Illacme tobini Marek, Shear & Krejca, 2016

Marek, Paul E., Krejca, Jean K. & Shear, William A., 2016, A new species of Illacme Cook & Loomis, 1928 from Sequoia National Park, California, with a world catalog of the Siphonorhinidae (Diplopoda, Siphonophorida), ZooKeys 626, pp. 1-43 : 7-17

Taxon classification Animalia Siphonophorida Siphonorhinidae

Illacme tobini Marek, Shear & Krejca, 2016 sp. n.

Material examined.

♂ holotype (Virginia Tech Insect Collection, VTEC catalog # MPE000735) from United States, California, Tulare County, Sequoia National Park, Lange Cave, a marble cave near intersection of Yucca and Cave Creeks, Elevation 1231 m, 9 October 2006, from within cave (Coll: J. Krejca). Exact coordinates withheld due to species rarity and habitat sensitivity.

Diagnosis.

Adult males of Illacme tobini sp. n. are distinct from Illacme plenipes , its sole congener, based on the combination of: Metazonites wider than prozonites with slightly enlarged paranota (Fig. 10A), not subequal in width as in Illacme plenipes (cf. Fig. 10B). Peritreme without the 2 large backwards projecting spines (Fig. 10C) as in Illacme plenipes (cf. Fig. 10D), ozopore ringed with ca. 15 setae. Ozopores nearer to margin, oriented dorsolaterally (Fig. 10A), not dorsally as in Illacme plenipes (cf. Fig. 10B). Metazonite posterior margin (limbus) lined with quadrate posteriorly projecting spines (Fig. 10E), not anchor-shaped as in Illacme plenipes (cf. Fig. 10F). Posterior margin sinuate, with anteriorly curved paramedial margins (Fig. 10A), not straight as in Illacme plenipes (cf. Fig. 10B). Telson densely covered with irregularly oriented and unevenly distributed stout spines on lateral surface only (Fig. 11A); telson not covered with stout spines on all surfaces and without posterior margin lined with posterodorsally oriented anchor-shaped spikes as in Illacme plenipes (cf. Fig. 11B). Hypoproct with two setae (Fig. 11A), not as in Illacme plenipes with> 2 seta present and arranged in a setal row (cf. Fig. 11B). Anterior gonopodal apex (podomere 7) spinose (Fig. 9C, E), with two-fold more spines than Illacme plenipes (cf. Fig. 9D, F). Anterior gonopodal podomere 3 with 2 long setae (Fig. 8E), not ringed with 6 setae, as in Illacme plenipes (cf. Fig. 8F). Posterior gonopodal apex (podomere 7) comprising a bundle of 4 styliform articles, with one article spike-shaped (Figs 11C, 12B), not bundle of 3 styliform articles as in Illacme plenipes (cf. Fig. 11D). The differential diagnosis of Illacme tobini sp. n. vs Illacme plenipes is summarized in Table 1, and a comparison of measurements between Illacme tobini sp. n. vs a male individual of Illacme plenipes (VTEC catalog # SPC000932) with an equivalent number of rings shown in Table 2.

Description of holotype

(♂) (Fig. 13). Counts and measurements: p = 106. a = 2. l = 414. (106 + 2 + T). BL = 19.73. HW = 0.34. HL = 0.39. ISW = 0.21. AW = 0.11. CW = 0.44. W1 = 0.52. L1 = 0.20. H1 = 0.31. AS1 = 0.43. A7W = 0.04. P7W = 0.03. Head pear-shaped, tapered anteriorly to round point at a 120° angle from antennal sockets; occiput gradually curved medially towards cervical area (Figs 2C, 5F, 13). Head covered with long, slender setae (Figs 2C, E, F; 3C, D). Gnathochilarium, labrum tightly appressed, tapered anteriorly to round point (Figs 2C, E, F; 3C, D, 6E, F). Mandibles not externally visible. Labrum with tooth-lined slit (Figs 6C, E, F; 7 A–F). Labrum at base of slit with deeply-incised tridentate projection (Fig. 7E). Labrum posterior to slit with ca. 200 unevenly distributed pores, some with unidentified secretion extruded from the opening (Fig. 7F). Denticulate shelf-like carina, projecting dorsally from labrum-epistome margin (Figs 6E, 7D, 8A). Gnathochilarium, mandible, head capsule noticeably separate at base (Fig. 2E, F). Mandibular stipes concealed, commissure between gnathochilarium, head capsule visible distally (Fig. 2E, F). Gnathochilarium thin, plate-like, occupying three-quarters ventral length of head. Gnathochilarium tightly appressed to the ventral surface of the head, leaving a small opening anteriorly between labrum, gnathochilarial stipes. Lateral opening apparent be tween gnathochilarium and head capsule (Figs 2C, E, F; 3C, D). Gnathochilarium with reduced sclerites: stipes, mentum, lamellae linguales present; cardines absent (Fig. 3D). Stipes of gnathochilarium with inner, outer palps (Figs 7C, D; 14B). Lamellae linguales with palps (Fig. 14B). Mandibles not externally visible, mandibular cardo base noticeable between head capsule, gnathochilarium (Figs 2E, 3D, 5E). Mandible with ca. 5 flabellate external teeth, pectinate lamella with numerous rows of jagged ventrally projecting serrulae, nested in groove of endochilarial frontal body (Figs 7 A–D; 14C). (Alternative description, primary homology with epipharynx: Epipharynx with distal flabellate side lobes, spiniferous keel with zipper construction. Mandibles, as in Illacme plenipes thin, stylet-like, with heavily calcified apices-not apparent externally, only visible at 400 × through translucent head capsule with phase-contrast imaging on a compound microscope). Mandible (or epipharyngeal) keel nested in groove of endochilarial frontal body. Endochilarium with V-shaped frontal body (Fig. 7C, D). Endochilarium with fringed lobes (Figs 7C, D; 14B). Endochilarial fringed lobes (spatulae sensu Silvestri, 1903) protruding distally through gnathochilarial stipes and lamellae linguales (Figs 7C, 14B). Antennae sub-geniculate, elbowed between antennomeres 3, 4, comprising 7 antennomeres (Fig. 3A). Antennomeres 5, 6 enlarged. Five sensillum types: 4 apical cones (AS) oriented in a trapezoidal cluster on 7th antennomere, with longitudinally grooved outer surface and circular pore apically (Fig. 15A). Chaetiform sensilla (CS) widely spaced on antennomeres 1-7, each sensillum with 2 or 3 barbules (Fig. 3A). Trichoid sensilla (TS) oriented apically encircling antennomeres 1-7, lacking barbules (Fig. 3A). Small basiconic sensilla (Bs2) in clusters of 3 and 4 oriented apical dorsally (retrolaterally) on antennomeres 5 and 6; smooth, capsule-shaped, 1/2 length of chaetiform sensillum (Figs 3A, 15A). Spiniform basiconic sensilla (Bs3) in cluster of 4, oriented apical dorsally on 7th antennomere; tips facing apical cones (on longitudinal axis with Bs2 on antennomeres 5, 6); each sensillum with 3-5 barbules (Fig. 15A). Antennae extend posteriorly to middle of 3rd tergite. Relative antennomere lengths 6>2>5>3>4>1>7. Collum not covering head, with straight cephalic edge, gradually tapering laterally (Figs 2A, C; 5E). Lateral margin of collum round, with thickened scaly carina (Figs 3D, 5E). Carina repeated serially on lateral tergal and pleural margins (absent from telson). Lateral tergal and pleural carinae jagged, pronounced on midbody segments (Fig. 15C, E). Metazonites wider than prozonites, with slightly enlarged paranota (Fig. 10A). Metazonites trapezoidal, anterior margin 3 × wider than long, posterior margin 3.5 × wider than long. Metazonites slightly convex (Figs 6A, 15E). Metazonite dorsally covered with long, slender setae (Figs 6A; 10A; 16A, C). Tergal setae hollow, cavity diameter at base 1/4 that of setae diameter; tipped with silk-like exudate, tangled, appearing adhered to neighboring setae (Figs 6A; 16A, C). Metazonite posterior margin (limbus) lined with quadrate posteriorly projecting spines, not anchor-shaped, with row of spines anterior to limbus on posterior rings only (Figs 10E; 15E; 16A, C, D). Limbal quadrate spikes uniform in size along margin. Ozopores oriented dorsolaterally, located near lateral metazonal margin, 1/4 length of metazonite anteriorly from limbus (Fig. 10A). Ozopores absent from collum, tergites 2-4, and telson. Ozopores elevated slightly on peritremata (porosteles absent), without 2 large backwards projecting spines, encircled with ca. 15 robust setae (Figs 10C; 16A, C, E). Without lunate-arranged stout flat tubercles encircling ozopore. Posterior tergites more convex, covered with a greater density of long, slender setae (Figs 11A, 15F, 16C). Apodous segment lacking sternum, pleurites contiguous in midline. Apodous tergite densely setose, without vestiture of spikes (Fig. 11A). Telson covered with irregularly oriented and unevenly distributed stout spines on lateral surface only; without posterodorsally oriented anchor-shaped spikes (Fig. 11A). Prozonite highly sculptured, with ca. 12 rows of discoidal flat tubercles; anterior 9 rows aligned and posterior 2 rows staggered (Figs 15E, 16D). Prozonal posterior discoidal tubercles button-shaped protuberant, anterior tubercles flush with surface. Pleurites quadrate, flat, with jagged scaly lateral, posterior and medial margins (Fig. 15C). Pleurite medial margin broad, with scaly carina (Figs 3E; 8C; 15C; 17A, C). Pleurites plate-like, left and right combined comprising four-fifths of ventral segment area. Pleural medial margins broadly overlapping sternite, covering spiracles (Fig. 3E, 4A, 15C). Anterior, posterior sternites free, separate from pleurites; heart-shaped, wider anteriorly (Figs 17E, F; 18A). Sternum with prominent midline triangular ridge projecting ventrally, with spiracles and legs oriented ventrally (Figs 3E; 4A; 15C; 17E, F; 18A). Spiracles circular, orifice open; oriented dorsal to legs (Figs 3E, 4A, 17E). Tergites, pleurites and sternites separated by arthrodial membrane (Figs 11A; 15C, F; 17A). Arthrodial membrane between tergites and pleurites wider posteriorly, pleated (likely permitting telescoping body rings). Telson covered with long slender posteriorly curved setae (Fig. 11A). Paraprocts semihemispherical, anterior margins slightly scaly (Fig. 11A). Hypoproct small, one-eighth area of paraproct, with two posterior projecting setae. Legs with six subequally shaped podomeres, with coxa slightly shorter and tarsus slightly longer. Legs with sparse setae, appearance similar to trichoid sensilla, with 2 or 3 barbules. Coxae nearly contiguous medially, separated by thin sternal ridge. Large posteroventral D-shaped opening for eversible sac (Figs 3E, 8C, 15C, 17C). Eversible sacs membranous, bulging slightly within aperture (Figs 3E, 17C). Tarsus with pincer-like claw; dorsal claw arcuate, ventral accessory seta thick, stout (Figs 2A, C, F; 6E, 17A). 2nd leg pair with posteriorly oriented coxal gonapophyses; rounded, protuberant, one-half length of prefemur (Fig. 18B). 9th, 10th leg pairs modified into gonopods, each comprising 7 podomeres (Figs 4C, E; 8C, E; 9A, C, E; 12A, B). Anterior gonopod robust, thicker than posterior gonopod (Figs 4C, 8E, 12A). Anterior gonopodal apex (podomere 7) shovel-shaped; in repose cupped around flagelliform posterior gonopodal apex (podomere 7, Figs 4C, E; 8E; 9A, C; 12A). Posterior gonopodal podomere 7 deeply divided, comprising a bundle of 4 stylus-shaped articles (Figs 4C, E; 5A, C; 8E; 9A, E; 12B; 18C, E, F; 19B, C). 3 dorsal-most, longest articles laminate distally, recurved laterally, denticulate posterior margins (Figs 5C, 12B). Ventral-most, 4th article acuminate distally, spike-like (Figs 4E, 12B). Thin ridge-shaped sterna present between left and right gonopods, thicker between anterior gonopods. Supplementary micrographs of Illacme tobini sp. n. are archived in the Dryad Data Repository at http://dx.doi.org/10.5061/dryad.tk0b8.

Female unknown.

Etymology.

This new species is named for Ben Tobin, Cave Specialist and Hydrologist at Grand Canyon National Park. Ben organized and carried out numerous cave surveys in the U.S., including the field visit that uncovered Illacme tobini sp. n., and has facilitated the discovery of many new species of invertebrates and other cave fauna in Sequoia National Park. The specific name is a genitive noun derived from his surname.

Variation.

Unknown. Illacme tobini sp. n. is known from a single male specimen (Fig. 13).

Habitat and distribution.

Illacme tobini sp. n. is only known from a single in-cave collection, within the upper foothills of the Giant Forest in Sequoia National Park (Fig. 1B). Lange Cave is situated at the base of Yucca Mountain at the boundary of the Sierra Nevada Forest and California Interior Chaparral and Woodlands ecoregions (Fig. 20). A region characterized by a Mediterranean climate with temperature and humidity extremes encompassing cold wet winters (<0 °C and 700 mm precipita tion) and hot dry summers (> 40 °C and <2 mm precipitation) ( Tobin et al. 2013). The cave is composed of Jurassic-Triassic marble of a white, coarsely crystalline, and schistose to gneissose composition ( Sisson and Moore 1994). The marble cave system is encompassed by biotite-feldspar-quartz schist rocks. The cave is ca. 90% surveyed, and has a total volume of 354.2 m3, average diameter of 2.1 m, wall area of 733.3 m2, and floor area of 124.6 m2. Inside the cave, temperatures range between ca. 6 °C in the winter months ( October–May) to ca. 9 °C in the summer months ( June–September). The woodland habitat around the cave was primarily composed of California live-oak ( Quercus agrifolia ), California bay ( Umbellularia californica ), Giant sequoia ( Sequoiadendron giganteum ), and Mountain maple ( Acer glabrum ). Understory flora included Scouringrush horsetail ( Equisetum hymale ), California wood fern ( Dryopteris arguta ), and Thimbleberry ( Rubus parviflorus ). Other organisms encountered in the habitat included millipedes- Parcipromus cooki , Californiulus yosemitensis , Taiyutyla loftinae , Amplaria muiri ; arachnids- Yorima sp., Ceratinops inflatus , Nesticus spp., Pimoa spp., Mundochthonius sp., Ortholasma colossus , Calicina sp.; hexapods- Tomocerus sp., Amoebaleria caesia , Heleomyza sp., Hippodamia convergens; and the salamander Ensatina eschscholtzii platensis.

Discussion.

Illacme species have extremely limited known geographic ranges. This feature suggests a formerly widespread, perhaps ancient, distribution, and/or membership in a larger hidden diversification in California encompassing many undiscovered taxa. Illacme individuals occur in the mesovoid shallow substratum (MSS), a cryptic ecosystem, which are miniscule subterranean microhabitats encompassing fissures and cracks below the soil surface ( Ortuño et al. 2013). These subterranean areas are the microcaverns (<1 mm) and mesocaverns (1 mm– 20 cm) described by Howarth (1983). The fauna of the MSS likely represents a considerable fraction of unknown biodiversity, yet the habitat is unexplored and its diversity poorly known. Species discovery from these microhabitats has only recently begun, and recent advances in collecting techniques are uncovering a considerable amount of new taxa. These microhabitats are fundamentally miniature caves and many MSS taxa also include cave-restricted species ( Espinasa et al. 2014). As a result, MSS organisms possess some troglomorphic features-e.g., lack of eyes, no pigment-but lack the open-space adaptations of cave animals, including long limbs and elongate sensory structures (e.g., antennae and setae). Frequently MSS taxa possess shorter legs than cave or epigean forms and a covering of thin, delicate setae on the exoskeleton ( Espinasa et al. 2014). Albeit anecdotally, Manton (1961, pg. 395) associated the hirsute covering of Siphonophora individuals as an adaptation for maneuverability, including spiraling within narrow crevices, and crawling upside-down on the ceilings of caverns; however, it is unclear precisely how this occurs biomechanically. Illacme plenipes individuals are found exclusively beneath large deep-set stones-a common place of discovery for MSS arthropods ( Marek et al. 2012). In contrast, Illacme tobini sp. n. was documented solely from a marble cave. Considering that Illacme plenipes individuals were found in the MSS, and that they possess MSS adaptations (including a vestiture of setae and absence of long sensory structures and limbs), the possibility that Illacme tobini sp. n.-with similar adaptations-is cave-restricted is uncertain. Additional material of Illacme tobini sp. n. would provide evidence to address this claim. Notwithstanding the paucity of material, the significance of the discovery highlights the importance of the Sequoia caves and MSS as a habitat of distinctive biodiversity.

The species Illacme tobini sp. n. and Illacme plenipes are the sole members of the genus and family in the Western Hemisphere. Shared morphological characters indicate the family is monophyletic, yet these features have not been considered within the context of a rigorous phylogenetic systematic framework. The features, including lack of a beak and absence of antennal pits, are broadly distributed across helminthomorph millipedes and are potentially shared ancestral traits and thereby do not indicate monophyly. The species Illacme tobini sp. n. is closely allied to Illacme plenipes based on unique shape of the head, consistency in appearance of mouthparts, similarly shaped gonopods, and possession of many legs. However, Illacme tobini sp. n. differs from Illacme plenipes in noteworthy characters such as the shape of metazonites, ornamentation of the ozopore, and chaetotaxy and number of articles of the posterior gonopods. The divergence in these traits, considering the usual divergence in morphology between siphonorhinid taxa, suggests generic differences. Our PCR possibly failed because specimen preservation in dilute ethanol degraded the DNA ( Vink et al. 2005). Pending discovery of additional individuals suitable for DNA sequencing, and phylogenetic analysis within the context of relatives in the Siphonorhinidae , a new generic designation may be justified.

Our knowledge of the cephalic morphology of the Colobognatha is limited due to their small size and derived anatomy, thereby making the generation of homology hypotheses difficult. In the current study, we revise the morphological assessment of the labrum, gnathochilarium, and mandibles. The labrum of Illacme tobini sp. n. is apically deeply divided into a slit. The dorsal margins of the slit are lined with sharp upwards-projecting spines. Moving posteriorly into the head, the labrum is further divided into a tridentate projection with additional upwards projecting spines. The remainder of the labrum posterior to the epistome is covered in a field of ca. 200 pores, half of which possess a secretion seemingly extruded from the pore openings (Fig. 7F). These labral features are not observed in other diplopods, and their homology and function is unclear. The pores appear deep and may open to the buccal cavity. The gnathochilarium of Illacme plenipes was described as "indistinguishably fused" ( Marek et al. 2012, pg. 89). However, we now think the gnathochilaria of both species are composed of a mentum and pair of stipes. Illacme tobini sp. n. has paired lamellae linguales each with a palp (Fig. 14B), but whether this feature is present in Illacme plenipes is unclear. The mandibles of Illacme tobini sp. n. lack sharp teeth distally (as in other Chilognatha) and possess finger-like rounded teeth. The mandibular pectinate lamella are composed of numerous rows of small jagged teeth that project ventrally and nest in a groove in the frontal body of the endochilarium. It is evident that these structures are the mandibles and not the epipharynx based on the articulated nature of the articles and separation between the mandibular gnathal lobe and base. In the description of Kleruchus olivaceus , Attems (1938, pg. 296, fig. 195) similarly illustrates the right mandible of the male holotype. In the drawing, the finger-like mandibular teeth and pectinate lamella are strikingly similar in appearance to the equivalent structures in Illacme tobini sp. n.

Based on examination of the mouthparts of Illacme and other siphonophoridan species, individuals consume liquid or gelatinous foods. In Siphonophorida (and most Colobognatha), the mouthparts are drawn into a cone with a small aperture distally. The mandibles are reduced and are not divided between the cardo, stipes and galea. A suctorial feeding mode has been suggested previously, and Manton (1961, pg. 386) indicated that species of Siphonophora possess a "suctorial fore-gut", proboscis, skeleto-muscular features, and head movement behaviors that strongly implicate suction feeding. Manton did not elaborate upon precise modifications of the foregut for suction, but filtration devices and muscular thickening are potential features to explore in the future. The presence of a coiled hindgut and elongation of the trunk (and thereby also the gut) for processing a nutrient poor diet are consistent with plant sap feeding ( Marek et al. 2012). Dissecting individual hindguts of Illacme plenipes suggested a liquid diet since gut contents were gelatinous and homogenous, and lacking particles completely. The mouthpart morphology of Illacme tobini sp. n. is peculiar and hypothetically represents a morphology adapted for consuming fungus as they are similar in gross anatomy with some sporophagous beetles ( Betz et al. 2003, Lipkow and Betz 2005, Yavorskaya et al. 2014). Specifically, Illacme tobini sp. n. possesses (1) mandibles with inner brush-like “bristle-trough” structures (Fig. 14C-mouthpart feature ii of Lipkow and Betz 2005) that hypothetically sweep in loose food material; (2) mandibles with outer lobes for manipulating dispersed food material and transporting it posteriorly (Figs 7 A–D, 14C-feature iii of Lipkow and Betz 2005); and (3) a flat crushing or grinding surface of the endochilarium (Fig. 7C, D-feature iv of Lipkow and Betz 2005).

While the mouthparts of the Siphonophorida are more derived in morphology and function relative to other helminthomorph millipedes, the gonopods are primitive due to their leg-like structure. In contrast with gonopods of eugnathan millipedes, many of which possess two leg podomeres (coxa and telopodite), colobognaths typically have a greater number of podomeres. Although Marek et al. (2012) counted six gonopodal podomeres in Illacme plenipes , we have reexamined Illacme plenipes males and found that they, as with Illacme tobini sp. n. males, have seven gonopodal podomeres, representing the primitive complement, including a seventh tarsungulum that is the terminal article. As in other colobognaths, the tarsungulum of the posterior gonopod is stylus-like, and the anterior tarsungulum spade-shaped with a deep groove. The groove of the anterior gonopod cups the stylus, which is often observed resting within the recess, and may act as a conductor allowing the posterior gonopod to slide into the cyphopods of the female during copulation. This process may be functionally analogous to the spider embolus (=posterior gonopod in millipedes) and conductor (=anterior gonopod in millipedes).

Several groups of dispersal-limited Californian animals show a distribution in which a Sierra Nevada clade is most closely related to a clade in the Coast Ranges. Examples of this spatial pattern occur in bioluminescent millipedes (genus Motyxia ), harvestmen (genus Calicina ), mygalomorph spiders ( Aliatypus californicus , Aliatypus erebus ), and several species of salamanders ( Batrachoseps attenuatus , Ensatina eschscholtzii , Aneides lugubris - Jockusch and Wake 2002, Martínez-Solano et al. 2007, Kuchta et al. 2009, Lapointe and Rissler 2005). Most studies that demonstrate this biogeographical pattern among taxa infer directionality of diversification from the Coast Ranges to the Sierra Nevada (reviewed in Emata and Hedin 2016). The phylogenetic studies of salamanders indicate a west-to-east pattern, relatively recent in the mid-late Pleistocene. In contrast, the studies of mygalomorphs and diplopods recover an east-to-west directionality of diversification ( Satler et al. 2011, Marek and Moore 2015). Several of these taxa (e.g., Calicina and Batrachoseps ) have occurred in California since the Eocene, with a “trans-valley” split occurring in the harvestman Calicina during mid-late Miocene ( Emata and Hedin 2016). Inferred dates for the east-west splits in other taxa are unknown.

Conservation.

Illacme tobini sp. n. is a short-range endemic restricted to the base of Yucca Mountain between the North and Marble forks of the Kaweah River in Sequoia National Park, California. The species is only known to occur in one small cave, though its range is likely to include the MSS. Management of this species should include careful consideration of activities that may impact the surface or subsurface. Actions that include vegetation changes, ground disturbance, or alteration of drainage patterns should be restricted in scope to preserve the soil and moisture of this river basin. The abundance and composition of MSS invertebrates in most global habitats remains uncertain, and further exploration and survey of these systems, thereby building knowledge of this fauna, will help to understand more fully biodiversity that is responsible for supporting healthy forests and ecosystem services.