Acyrtus simon Gasparini & Pinheiro, 2022

Quintão, Thais L., Gasparini, João Luiz, Joyeux, Jean-Christophe, Rocha, Luiz A. & Pinheiro, Hudson T., 2022, Recent dispersal and diversification within the clingfish genus Acyrtus (Actinopterygii: Gobiesocidae), with the description of a new western Atlantic species, Neotropical Ichthyology (e 210137) 20 (3), pp. 1-22 : 5-15

Acyrtus simon Gasparini & Pinheiro , new species urn:lsid:zoobank.org:act:242B5ECF-E791-41DD-92E3-0BC8BA496910

( Fig. 1 ; Tab. 1)

Arcos sp. —Gasparini, Floeter, 2001:1646 [Trindade Island]. —Pereira-Filho et al., 2011:204 [Trindade Island]. —Simon et al., 2013:2123 [Trindade Island].

Acyrtus sp. —Macieira et al., 2015:390 [Trindade Island]. —Pinheiro et al., 2015:5 [Trindade Island]. —Pinheiro et al., 2017:83 [Trindade Island]. —Pinheiro et al., 2018:86 (Supplementary material) [Trindade Island]. —Guabiroba et al., 2020:701 [Martin Vaz Archipelago].

Acyrtus sp. nov. —Gasparini, 2017:78 [Trindade Island].

Holotype. CIUFES 2915, 26.41 mm SL, Brazil, Trindade Island , Calheta, 28 Jun

2009, H. T. Pinheiro & J. L. Gasparini ( Fig. 1 ).

Paratypes. CAS-ICH 247280, 1, 22.21 mm SL; CIUFES 2914 , 1 , 26.00 mm SL ; CIUFES 4448 , 1 (dissected specimen), 32.23 mm SL ; MNRJ 52794 , 1 , 24.71 mm SL ; MZUSP 125855 , 2 , 21.81–25.44 mm SL ; NPM 6839 , 1 , 25.79 mm SL ; ZUEC 17336 , 1 , 30.60 mm SL, same data as for the holotype .

Diagnosis. Acyrtus simon differs from A. artius by having a deeper head depth (19– 21% vs. 14–18% SL), a larger pelvic disc (36–39% vs. 29–36% SL), larger eye diameter (32–40% vs. 24–31% HL), and number of pectoral-fin rays (21–23 vs. 24–27) ( Tabs. 1–2). Acyrtus simon can be distinguished from A. lanthanum by a deeper head depth (19–21% vs. 15–18% SL), larger eye diameter (32–40% vs. 24–31% HL), and number of pectoral-fin rays (21–23 vs. 24–25) ( Tabs. 1–2). The new species differs from A. rubiginosus by a deeper head depth (19–21% vs. 13–16% SL), a larger pelvic disc (36– 39% vs. 27–31% SL), wider pelvic disc (30–36% vs. 22–30% SL), larger eye diameter (32–40% vs. 23–28% HL), and number of pectoral-fin rays (21–23 vs. 24–27) ( Tabs. 1–2). It differs from A. pauciradiatus by a larger pelvic disc (36–39% vs. 27–34% SL), shallower caudal peduncle (8–10% vs. 10–11% SL), longer caudal peduncle (10–17% vs. 5–8% SL), shorter anus–disc distance (6–12% vs. 12–13% SL), longer anus–anal fin distance (11–15% vs. 6–9% SL), longer snout length (20–33% vs. 9–15% HL), and narrower interorbital space (18–29% vs. 40–45% HL) ( Tabs. 1–2). Acyrtus simon also differs from Acyrtus arturo by having shorter anus–disk distance (6–12 vs. 13–18% SL), longer anus–anal fin distance (11–15 vs. 4–9% SL), and longer snout length (20–33 vs. 10–15% HL) ( Tabs. 1–2). It also differs from Arcos nudus [= Acyrtus nudus ] by having a different number of pectoral-fin rays (21–23 vs. 23–25) ( Tab. 1).

Description. Meristic and proportional measurements of the holotype and seven paratypes given in Tab. 1. Dorsal-fin rays 8 (8–9). Anal-fin rays 6 (6–8). Principal caudal-fin rays 5+5. Procurrent caudal-fin rays 6 (5–7) + 5 (5–7). Pectoral-fin rays 21 (21–23; one with 25). Pelvic-fin rays I,4 (I, 4). Vertebrae 12 (11–13) + 17 (16–18). Body moderately depressed anteriorly, depth 4.9 (4.7–5.3) in SL. Head depressed, head width 2.4 (2.4–3.0) and head length 2.9 (2.1–2.9) in SL. Snout steep with a rounded outline, 3.1 (3.3–4.9) in head length. Posterior nostril surrounded by low fleshy rim and situated in front of anterior edge of eye; anterior nostril tubular, with a bifurcated cirri extending from posterior margin. Mouth terminal, upper lip broad, much wider in front of snout than on the sides. Upper jaw with 2+2 incisiform teeth anteriorly, followed by a single row of 10 small coniform teeth. Lower jaw with 2+2 incisiform teeth anteriorly, followed by single row of 6 coniform teeth. Diameter of eye 2.5 (2.5–3.1) and interorbital space 4.1 (3.4–5.4) in HL. Adhesive disc length 2.7 (2.5–2.7) and width 2.9 (2.8–3.3) in SL; 8 (7–9) transverse rows of papillae across width of disc region A; 10 (9–12) transverse rows of papillae across width of disc region B; 5–5 (3–5) longitudinal rows of papillae across width of disc region C. Pectoral length 4.8 (5.2–6.1) in SL. Pre-dorsal distance 1.4 (1.4–1.5). Dorsal length 5.7 (4.7–6.9). Caudal peduncle length 7.7 (5.9–10.4) and depth 11.0 (10.1–12.3) in SL.

Color in alcohol. Body overall pale, with orange blotches and bands on the dorsal side and on the head; fins hyaline; pupils hyaline with black margin; orange blotches on the iris ( Fig. 1 ).

Coloration in life. Based on color photographs of live specimens ( Figs. 1–2 ): body with variable red and white bands covered by small red spots; white bands might present red blotches; bands wider anteriorly and narrowing towards the caudal fin; pupil rounded and black, with thin white margin; white and red stripes and bands

Head length 34–47 40–44 44–47 39–43 32–39 41–43 Head depth 19–21 18–2 14–18 15–18 13–16 19–27 Pelvic disc length 36–39 27–34 29–36 30–39 27–31 34–39 Pelvic disc width 30–36 32–36 29–34 31–38 22–30 31–32 Pre-dorsal distance 64–69 67–71 65–71 64–73 61–71 62–72 Pre-anal distance 70–75 69–76 67–78 71–77 66–80 70–76 Caudal Peduncle length 10–17 05–08 09–15 08–11 09–13 03–11 Caudal peduncle depth 08–10 10–11 07–10 09–14 07–09 07–09 Anus-Disk distance 06–12 12–13 08–15 04–08 12–14 13–18 Anus-anal fin distance 11–15 06–09 08–13 10–14 12–14 04–09

Proportion in head length

Snout length 20–33 09–15 20–27 22–30 26–32 10–15 Diameter eye 32–40 24–33 24–31 24–31 23–28 26–33

Interorbital 18–29 40–45 14–21 15–21 18–25 18–25

radiating outward from pupil across iris; iris also with thin white margin; first one-third of pectoral fin red, the posterior part hyaline; dorsal fin over red band red, and over white band hyaline with small red spots; caudal fin with variable white and red bands.

Geographical distribution and habitat. Acyrtus simon is only known from

Trindade Island, situated 1,160 km from the Brazilian coast. There are unconfirmed records for its presence in the Martin Vaz Archipelago (Guabiroba et al., 2020), which lies 40 km from Trindade. The species lives from intertidal habitat down to reefs 15

m depth ( Fig. 2A ). Acyrtus simon is commonly found taking shelter in cavities used by

Diadema antillarum during the day ( Fig. 2B ), often sharing the protection from predators offered by spines with the Vitória-Trindade Chain (VTC) endemic Hypleurochilus brasil

Pinheiro, Gasparini & Rangel, 2013, Apogon americanus Castelnau, 1855 and a number of others hosts.

Etymology. The specific name honors Thiony Emanuel Simon, our ichthyologist friend, who dedicated his career to study reef fishes, especially the fish biodiversity of the

Vitória-Trindade Chain. To be treated as a noun in apposition.

Popular name. Thiony’s clingfish; Peixe-ventosa de Thiony.

Conservation status. Acyrtus simon is endemic of Trindade Island. Endemic fishes from this island have not been assessed by the International Union for Conservation Nature (IUCN, 2021), with the exception of Scartella poiti Rangel, Gasparini & Guimarães, 2004 ; it is considered Vulnerable (VU) due the possibility of habitat degradation associated with its limited distributional range. The latest Brazilian Red List (Portaria MMA Nº 148, de 7 de junho de 2022) considers several Trindade Island endemic species as VU (i.e., Halichoeres rubrovirens Rocha, Pinheiro & Gasparini, 2010 , Malacoctenus brunoi Guimarães, Nunan & Gasparini, 2010 , Stegastes trindadensis Gasparini, Moura & Sazima, 1999 , and Sparisoma rocha Pinheiro, Gasparini & Sazima ,

2010, but not S. poiti nor Elacatinus pridisi Guimarães, Gasparini & Rocha, 2004 ), possibly for the same reasons, and in addition to the risks of fishing and ornamental trade. Therefore, Acyrtus simon is recommended to be categorized as VU according to the IUCN categories and criteria (IUCN Standards and Petitions Subcommittee, 2019).

Phylogenetic analyses of Acyrtus . COI sequences of 573 bp were obtained for

73 individuals of 20 species. Our analyses suggest the northwestern Atlantic as the center of the diversification of Acyrtus , and show that the genus is composed by at least nine species, forming a non-monophyletic group of three major clades ( Fig. 3 ). One clade is composed by Caribbean and Brazilian species, another clade by the Caribbean

A. rubiginosus lineage 1, A. rubiginosus lineage 2 and Arcos nudus , and a third solely composed by A. arturo , from the tropical eastern Pacific. Although three species ( A.

artius, A. lanthanum and A. rubiginosus ) present a high distributional overlap along most of the Caribbean, our analysis revealed two cryptic species supported by high values of posterior probability, Acyrtus aff. artius from Tobago Island, and Acyrtus aff. rubiginosus from Belize ( Fig. 3 ). Three species are endemic to the Brazilian Province and form a monophyletic group, which has Acyrtus aff. artius as the closest related species ( Fig.

3). Brazilian species present small distributions: Acyrtus simon is restricted to Trindade

Island, A. pauciradiatus , is restricted to Fernando de Noronha Archipelago and Rocas

Atoll, and the undescribed species ( Acyrtus sp. , Fig. 3 ) is only known from the Salvador region, on the northeastern Brazilian coast. In general, Caribbean species present higher interspecific divergence than Brazilian species ( Tab. 3).

The estimated date for the most recent common ancestor of the Atlantic species and A. arturo (eastern Atlantic) is at least 15 Mya, and the origin of Arcos nudus and the Acyrtus rubiginosus clade was among the oldest diversification events of the genus within the Atlantic ( Fig. 4 ; Tab. 4). Most of the diversification in Acyrtus is recent, occurring during the Pliocene and Pleistocene. The Brazilian clade is the youngest, diversifying around 2.55 Mya, and the divergence time between Acyrtus simon and Acyrtus sp. is around 1.7 Mya ( Fig. 4 ). Divergences were higher among Caribbean species than among Brazilian species.

Evolutionary history of Acyrtus simon . The close relationship between Acyrtus simon , from Trindade Island, and Acyrtus sp. from the Brazilian coast was also revealed in the haplotype network ( Fig. 5 ) and through smaller F ST values than Acyrtus pauciradiatus (Tab. 5). Acyrtus simon , represented by only three haplotypes ( Fig. 5 ), presented low haplotype and nucleotide diversity (Hd = 0.362; π = 0.001). Neutrality tests presented negative values ( Tab. 6), though the Skyline plot did not present evidence of recent population growth in Trindade Island ( Fig. 6 ) due to the low number of haplotypes.

3 0.362 0.145 0.00110 0.00048 -0.0063 -0.9481

Figures

FIGURE 1 | Acyrtus simon, holotype CIUFES 2915, 26.41 mm SL. A. Specimen alive, photo taken by J. L. Gasparini in June 2009; B–D. Specimen preserved, photo taken by R. M. Macieira on 31 October 2020. E. X-ray taken by M. M. Mincarone on 11 May 2022.

FIGURE 2 | Acyrtus simon in the natural environment at Trindade Island. A. Photos taken during a night dive by J. L. Gasparini; and B. During the day by J-C. Joyeux.

FIGURE 3 | Bayesian phylogeny of Acyrtus based on the COI gene. Bayesian posterior probability values are shown and the biogeographic province of lineages presented in the right. SWA: southwestern Atlantic; NWA: northwestern Atlantic; EP: eastern Pacific.

FIGURE 4 | Bayesian estimates of divergence time based on the mitochondrial COI gene. Posterior probability values reached 1–0.99 for all the main nodes (represented by the orange circle). The horizontal purple bars indicate 95% credibility intervals of node age estimation. The calibration nodes represent the divergence of the last common ancestors between (A) Pseudochromidae + Grammatidae + Gobiesocidae, (B) Grammatidae + Gobiesocidae, (F) all Gobiesocidae species, and (G) Acyrtus + Arcos + Gobiesox (see Conway et al., 2017).

FIGURE 5 | Haplotype network of Acyrtus artius and the representatives of Acyrtus in the southwestern Atlantic. FN = Fernando de Noronha.

FIGURE 6 | Bayesian skyline plot showing the effective population size fluctuation of Acyrtus simon through time (Mya) (black line: median estimation; purple: confidence interval).