Ameronothrus retweet Pfingstl and Shimano, 2022

Pfingstl, Tobias, Hiruta, Shimpei F., Bardel-Kahr, Iris, Obae, Yuito & Shimano, Satoshi, 2022, Another mite species discovered via social media - Ameronothrus retweet sp. nov. (Acari, Oribatida) from Japanese coasts, exhibiting an interesting sexual dimorphism, International Journal of Acarology 48, pp. 348-358 : 349-356

Ameronothrus retweet Pfingstl and Shimano sp. nov.

[New Japanese name: Iwado-hamabe-dani]

Type material/locality

Holotype: adult female (length 844 µm, width 444 µm); allotype: adult male (length 641 µm, width 363 µm), Japan, Honshu , Tottori prefecture, Tottori City; Fukube , Iwado , Iwado Rock Beach ; 31 March 2021, leg. OBAE Yuito. Preserved in ethanol and deposited at the Collection of Arachnida, Department of Zoology, National Museum of Nature and Science, Tokyo ( NMST) . Four paratypes (2 males, 2 females) from the same sample deposited in the collections of the Senckenberg Museum für Naturkunde Görlitz ( SMNG).

Etymology

The specific name ‘ retweet ’ is given as noun in apposition. “Retweet” is used as both a verb and noun on the social media application Twitter ( twitter Inc. ) and means repost or forward a message. The present work does not represent a direct act of retweeting in a strict sense, but the species was discovered by a post as a response to the message about the discovery of A. twitter .

Differential diagnosis

The colour is dark brown, nearly black. Body length is 641–859 µm. In centrodorsal notogastral cuticle with dense granulation, lateral parts are covered with larger granules. Prodorsal lamellar keels are converging. Short clavate sensilli are present. Interlamellar and exobothridial setae are absent. Labiogenal articulation is complete. One pair of adanal setae located posteriorly of anal orifice. Remarkable sexual dimorphism is present, females with strongly folded gastronotic integument and considerably shorter epimeral, genital, and aggenital setae. Male spermatopositor conspicuously elongated, female ovipositor very short. Primilateral setae pl on tarsus I are present. Dorsal companion seta d on genu I, II, and III and all tibiae are present. Tarsal distal setae end with a small nodule. Juveniles is unknown.

Description

Measurements. Females (N = 4), length: 813–859 μm (mean 844 μm) and width: 444–475 μm (mean 456 μm); males (N = 10), length: 641–719 μm (mean 698 μm) and width: 363–413 μm (mean 390 μm).

Integument. Cuticle was thin and easily deformable. Cerotegument shows overall dense granulation. The colour is dark brown, almost black in stereomicroscope.

Prodorsum ( Figures 1 (a,c)). Rostrum is rounded in dorsal view, demarcated from remainder of prodorsum by faint transverse caudally arched ridge ct. Pair of converging lamellar keels (cl), reaches slightly beyond insertion of lamellar seta (le). Area between lamellar keels shows several irregular smaller ridges. Rostral seta (ro) spiniform is long and smooth (52–63 µm). Lamellar seta (le) is short, thickened, blunt and smooth (approx. 16 µm). Interlamellar seta (in) and exobothridial seta (ex) are absent. Bothridium is cup-like, orifice wide, and circular. Sensillum (ss) is short (approx. 25 µm), strongly clavate, globular head (diameter ca. 17 µm) ( Figures 2 ).

Gnathosoma. Palp pentamerous 0-2-1-3-9 (solenidion not included), trochanter very short, femur by far longest segment, genu, tibia, and tarsus of almost equal length ( Figure 3 (a)). Solenidion ω on palptarsus is loosely associated with eupathidium acm, tips close to each other. Atelebasic rutellum: Distal part with wide and darker sclerotized external tooth followed by a smaller dark sclerotized tooth merging into a series of three lobe-like projections forming an undulating membranous edge ( Figure 3 (b)). Setae a (approx. 30µm) and m (approx. 23µm) is spiniform, robust, and smooth. Mentum regular, seta h is long, setiform, robust (approx. 46µm). Labiogenal articulation is complete. Chelicera chelate, mobile digit darker sclerotized; distinct strong interlocking teeth. Träghårdhs organ (tg) has slender blunt lamella, slightly upward orientated. Seta cha and chb is robust and barbed, approximately the same length (59–63 µm) ( Figure 3 (c)). Large porous area is present on chelicera.

Gastronotic region ( Figures 1 (a, c)). Oval and slender in dorsal view, slightly convex in lateral view; no distinct border between anterior median notogastral and prodorsal region, instead large U-shaped fold extending from posterior prodorsal area into anterior gastronotic region. Centrodorsal area with dense and fine granulation, lateral and posterior edges with conspicuously larger granulation. Fifteen pairs of slightly thickened and blunt notogastral setae (15–30µm), c 1-3, da, dm, dp, la, lm, lp, h 1-3,p 1-3; seta dp shortest and setae p 1 and h 1 longest.

Dimorphic characters: Males with domed even dorsal gastronotic plate show a weak arch-like deepening in the anterior part (best seen on Figure 2 ). Five pairs of notogastral lyrifissures are present but difficult to trace due to rough cuticular surface; ia between seta c 2 and c 3, but closer to the latter; im between seta lm and lp; ih laterad and anterior to h 3; lyrifissures ip and ips laterally of seta p 3 and p 2, respectively. Orifice of opisthonotal gland (gla) is posterior to lyrifissure im. Females with strongly folded gastronotic plate (especially in the centrodorsal area) are largely overhanging in humeral areas so that bothridia are more or less completely covered in dorsal view. Strong folding of integument lyrifissures and orifice of opisthonotal gland is not traceable in females.

Lateral aspect. Pedotectum I and II are absent. Discidium between acetabulum III and IV is developed as rounded ridge.

Podosoma and venter ( Figures 1 (b), 2(b)). Epimeral setation 3-1-2-2, all setae are setiform and smooth, seta 1b is conspicuously longer than others. Genital orifice is large, rectangular, anterior edges more rounded. Six pairs of spiniform genital setae arranged in longitudinal rows, first and last pair longest. One pair of setiform aggenital setae ag. Anal valves triangular but strongly rounded. Outer part of preanal organ is rectangular with rounded edges, inner part is shaped like a transverse bar. Two pairs of anal setae, an 1-2 (28–32µm) insert close to median border. Three pairs of adanal setae, ad 1-3 (39–42µm), ad 3-2 are located laterally and ad 1 posteriorly of anal orifice. Lyrifissure iad flanking anterior third of anal plates.

Dimorphic characters: Males with more even ventral plate show only faint ridges or folds. Epimeral, genital, and aggenital setae conspicuously are longer than in female. Epimeral setae 1a, 2a, 3a (8–13µm), 1b (ca. 63µm), 3b (ca. 47µm), 4a (31µm), 4b (45µm); genital setae (25–55µm) and aggenital seta (31µm). Females with strongly folded ventral plate (see Figure 2 ) and shorter epimeral, genital and aggenital setae. Setae 1a, 2a, 3a (8–10µm), 1b (ca. 26 µm), 3b and 4b (ca. 22µm), 4a (16µm); genital setae (19– 31µm) and aggenital seta (ca. 20µm).

Legs. Ambulacrum tridactylous, median claw broad and strong, lateral claws weaker developed and dorsally slightly dentate. Extensive brachytracheae with slit-like stigmata on dorsal paraxial face of all femora and tracheal sacculi ventrally on all tibiae and dorsally on trochanter III and IV. Dorsal companion setae d associated with solenidia on genu I, II, III, and all tibiae are present. Primilateral setae of tarsus I present. Tectal (tc) and iteral (it) setae as well as most other terminal tarsal setae are with spoon-shaped or nodular tips (difficult to observe) ( Figure 4 ). Famulus on tarsus I rod-like, blunt and next to solenidion ω 1, solenidion ω 2 shorter. Solenidia ω 1 and ω 2 on tarsus II adjacent. For Chaetome and solenidia, see Table 1 .

Dimorphic characters: Legs of females are shorter than their body width, while legs of males are considerably longer than body width and therefore males possess relatively longer legs than females.

Reproductive organs. Male spermatopositor elongated consisting of a proximal and a distal smooth tube, latter is fitted in the former when retracted. Distal part is three lobes containing darker sclerotized plates. Posterior lobe bearing setae εε and c, lateral lobes bearing setae ε 1, 1,a and b ( Figure 5 (a)). Female ovipositor, very short, tube-like structure strongly plicated, allowing strong increase of diameter. Three short terminal lobes are present, posterior lobe bearing setae εε and c, lateral lobes bearing setae ε 1, 1,a and b ( Figure 5 (b)), k setae is absent.

Remarks

The new species A. retweet sp. n. can be easily distinguished from all congeners by its conspicuous sexual dimorphism, with males showing a completely different notogastral surface structure. Apart from this dimorphism, A. retweet sp. n. differs distinctly from A. bilineatus , A. marinus and A. schneideri in the presence of a sensillum (vs. absence) and from A. nigrofemoratus by the presence of 3 claws (vs. 1 claw). Ameronothrus maculatus possesses only one pair of anal setae (instead of two in A. retweet sp. n.), A. lineatus lacks the dorsal setae on all tibiae (these are present in A. retweet sp. n.), and A. schusteri and A. schubarti show an incomplete labiogenal articulation (vs. complete). Ameronothrus lapponicus and the Russian A. dubinini , A. oblongus , and A. nidicola show different femoral surface patterns (either reticulate or smooth versus granular in A. retweet sp. n.), and the Japanese A. yoichi and A. twitter exhibit strongly nodular notogastral integuments (vs. granular and folded in A. retweet sp. n.). These are just the most important distinctive characters, a detailed comparison of diagnostic traits of all Ameronothrus species is given in Table 2 .

Genetic data

Mitochondrial COI as well as nuclear 18S rRNA sequence data ( Table 3 ) confirm all investigated dimorphic Ameronothrus specimens as a single distinct species and thus support their description as new species Ameronothrus retweet sp. n. A maximum likelihood tree and a Bayesian inference tree based on nuclear 18S rRNA produced identical topologies, whereas node support was higher in the latter and thus only this tree is shown ( Figure 6 ). All Ameronothrus species are closely related and form a monophyletic clade. Interestingly, the two A. maculatus specimens, one from the North Sea coast of Germany and the other from the coast of Portugal, are placed as separate taxa. Paraquanothrus grahami (GenBank synonym Aquanothrus sp. ) and Halozetes capensis , which are supposed by most authors as members of Ameronothridae , are placed in apparent paraphyletic positions ( Figure 6 ). Marine-associated Fortuyniidae and Selenoribatidae are given as monophyletic families representing sister groups in the phylogenetic tree.

Discussion

Systematics

Based on synapomorphic characters, Schubart (1975) classified the Ameronothrus species into four groups, (I) the A. marinus group ( A. marinus , A. bilineatus , A. schusteri , A. schubarti ), (II) the A. maculatus group ( A. maculatus , A. schneideri ), (III) the A. lineatus group ( A. lineatus , A. nigrofemoratus ) and (IV) the A. lapponicus group (monotypic). Similar to the other two recently discovered Japanese species, A. yoichi and A. twitter ( Pfingstl et al. 2019a, 2021a), the new species cannot be unequivocally assigned to one of these groups, because it diverges at least in one of the respective synapomorphic characters. In the A. marinus group, the solenidia on tarsus II are associated with the seta ft”, the tarsal setae (tc) and (it) show hook-like tips and the labiogenal articulation is incomplete and A. retweet sp. n. shows none of these traits. In the A. maculatus group the primilateral setae of tarsus I (pl) are absent, there is only one pair of anal setae, the ascleritic incision of notogaster is strongly reduced or lacking and the labiogenal articulation is complete. Ameronothrus retweet sp. n. shares the latter two characteristics but clearly differs in the former two. The A. lineatus group lacks dorsal setae on all tibiae, shows an incomplete labiogenal articulation, and possesses an elongated penis or spermatopositor, but apart from the long reproductive organ all these characters differ in A. retweet sp. n. Finally, the A. lapponicus group shares the complete labiogenal articulation with A. retweet sp. n. but diverges strongly in the morphology of pedipalp. Consequently, no clear classification is possible using Schubart’s (1975) synapomorphies. Nevertheless, the strongly elongated spermatopositor shared by A. retweet sp. n. and the A. lineatus group represents a rare and unique character indicating a closer relationship between these species. Moreover, the specific cuticular pattern of these three species is very similar, all possess granulated femora and a conspicuously folded gastronotic integument. Males of A. retweet sp. n. deviate from this pattern by lacking these folds, but males of A. lineatus and A. nigrofemoratus were also reported to show weaker developed gastronotic ridges or folds ( Schubart 1975), and although the sexual dimorphism of the latter two species is by far not as pronounced as in A. retweet sp. n., the reduction of the folded integument may be seen as another synapomorphic character. Moreover, males of A. lineatus and A. nigrofemoratus show relatively longer legs than females, i.e. the basically smaller males exhibit the same leg length than the larger females, and this kind of sexual dimorphism is also shown in A. retweet sp. n.

The Russian A. nidicola may represent a further close relative of the A. lineatus group as it shows a similar notogastral integumental structure ( Sitnikova 1977). However, A. nidicola is difficult to classify and problematic for various reasons: (1) the description of this species ( Sitnikova 1977) is incomplete, as it provides only a dorsal depiction and lacks details about important morphological features, such as the legs, mouthparts, and reproductive organs; (2) only female specimens are known yet in this species ( Sitnikova 1977; Klimov 1998) and therefore it is unknown if a distinct sexual dimorphism is present or not; and (3) A. nidicola should be distinguishable from A. retweet sp. n., A. lineatus , and A. nigrofemoratus by the smooth podosomal and femoral surface structure (vs. granular) and by an epimeral setation of 3-1-3-1 (vs. 3-1-2-2), but depictions or details of the ventral aspect and the femora are lacking and the epimeral formula could be based on an erroneous notation (numbers of setae are equal and if one of the setae on epimeron III is assigned to epimeron IV, there is no difference anymore). If further specimens of this species are found in the future, a detailed redescription and possibly molecular genetic data should be provided to clarify the systematic position of this species.

Generally, molecular genetic data of Ameronothrus species are scarce and thus a phylogenetic reconstruction based on these characters is not yet feasible. However, the present study included genetic data of at least the Japanese species and of A. maculatus , showing that all species are closely related and form a distinct monophyletic genus. Ameronothrus maculatus specimens are placed in different positions in the phylogenetic tree, indicating a high genetic divergence within this morphospecies. Cryptic diversity is a quite common phenomenon among marine associated oribatid mites (e.g. Pfingstl et al. 2021b) and this could also be the case here. The specimens were sampled from far distant locations at the North Sea coast of Germany and the Atlantic coast of Portugal (>2000 km) and due to this distance gene flow may have been restricted and resulted in strong genetic divergence. Future studies on Ameronothrus species from these areas should consider this possibility and thus include comprehensive molecular genetic data.

In a larger phylogenetic context, members of Ameronothridae are placed in paraphyletic positions whereas the Fortuyniidae and Selenoribatidae are given as sister taxa with a monophyletic origin. These results support the theory of an independent evolutionary origin of marine associated Ameronothroidea (e.g. Pfingstl 2017) and justify the family Podacaridae (with H. capensis ) as a distinct taxon outside Ameronothridae .

Sexual dimorphism

Only 1% of bisexual oribatid mites are distinctly sexually dimorphic and this dimorphism seems to be an evolutionary response to intermittent dryness or aquatic habitats ( Behan-Pelletier 2015). The intertidal environment clearly represents such an environment; therefore, it is not surprising to find sexually dimorphic species there. Nevertheless, only a minority of intertidal oribatid mites is known to exhibit an obvious sexual dimorphism. Males of the podacarid Halozetes belgicae (Michael, 1903) , Alaskozetes antarcticus (Michael, 1903) , and Podacarus auberti Grandjean, 1955 show aggenital neotrichy, whereas males of the latter additionally show epimeral neotrichy and larger claws (summarized in Behan-Pelletier 2015). Males of the fortuyniid Fortuynia yunkeri Hammen, 1963 possess modified tibiae on the fourth pair of legs, Fortuynia atlantica Krisper & Schuster, 2008 males exhibit modified anterior notogastral setae and lateral notogastral protuberances (summarized in Behan-Pelletier 2015), and male Fortuynia dimorpha Pfingstl, 2015 specimens show a large porous area on their posterior notogastral region ( Pfingstl 2015). Males of A. lineatus and A. nigrofemoratus show relatively longer legs ( Schubart 1975; Behan-Pelletier 2015), a morphological condition that is also shown in the new species. The specific function of these different sexually dimorphic structures is unknown for each species and consequently only a matter of conjecture. Pfingstl (2015) assumed that the modifications in Ameronothridae and Podacaridae allow a special mode of spermatophore deposition or transfer while the dimorphism of Fortuyniidae is supposed to be involved in some kind of mating behaviour. The long spermatopositor in connection with longer legs of A. retweet sp. n., A. lineatus and A. nigrofemoratus indeed indicates that these species may show different spermatophore deposition strategies. Moreover, we observed that the distal part of the extruded spermatopositor of preserved male A. retweet sp. n. specimens was always bent backwards at an almost right angle. A similar condition is shown in Collohmannia gigantea Sellnick, 1922 and Collohmannia johnstoni Norton & Sidorchuk, 2014 , where males deposit a nuptial fluid with their backwards bent spermatopositor on their fourth pair of leg, which is then presented to the female ( Schuster 1962; Norton and Sidorchuk 2014). However, if a nuptial gift is also presented in these Ameronothrus species can only be verified by observations of living specimens.

The strongly folded notogastral cuticule of female A. retweet sp. n. is a unique dimorphic character among marine associated oribatid mites and its function is also unknown. Considering the leathery and flexible nature of the cuticle in the genus Ameronothrus (e.g. Schubart 1975), it is assumable that females may increase their body volume considerably, so maybe they are able to either produce more eggs or larger eggs at a given time. However, among the A. retweet sp. n. specimens investigated here, there was not a single female carrying eggs or larvae and thus there is yet no indication supporting such an assumption.

Biogeographic aspects

Ameronothrus retweet sp. n. is the third species of Ameronothridae to be reported from Japanese landmasses. Ameronothrus yoichi is known to occur on the coasts of Hokkaido ( Pfingstl et al. 2019a), A. twitter was found at the Pacific coast of Honshu in a port east of Tokyo ( Pfingstl et al. 2021a) and A. retweet sp. n. was discovered at the Sea of Japan coast of Honshu. Indeed, the latter represents the recent and first record of an Ameronothrus from the Sea of Japan coast. Apart from that, no other record of any ameronothroid taxon is known yet from this coastline. Pfingstl et al. (2022) already mentioned the presence as “ Ameronothrus sp. ” from the latter coast near Tottori and this report referred to A. retweet sp. n. Moreover, Pfingstl et al. (2022) assumed that cold adapted Ameronothridae are not able to persist above a mean annual average air temperature of 17°C and a mean annual average of 20°C sea surface temperature and these temperatures are not exceeded in Tottori which confirms their assumption and classifies this presence as the most southern occurrence of an Ameronothrus species on this specific coastline. In this respect, the report of A. retweet sp. n. in this area may shed further light on the factors that determine the distribution of Ameronothroidea. However, north of this occurrence, the Sea of Japan coastline is still completely uncharted in terms of intertidal mites and thus a wider distribution of A. retweet sp. n. along this coastline should be considered. Further faunistic studies on Japanese shores are clearly needed to assess the real number of present taxa and their real distribution areas.

Figures

Figure 1. Ameronothrus retweet sp. n. adults.(a) Male,dorsal view,legs omitted. (b) Male, ventral view, distal leg segments and gnathosoma omitted.(c) Female,dorsal view, legs omitted. (d) Female, ventral view, distal leg segments and gnathosoma omitted.

Figure 2. Photographs of male (upper row) and female (lower row) Ameronothrus retweet sp. n. specimens in dorsal (left side) and ventral view (right side).

Figure 3. Ameronothrus retweet sp. n. mouthparts. (a) Right pedipalp, paraxial view. (b) Right rutellum ventral view. (c) Right chelicera, paraxial view.

Figure 4. Ameronothrus retweet sp. n. adult male left legs, antiaxial view. (a) Leg I. (b) Leg II. (c) Leg III. (d) Leg IV.

Figure 5. Ameronothrus retweet sp. n. reproductive organs. (a) Male, extruded spermatopositor in lateroposterior view. (b) Female, ovipositor, ventral view.

Figure 6. Bayesian inference tree of marine associated ameronothroid mites and selected terrestrial taxa based on 18S rRNA gene sequences. Bootstrap values (>50) and posterior probabilities (>0.9) are shown near nodes. Sequences generated in this study are marked by *, all others were taken from GenBank and are listed in Table 3. Abbreviations: PRT – Portugal, DEU – Germany.