana (red star) and Schindleria brevipinguis (red square), the two smallest Schindleria species of the Pacific Ocean. The sampling location, Lizard Island (black square), is off the north-eastern Australian coast. Available at  https://apps.gov.au/reef-monitoring/reefs.

Schindleria nigropunctata: Holotype (SMF 35956), 15.9 mm SL, female, Red Sea, Egypt, Magawish Island. Paratype (SMF 35957), male, 13.9 mm SL, same data as holotype.

Schindleria parva: Photograph of the holotype (SMF 38020), 11 mm SL, female, Red Sea, Shaara Public Beach, Jeddah, Saudi Arabia. Paratype (SMF 38021), 9 mm SL, male, same data as holotype.

Schindleria pietschmanni: 42 syntypes (NMW 99182), 15.1-17.0 mm SL, North West Hawaiian Islands, French Frigate Shoal.

Schindleria praematura: 49 syntypes (NMW 99183), 18.3-20.5 mm SL, North West Hawai'ian Islands, French Frigate Shoal.

Schindleria qizma: Holotype (NMW 99999), 10.6 mm SL, female, north Al Fahal reef, sheltered side, north-central Red Sea, Thuwal, Saudi Arabia. Paratypes (NMW 10000), 10.7 mm SL, female and NMW 100001, approx. 10.9 mm SL, female. Otherwise, the same data as the holotype.

Schindleria squirei: Holotype (NMW 100576), female, 19.2 mm SL, female, 20.7 mm SL, Southeast Pacific, Chile, Rapa Nui (Easter Island), Hanga Roa. Paratypes (NMW 100577); 19.2 mm SL, female, and 20.9 mm SL; one male, 17.2 mm SL. Otherwise, the same data as the holotype.

Results

Table 1.

Ratio of the depth of the hypural plate (HYP) to the length of the urostyle (UL) of adult Schindleria species of the ‘long dorsal fin type’ (n = 7) and of Schindleria species of the ‘short dorsal fin type’ (n = 3); latter are shaded in grey. Values for two species, S. elongata and S. parva, were not available.

Fig. 3.

Holotype of Schindleria nana, AMS.I.23115-004, female, 9.0 mm SL; Australia, Queensland, Lizard Island. an – anus, ug – urogenital opening. Black asterisk – position of first anal-fin ray, white asterisk – position of first dorsal-fin ray. Scale bar: 1 mm.

Fig. 4.

Paratypes of Schindleria nana, AMS.I.23115-040; A – female, 8.5 mm SL; B – juvenile, 6.8 mm SL; Australia, Queensland, Lizard Island. Scale bar: 1 mm.

Table 2.

Body proportions in % of standard length (SL) of Schindleria nana sp. n., holotype, AMS.I.23115-004, paratype, AMS.I.23115-040 in comparison with the other four small (< 11.5 mm SL, all SDF) species of Schindleria: S. brevipinguis (AMS.I.26323-003, male and AMS-I-23552-006, female), S. edentata (BMNH 2007.5.20.1), S. parva (SMF 38021), and S. qizma (NMW 100000, 100001). Data for S. parva were calculated from measurements by Abu El-Regal et al. (2021). Data for the holotype of S. brevipinguis were calculated from Watson & Walker (2004). Characters highlighted in light grey are different in S. nana sp. n. compared to all other species. Values highlighted in dark grey indicate additional differences between S. nana sp. n. and the sympatrically occurring S. brevipinguis.

continued.

Table 3.

Meristic information for Schindleria nana sp. n., holotype, AMS.I.23115-004, paratypes, AMS.I.23115-040 in comparison with the other four small (< 11.5 mm SL, all SDF) species of Schindleria: S. brevipinguis (AMS-I-23552-006), S. edentata (BMNH 2007.5.20.1), S. parva (SMF 38021), and S. qizma (NMW 100000, 100001).

Fig. 5.

A, B – Dentition of Schindleria nana, paratype (AMS.I.23115-040), 8.5 mm SL; C – right lower jaw of Schindleria sp. (S. pietschmanni or S. praematura), Hawai'i (CAS uncatalogued) in dorsomedial view; the teeth were lost during the staining process, only the bases for the teeth are visible. A – dorsal view of the head, B – ventral view of the head. Teeth on the right dentary are encircled; two isolated teeth on the left dentary are marked with arrows. Note continuous row of small, conical teeth along the entire ventral margin of the premaxilla. ang – anguloarticular, bt – bases for the teeth, den – dentary, mck – Meckel's cartilage, pmx – premaxilla. Scale bar: 0.2 mm.

Fig. 6.

Dentition of Schindleria nana, head, lateral view. A – Holotype (AMS.I.23115-004), 9.0 mm SL; B – Paratype (AMS.I.23115-040), 8.5 mm SL. A – no teeth on the dentary, tiny conical teeth on the premaxilla. B – two isolated teeth on dentary (arrows); maxillary out of position, broken, and distorted. Conical and densely set teeth along the entire ventral margin of the premaxilla. a – anterior, ang – anguloarticular, den – dentary, mx – maxillary, pmx – premaxillary. Scale bar: 0.5 mm.

Discussion

The relative position of the dorsal fin to the anal fin is a reliable character to group species of Schindleria and has resulted in two groupings: the SDF species group and the LDF species group (Ahnelt 2019). Although adult specimens can generally unambiguously be assigned to one of these two groups, the assignment is less evident in juvenile LDF species because juveniles have fewer dorsal fin rays than adults (see Fig. 177D in Watson 2000, Fig. 1 in Ozawa & Matsui 1979). This ontogenetic difference in fin ray number is characteristic of teleost fishes because the dorsal fin rays appear sequentially in a bidirectional pattern during larval development (e.g. Mabee et al. 2002, Ott et al. 2012, Figs. 2, 6 in Koch et al. 2022). This difference is also true among gobiid fishes (e.g. Daoulas et al. 1993, Figs. 2, 3 in Strydom & Neira 2006, González-Navarro et al. 2021), where late larvae have more fin rays developed than earlier larval stages of the same species. Schindleria species are extremely progenetic (Johnson & Brothers 1993) and do not develop beyond a larval stage (Kon & Yoshino 2002, Kon et al. 2007). Generally, the first anal fin ray is positioned below the dorsal fin ray eight to eleven in LDF species such as S. macrodentata, S. multidentata, S. nigropunctata, S. praematura, or S. squirei (Ahnelt & Sauberer 2018, Ahnelt 2019, 2020, Robitzch et al. 2024) and below the dorsal fin ray one to four in SDF species such as S. brevipinguis, S. parva, S. pietschmanni, or S. qizma (Schindler 1932, Watson & Walker 2004, Abu El-Regal et al. 2021). In the new species, S. nana, the only known small-sized (< 11 mm SL) LDF species, the first anal fin ray is positioned below the dorsal fin ray six. This is not as distinctly far anterior as in the larger (> 15 mm SL) adult LDF species and could be related to an even faster progenic development in S. nana sp. n., where specimens reach maturity at an earlier larval stage than larger LDF species.

Table 4.

The species of Schindleria grouped in typical ‘large’ species (> 15 mm SL), and very small (‘dwarf’) species (< 11 mm SL). Additionally, the number of ovaries (from S. edentata, no females are known), the size of the eggs and the origin of the type localities (for details, see Fig. 1) are given. The five ‘dwarf’ species are shaded in grey. No data concerning the ovaries and the size and number of the eggs are available from the twelfth species, S. elongata (Red Sea); therefore, this species is not considered in this Table.

Fig. 7.

A, B – ventral view of the abdomen of A) the holotype of Schindleria nana, AMS.I.23115-004, 9.0 mm SL, four eggs (photo Oliver Macek and Harald Ahnelt) and of B) the holotype of Schindleria brevipinguis, AMS.I.23552-006, 8.4 mm SL, 10 eggs (photo Anthony Miskiewicz, Australian Museum) to show the single rows of few and large eggs. a – anterior, asterisks – squeezed and/or distorted eggs, white arrowheads point to anus, black arrowheads point to urogenital opening. Scale bar: 0.5 mm.

Another character which allows the differentiation of Schindleria species is the dentition of the oral jaws, which is also hypothesized to be related to size (Ahnelt et al. 2022). In many gobiid fishes, teeth first appear in a larval stage of 4-9 mm TL (e.g. Kondo et al. 2012, Zanella et al. 2017, Hwang et al. 2018). Watson (2000) found teeth in Schindleria sp. larvae at a size of 4.2-4.5 mm SL, and Watson & Walker (2004) in S. pietschmanni larvae of 4.5-5 mm SL, with teeth first forming on the premaxilla and subsequently on the dentary. The large Schindleria species S. macrodentata, S. multidentata, S. praematura, S. nigropunctata, S. pietschmanni, and S. squirei have teeth on both oral jaws (Schindler 1930, Fricke & Abu El-Regal 2017, Ahnelt & Sauberer 2018, Ahnelt 2020, Robitzch et al. 2024). The smaller species (< 11 mm SL) S. brevipinguis, S. edentata, and S. qizma are characterized by the lack of teeth on the oral jaws (Watson & Walker 2004, Ahnelt et al. 2022, 2023) or by teeth only on the premaxilla and no teeth on the dentary as is the case for S. parva (Abu El-Regal et al. 2021). Ahnelt et al. (2022) discussed the possibility that the toothlessness of S. brevipinguis, S. edentata, and S. qizma and the lack of teeth on the dentary of S. parva could be the result of a more truncated development of these small species (< 11 mm SL) compared to the larger Schindleria species (> 15 mm SL). The few teeth on the lower jaw and their asymmetric position, or the overall lack of teeth in S. nana sp. n., a species of only 10 mm SL, supports this hypothesis. Seemingly, S. nana sp. n. reaches maturity during and prior to the full development of dentition, which is hence completed for the premaxilla but not for the dentary. This pattern also aligns with the observation by Watson & Walker (2004), where the formation of teeth (in S. pietschmanni) starts earlier in development on the premaxilla than on the dentary. This chronological appearance of the first teeth on the oral jaws is also known from other gobioids such as Bathygobius soparator Valenciennes, 1837 (Peters 1983) and Tridentiger obscurus Temminck & Schlegel, 1845 (Hwang et al. 2018), but it is reverse in some percomorphs such as Porichthys notatus Girard, 1854 (Vaz & Hilton 2022) or Sander lucioperca Linnaeus, 1758 (Löffler et al. 2008).

Fig. 8.

The holotypes of the four small Schindleria species (< 11.1 mm SL). A – S. parva, SMF 38020, 11.0 mm SL; B – S. nana, AMS.I.23115-004, 9.0 mm SL; C – S. qizma, NMW 99999, 10.6 mm SL; D – S. brevipinguis, AMS.I.23552-006, 8.4 mm SL. Note the high total number of small eggs (approx. 60) of S. parva and the low total number of large eggs (approx. 4-12) of the other three species. Scale bar: 1 mm.

Another interesting morphological character of Schindleria is the relation between the depth of the hypural plate and the length of the urostyle. The urostyle is extremely elongated (Johnson & Brothers 1993) in Schindleria and plays a crucial role in swimming behaviour (Robitzch et al. 2022). Hence, we compared the relation of the depth of the hypural plate and the length of the urostyle of ten of the twelve described species and concluded that the hypural plate is distinctly less deep in the large species compared to the small species, regardless of whether they belonged to the LDF or the SDF species group (Table 1). Except for S. nana sp. n., the other three small species have less elongated but deeper bodies than the large species and deeper caudal peduncles (e.g. Ahnelt 2020, Ahnelt et al. 2022, 2023) (Fig. 8). This is also characteristic for S. edentata, the fifth small Schindleria species described, based on a single male. These characters are linked to the swimming abilities of fishes (Langerhans & Reznick 2010). Occurrence in different habitats often results in adaptive differences in fish species, particularly affecting locomotion (e.g. Walker 1997, McGuigan et al. 2003). Detailed habitat descriptions are missing for S. brevipinguis, S. edentata, S. nana sp. n., S. parva, and S. qizma, but seemingly all five small-sized species occur in calm waters of sheltered coastal lagoons (S. edentata, S. nana sp. n., S. parva) (Abu El-Regal et al. 2021, Ahnelt et al. 2022, present study) or in especially sheltered sites of a coral reef (S. brevipinguis, S. qizma) (Watson & Walker 2004, Ahnelt et al. 2023).

Yet an enigma, is the spawning strategy and the mode of reproduction in Schindleria. Although some authors assume a demersal egg deposition (Watson & Leis 1974, Whittle 2003, Thacker & Grier 2005), offshore records of up to 360 km distance to the next shore (Ahnelt & Sauberer 2020) may indicate that at least some species could be pelagic spawners. High diversity in the shape of urogenital papillae (Kon et al. 2007, Ahnelt et al. 2023) and in the size and number of eggs (Ahnelt & Sauberer 2018, Ahnelt et al. 2023) in Schindleria can be further indicative of differences in spawning strategies. Kon et al. (2007) described ten different types of male urogenital papillae. Among females, three morphotypes of urogenital papillae are known, i) two long, flat, and flexible bifurcated projections flanking the urogenital opening (Ahnelt et al. 2023), ii) a roundish and bulbous papilla with two short horn-like projections (e.g. Bruun 1940, Sardou 1974, Ahnelt 2019), and iii) a plain urogenital opening (Ahnelt & Sauberer 2018, Ahnelt 2020, this study). The most common urogenital papilla morphotype among female Schindleria across the Indo-Pacific is a bulbous-like opening with two horn-like projections (Bruun 1940, Sardou 1974, Ahnelt & Sauberer 2020). Furthermore, in the ovaries of some large species (i.e. S. pietschmanni and S. praematura), more than one size class of eggs have been found in the same specimen (Jones & Kumaran 1964, Whittle 2003, Thacker & Grier 2005), indicating that these species are capable of reproducing multiple times. On the other hand, in small-sized species with few but large eggs (S. brevipinguis, S. nana sp. n., and S. qizma), only one size class of eggs has been found (Ahnelt et al. 2023, this study), which may hint towards a shorter lifespan in these species, with only a single spawning event, and/or at least the production of only a single, very small egg clutch.

Like in most teleost fishes, the ovaries of female gobioid fishes are paired and of about equal size (Thacker & Grier 2005). However, a shift from paired ovaries to eggs in a single, unpaired ovary, as in some very small-sized Schindleria species, is not likely linked to their small size. Similar to the larger Schindleria species, the very small S. parva has paired ovaries and relatively small eggs (1.0-1.8% of SL). In contrast, the eggs of S. nana are about twice the size (3.4-3.9% of SL) of those found in S. parva and are arranged in a single, unpaired ovary (Table 4). Therefore, we conclude that the distinctly increased egg size likely induced the shift from paired-ovary eggs to a single-ovary egg row in Schindleria.

The high diversity in the shape of urogenital papillae and the size and number of eggs suggest reproductive isolation (Langerhans et al. 2016). Based on two genetic studies, Kon et al. (2007, 2011) identified 25 genetic species-level lineages from the Ryukyu and Ogasawara Islands (Japan) and Palau (Western Pacific). Many of these lineages were restricted to single islands, and because of the short lifespan and extremely short generation times of Schindleria (Kon & Yoshino 2002), high levels of endemism were proposed (Kon et al. 2011).

Diversity in egg size and the shape of urogenital papillae could result in reproductive isolation and favour a high level of endemism. Interestingly, nine of twelve to date known and formally described Schindleria species occur sympatrically at least with one other species: S. praematura and S. pietschmanni at Hawai'i, S. elongata, S. nigropunctata and S. edentata in the northern Red Sea, S. parva and S. qizma from the Central Red Sea near Jedda and S. brevipinguis and S. nana sp. n. from Lizard Island-Carter Reef from Queensland, Australia (Fig. 1); and the species-pairs are comprised of an LDF and SDF species. Considering the vast distribution range of Schindleria, there may be hundreds of undescribed species within this unique genus.