Lacunicambarus chimera Glon & Thoma, 2019

Glon, Mael G., Thoma, Roger F., Daly, Marymegan & Freudenstein, John V., 2019, Lacunicambarus chimera: a new species of burrowing crayfish (Decapoda: Cambaridae) from Illinois, Indiana, Kentucky, and Tennessee, Zootaxa 4544 (4), pp. 451-478 : 462-474

Lacunicambarus chimera Glon & Thoma sp. nov.

( Figures 6 , 7 )

Cambarus obesus Forbes 1876:6 [in part].

Cambarus diogenes Hay 1895:478 [in part]. Ortmann 1905:123 [in part]. Rhoades 1944:111 [in part]. Eberly 1954:283 [in part]. Brown 1955:62 [in part]. Marlow 1960:229 [in part]. Page 1985:433 [in part]. Page & Mottesi 1995:23 [in part]. Taylor et al. 1996:29 [in part]. Simon 2001:104 [in part]. Taylor et al. 2007:382 [in part]. Taylor & Schuster 2004:80 [in part]. Taylor Schuster & Wylie 2015:66 [in part].

Cambarus diogenes diogenes Marlow 1960:233 [in part].

Cambarus (Lacunicambarus) diogenes diogenes Hobbs 1969:110 [in part]; 1974:20 [in part]. Bouchard 1972:56 [in part]; 1974:595 [in part].

Cambarus (Lacunicambarus) diogenes Hobbs 1989: 24 [in part]. Thoma et al. 2005:334 [in part]. Thoma & Armitage 2008:iii [in part].

Cambarus cf. diogenes Glon 2017:55 .

Lacunicambarus aff. diogenes Glon et al. 2018:604 [in part].

Diagnosis. Eyes pigmented, not reduced. Rostrum curved downwards in lateral view, margins converging, slightly thickened, without marginal spines or tubercles, lacking median carina, shallowly excavated. Acumen distinctly delimited basally by 45° angles. Cephalothorax cylindrical, with 3–10 (mean ± sd: 6 ± 1) small tubercles lining posterior margin of cervical groove. Anteroventral branchiostegal tubercles small, numbering 8–29 (mean ± sd: 18 ± 4). Suborbital angle acute. Postorbital ridges developed, lacking anterior spine or tubercle. Areola obliterated, constituting, in adults, 38–45% (mean ± sd: 42 ± 0 %) of entire length of cephalothorax. Antennal scale 2.41 to 3.35 (mean ± sd: 2.80 ± 0.18) times as long as wide, broadest distal to midlength, terminating in small spine, mesial margin forming straight edge. Dorsomesial margin of palm of chelae with 3 rows of tubercles, mesial-most row normally consisting of 6–10 (mean ± sd: 7 ± 1) probolos tubercles, running parallel to second row with 4–9 (mean ± sd: 6 ± 1) probolos tubercles, third row running diagonally from mesial base of palm to lateral dactyl articulation in the form of 5–8 (mean ± sd: 7 ± 1) subprobolos tubercles located in shallow dimples. No tufts of elongated setae at mesial base of fixed finger. Opposable margin of dactyl weakly concave at base. Ratio of dactyl length to palm length 1.78–2.49 (mean ± sd: 2.10 ± 0.16). Dorsomedian longitudinal ridges of dactyl and fixed finger of propodus weakly developed. Dorsolateral impression at base of propodus moderate. Ventral surface of chelae with 0–5 (mean ± sd: 2 ± 1) subpalmar tubercles. Mesial margin of dactyl with 12–33 (mean ± sd: 22 ± 4) prominent tubercles. Ventral surface of carpus with single spine on mesial articular rim, mesial margin with 4–10 (mean ± sd: 7 ± 1) spines of varying sizes. Merus spines numbering 2–9 (mean: 5 ± 2) on ventrolateral margin and 7–16 (mean ± sd: 11 ± 2) on ventromesial margin. Mesial ramus of uropod with distomedian spine not reaching caudal margin. Gonopods of Form I males contiguous at base, with moderately pronounced umbo near midlength of caudal surface; terminal elements consisting of 1) short, tapering, distally truncate central projection lacking subapical notch, shorter than mesial process, directed caudally at approximately 90°, reaching past margin of umbo, 2) mesial process with conical base tipped with protruding finger, directed caudally at approximately 90° and overreaching umbo by noticeable amount and 3) inconspicuous caudal knob sometimes present at caudolateral base of central projection. Hooks on ischium of third pereiopods only. Female with annulus ventralis subquadrangular or kiteshaped, approximately as long as wide, rather deeply embedded in sternum, flexible, with posterior half sclerotized and anterior half mildly pliable.

Holotypic male, Form I (OSUMC 10650; Figures 6 , 7A–D , G–J, L–M). Body subovate ( Figure 7J ), cephalothorax depth 95% of width ( Table 4). Abdomen narrower than cephalothorax (23.82 and 31.20 mm, respectively; Figure 6 ); maximum width of cephalothorax greater than depth at caudodorsal margin of cervical groove (31.20 and 29.73 mm, respectively). Areola obliterated; length 45% of total length of cephalothorax ( Figure 7J ). Rostrum curved downwards in lateral view from base to distal end, margins slightly thickened; acumen distinctly delimited basally by 45° angles, anterior tip upturned and not reaching ultimate podomere of antennular peduncle; upper surface of rostrum shallowly concave with minute punctations forming single row bordering margin. Subrostral ridge weak but evident in lateral aspect along entire length of rostrum. Postorbital ridges developed, grooved dorsolaterally, ending cephalically without spine or corneous tubercle. Suborbital angle acute; branchiostegal spine replaced by small spiniform tubercle. Posterior margin of cervical groove lined by 5 tubercles, single larger tubercle present in cervical groove. Branchiostegal region smooth. Anteroventral branchiostegal region with 14 small tubercles. Hepatic region with scattered small tubercles. Remainder of cephalothorax with slight punctations dorsal and laterally. Abdomen subequal in length to cephalothorax, 2.5 times as long as wide; pleura short, truncate, rounded caudoventrally. Cephalic section of telson with 2 spines in caudolateral corners, mesial spine moveable. Proximal segment of lateral ramus of uropod with 23 spines on distal margin, second most lateral spine distinctly longer than others; mesial ramus of uropod with prominent median rib ending distally as strong distomedian spine not reaching margin of ramus, laterodistal spine of ramus strong and curved mesially.

Cephalomedian lobe of epistome ( Figure 7I ) bell-shaped with uniform raised margins, lightly setate, ventral surface flat; main body of epistome with shallow fovea; epistomal zygoma mildly arched. Ventral surface of antennular peduncle’s proximal podomere with small spine at midlength. Antennal peduncle without spines; antennal scale 2.66 times as long as wide ( Figure 7L ), broadest distal to midlength, mesial margin straight from basal area to broadest distal point; distal antennal spine reduced, not reaching distal margin of penultimate podomore of antennal peduncle. Lateral half of ischium of third maxilliped densely studded with long, flexible setae; distolateral angle acute, spiniform.

Length of right chela ( Figure 7M ) 103% of cephalothorax length; chela width 44% of chela length; palm length 31% of chela length; dactyl length 2.11 times palm length. Dorsomesial margin of palm of chela with 3 rows of tubercles, mesial-most row composed of 8 tubercles running parallel to second row of 6 tubercles, third row running diagonally from mesial base of palm to lateral dactyl articulation comprised of 6 subprobolos tubercles located in shallow dimples, 4 distal tubercles between second and third (diagonal) row, dorsal, proximal dorsolateral half smooth, most distolateral area punctate, punctations moderately defined in vicinity of dorsolateral base of propodus; lateral margin of propodus not costate; ventromesial surface with small punctations, 2 bulbous tubercles on propodactyl articular rim; 5 subpalmar tubercles, 3 located proximally to ventral dactyl articulation, 2 located laterally to ventral dactyl articulation. Both fingers of chela with weakly developed dorsomedian longitudinal ridges. Opposable margin of propodus with row of 8 tubercles, decreasing in size except for third from base which is greatly enlarged over adjacent tubercles, ultimate tubercle with corneous tip, larger than penultimate tubercle, positioned ventrally relative to adjacent tubercles; single row of minute denticles extending distally from fifth tubercle. Opposable margin of dactyl with row of 8 tubercles approximately equal in size except for fourth from base which is enlarged over adjacent tubercles; single row of minute denticles extending distally from sixth tubercle; mesial surface of dactyl studded with 25 tubercles basally, not forming distinct rows, giving way to punctations distally. Dorsolateral impression at base of propodus moderate.

Cheliped carpus with distinct dorsal furrow; dorsomesial surface with row of 8 tubercles; dorsolateral surface with 11 punctations; mesial surface with row of 4 small spines plus 1 large procurved spine near distal margin, 3 spiniform tubercles triangularly arranged and located ventral to spines; ventral surface with spine on distal articular rim. Merus with 2 pre-marginal spines dorsally, ventrolateral margin with row of 6 spines, ventromesial margin with row of 13 spines, increasing in size from base ( Figure 7H ). Basioischial segment of first pereiopod with 4 small tubercles on ventral margin. Ischium of third pereiopod with simple hook extending proximally over basioischial articulation, not opposed by tubercles on basis ( Figure 7G ). Coxa of fourth pereiopod with setiferous, vertically disposed caudomesial boss, ventral surface calcified; coxa of fifth pereiopod lacking boss, ventral surface membranous.

Gonopods contiguous at base, reaching past caudomesial boss of fourth pereiopod; central projection ( Figure 7 B–D) short, tapering, lacking subapical notch, directed caudally at approximately 90°, shorter than mesial process, just overreaching umbo; mesial process conical at base, then tipped with protruding finger, directed caudally at approximately 90°, overreaching umbo; caudal knob inconspicuous but present at caudolateral base of central projection.

Sinistral gonopod, sinistral antennal scale, and sinistral second pleopod of specimen separated from specimen and placed in glass vials inside specimen jar. Dextral antenna missing from specimen. Two gills were extracted from sinistral gill chamber of specimen and preserved in 100% ethanol for future DNA extractions; one is frozen in the OSUMC crustacean collection (MGG 528) and the other was deposited as a tissue sample in the USNM biorepository (USNM 1480291).

Allotypic female (OSUMC 10652; Figure 7K ). The allotypic female differs from the holotype as follows: cephalothorax depth 106% of width ( Table 4). Abdomen wider than cephalothorax (31.91 and 30.91 mm, respectively); maximum width of cephalothorax less than depth at caudodorsal margin of cervical groove (30.90 and 32.65 mm, respectively). Areola length 41% of total length of cephalothorax. Posterior margin of cervical groove lined by 8 tubercles, lacking single larger tubercle in cervical groove. Anteroventral branchiostegal region with 23 small tubercles. Abdomen greater in length than cephalothorax, 2.01 times as long as wide. Cephalomedian lobe of epistome bell-shaped. Antennal scale 2.57 times as long as wide.

Length of right chela 88% of cephalothorax length; chela width 45% of chela length; palm length 29% of chela length; dactyl length 2.25 times palm length. Dorsomesial margin of palm of chela with 3 rows of tubercles, mesial-most row composed of 7 tubercles running parallel to second row of 7 tubercles, third row running diagonally from mesial base of palm to lateral dactyl articulation comprised of 6 subprobolos tubercles located in shallow dimples, 6 distal tubercles between second and third (diagonal) row. Opposable margin of propodus and dactyl both with rows of 11 tubercles; mesial surface of dactyl studded with 33 tubercles basally, not forming distinct rows, giving way to punctations distally. Mesial surface of cheliped carpus lacking tubercles but with 6 small spines plus 1 large procurved spine near distal margin. Merus ventrolateral margin with row of 7 spines, ventromesial margin with row of 12 spines.

Annulus ventralis ( Figure 7K ) kite shaped, 1.21 times wider than long, rather deeply embedded in U-shaped sternum, distal half sclerotized, proximal half mildly pliable, with leathery ridge mesially located in cephalic half, distal half of ridge bifurcated, ending in central fossa; tongue extending from sclerotized lingual (sinistral) wall into fossa disappearing under sclerotized supralingual (dextral) wall; lingual, supralingual walls approximately symmetrical, both curved on outer margin; sinus laterally oblong, forming deep fossa on dextral, sinistral sides. Distal margin of annulus ventralis projecting over oblong, approximately symmetrical post-annular sclerite, lacking setae. First pleopods overreach distal edge of annulus ventralis when abdomen flexed.

Morphotypic male, Form II (OSUMC 10651; Figure 7E–F ). The morphotypic Form II male differs from the holotype as follows: cephalothorax depth 101% of width ( Table 4); maximum width of cephalothorax less than depth at caudodorsal margin of cervical groove (23.41, 23.69 mm, respectively). Areola length 41% of total length of cephalothorax. Antennal scale 2.65 times as long as wide. Posterior margin of cervical groove lined by 7 tubercles, lacking single larger tubercle in cervical groove. Anteroventral branchiostegal region with 18 small tubercles. Abdomen greater in length than cephalothorax, 2.63 times as long as wide.

Length of right chela 74% cephalothorax length, chela width 51% of chela length; palm length 33% of chela length; dactyl length 1.91 times palm length. Dorsomesial margin of palm of chela with 3 rows of tubercles, mesial-most row composed of 8 tubercles running parallel to second row of 5 tubercles, 8 distal tubercles between second and third (diagonal) row. Opposable margin of propodus with row of 10 tubercles, opposable margin of dactyl with row of 12 tubercles. Mesial surface of cheliped carpus with 7 small spines plus 1 large procurved spine near distal margin, lacking tubercles. Merus ventrolateral margin with row of 6 spines, vendromesial margin with row of 12.

Central projection non-corneous and slightly shorter than mesial process, just overreaching umbo near midlength of cephalic surface of gonopod ( Figure 7 E–F). Mesial process conical, overreaching umbo near midlength of cephalic surface of gonopod, lacking protruding finger. Sinistral gonopod separated from specimen, placed in glass vial inside specimen jar.

Coloration and color pattern. We have observed a great deal of ontogenic variation in the coloration and color pattern of L. chimera . Adult specimens resemble the holotype ( Figure 6 ) in having the background of the cephalothorax predominantly olive, yellow green, or golden. The abdomen is similar in color to the cephalothorax, but usually a few shades darker. The proximal half of the uropod is similar in color to the abdomen, but transitions to a soft periwinkle color in the distal half. The chelae are mostly similar in color to the cephalothorax, with the exception of the lateral margins and the tips of the propodus and dactyl, which are apricot orange. The ventral side of the chelae is a similar shade of apricot orange. The proximal portions of the 1 st pereipods and the entirety of the 2 nd through 5 th pereiopods range from a light blue or white to a soft cream in color, as do the ventral sides of the cephalothorax and abdomen. The distal margins of the abdominal somites, telson, and rami, and the dorsal base of the dactyl are highlighted by a deep burgundy color, like that of Pinot Noir. The anterior tip of the postorbital ridge and the rostrum and acumen are highlighted either by this same burgundy color or, in some specimens, by an apricot orange similar to that of the distal portions of the chelae. Prominent tubercles and spines on the merus, carpus, and chelae range from an apricot to burnt orange. A faint longitudinal gladiate (i.e., sword-shaped) stripe highlighting the margins of the areola (i.e., handle), forming a diamond shape at the distal margin of the cephalothorax (i.e., hilt), then tapering and running down the abdomen (i.e., blade) is sometimes faintly present in adult specimens, in which case it is lighter in color to the cephalothorax and abdomen. This stripe is only faintly visible in the holotype.

The coloration of juvenile and young adult specimens is distinct from adults in several ways ( Figures 8 , 9 ). The gladiate stripe is much more pronounced in juvenile and young adult specimens and reminiscent of that seen in L. miltus ( Fitzpatrick 1978) . In these life stages, the stripe ranges from yellow green to orange. Young specimens exhibit mottling on the lateral sides of the cephalothorax and abdomen, of a color matching that of the gladiate stripe. This mottling gradually fades in young adult specimens, but the stripe remains visible in most, but not all, specimens up to a rather large size. The base color of the cephalothorax and abdomen of juveniles and young adults ranges from an olive green to a cider color. Lastly, the tips of dactyl and propodus are typically a red-orange color rather than the apricot color seen in adults.

Size. Lacunicambarus chimera is a sizable crayfish. The largest specimen we have measured is the allotypic female, which has a carapace length of 62.68 mm and a total body length of 129.32 mm from the anterior tip of the rostrum to posterior tip of the telson. The largest Form I male that we have measured is the holotype, which has a carapace length of 62.45 mm and a total body length of 121.95 mm. The smallest Form I male that we have measured has a carapace length of 38.90 mm and total body length of 79.05. The mean ± sd carapace lengths and total lengths of all Form I males that we have measured are 53.86 ± 6.01 mm and 106.52 ± 11.87, respectively. The large size of this species is reflected in the size of its burrows, which can have an inside diameter of 7–8 cm and chimneys as high as 30 cm.

Variation. Lacunicambarus chimera exhibits a moderate amount of variation across its range beyond the color variation mentioned above and normal ontogenic variation (i.e., juveniles having less developed features such as chelae sculpturing and tubercles). A small number of specimens from across the range have a complete row of tubercles consisting of as many as 6 tubercles, located ventrally and parallel to what is typically considered the 1 st row of tubercles on the mesial margin of the palm of the chela. Some specimens from Pike County, Indiana have a very rudimentary caudal knob at the caudolateral base of the central projection. The annulus ventralis of some specimens from across the range have small carinas that extend laterally in either direction in ventral view, giving the impression of small wings like those seen on aviator badges. We have occasionally encountered specimens with a single prominent tubercle or, occasionally, a spine, in the cervical groove. This spine or tubercle is far more conspicuous than the small tubercles that normally line the posterior margin of the cervical groove. Lastly, there is a great deal of variation in the overall shape of the rostrum and acumen, which can be spoon-shaped, subtrapezoidal, or lanceolate. The rostral margins are also quite variable and range from perfectly straight to slightly concave. As far as we can tell, none of this variation corresponds to sex, age, or geography.

Disposition of Types. The holotype, morphotype, and allotype have been deposited in the OSUMC (OSUMC 10650–10652). Paratypes have been deposited in the USNM (USNM 1480292–1480294).

Type Locality. We excavated the holotype and morphotype from burrows in a roadside ditch on the east side of Illinois Route 1 (Court Street) approximately 150 m north of the Illinois Route 1 intersection with County Rd 2450 N, 2.4 kilometers south of Grayville in White County, Illinois (38.23870° N, 87.99885° W). This ditch had been lined with large rocks, likely to prevent erosion, but still sustained a healthy population of L. chimera in burrows with characteristically large chimneys at the time of sampling in 2018. We dug the allotype from a burrow in a roadside ditch on the southeast corner of the intersection of Kentucky 109 and Press Road, approximately 2 km west of Sturgis in Union County, Kentucky (37.550308° N, 88.006743° W). This ditch was shallow and mostly surrounded by mown grass dotted with crayfish chimneys at the mouths of shallow burrows at the time of sampling in 2017.

Range. The majority of our collections of this species are from the Ohio River Basin in southern Indiana and Illinois and western Kentucky ( Figure 10 ). However, we have also collected L. chimera in the Lower Mississippi River and Tennessee River Basins in western Kentucky and Tennessee. Lastly, we have a single collection from the Upper Mississippi River Basin in Alexander County, Illinois. The range of this species, while bounded by the Mississippi River in the west, does not seem to correspond with any particular contemporary drainage basin. Likewise, this species’ range does not seem to correspond with any particular ecoregion, extending over parts of the Interior River Valleys and Hills, Interior Plateau, Southeastern Plains, and Mississippi Valley Loess Plains ( Wiken et al. 2011). This general range may suggest that this species is capable of dispersing via large streams and rivers like other species in this genus and is therefore not restricted by drainage basin boundaries ( Helms et al. 2013; Miller et al. 2014; Glon et al. 2018). Alternatively, this species’ contemporary range may be a remnant of a paleodrainage, as it corresponds well with the pre-Holocene Old Ohio River whose flow was altered as glaciers advanced southward during the Pleistocene (Strange & Burr 1987; Kozak et al. 2006).

Specimens Examined. We examined a total of 143 specimens from 24 counties in four states. See Table 1 for specific information on these specimens.

Conservation status. This species has a fairly large range and is common in appropriate habitat within that range. It seems fairly tolerant of anthropogenic habitat alterations, as evidenced by its success colonizing roadside ditches and artificial ponds. We suggest that it be considered Currently Stable following the American Fisheries Society’s Endangered Species Crayfish Subcommittee criteria ( Taylor et al. 2007) and of Least Concern following the IUCN criteria (IUCN 2001), but also recommend that potential threats specific to this and other burrowing species be explicitly examined.

Life History Notes. We did not explicitly focus on gathering life history data during this study, so our inferences may require revision after a more targeted life history study. Lacunicambarus chimera seems to follow the general life histories of the family Cambaridae and of other Lacunicambarus species ( Hobbs III 2001; Thoma et al. 2005; Miller et al. 2014; Figure 11 ). Specifically, our data suggest that most males are in Form I during winter and early spring, which coincides with mating. Some of these males then molt into Form II in late spring or early summer and remain in this Form throughout most of the summer. However, we also found several Form I males during the summer, perhaps because larger males grow more slowly and therefore molt less frequently than smaller conspecifics. It is unclear exactly when males molt back from Form II to Form I because we do not have data for September, October or November, but two Form II specimens that we captured in July 2018 and kept in aquaria molted to Form I in late August of the same year. We have limited sampling of females in fall and winter and therefore do not have any data on when they may be in glair; however, we examined ovigerous female specimens collected in March, suggesting that they had mated in fall or early winter. We found juvenile specimens from February to August, which further suggests that mating takes place in fall or winter, with eggs hatching in Spring.

We can only speculate about the lifespan of this species. Specimens we have kept in captivity do not seem to grow particularly fast relative to other species, suggesting that large specimens must be quite old. One of the authors (RFT) collected a gravid female of what we now recognize to be L. chimera from Gibson County, Indiana on March 23 rd, 2001. RFT raised the progeny that hatched from this female’s eggs in captivity. Most did not survive more than a few years, but a single individual survived in captivity until January 28 th, 2017, confirming that this species has a very high longevity potential, at least in captivity.

Ecological Notes. As mentioned above, L. chimera is a primary burrowing crayfish species. Like other Lacunicambarus species, L. chimera is commonly dug from burrows in fine-grained soils along the floodplains of streams and rivers and in roadside ditches. We have also collected this species in burrows on the banks of manmade ponds and in ditches that were lined with large stones. The chimneys at the mouths of L. chimera burrows are often large and conspicuous, attaining heights of 30 cm or more. These burrows, like those of other primary burrowing crayfishes, provide habitat for many other organisms (e.g., Creaser 1931; Pintor & Soluk 2006; Thoma & Armitage 2008). Glon & Thoma (2017) specifically documented the use of L. chimera burrows as brooding burrows by eastern cicada killer wasps in Pike County, Indiana.

Little is known about the ecology of L. chimera in situ, but specimens which we have kept in laboratory aquariums have readily consumed a variety of aquarium fish foods, snails, earth worms, and leaf litter from streams, suggesting that this species is an opportunistic omnivore. These specimens were mostly active at night, when they foraged around their enclosures. During the day, they rested inside of artificial burrows made from PVC pipes, occasionally twitching their antennae in response to stimuli. They did not appear to be particularly aggressive, compared to other crayfish species.

Figures

FIGURE 6. Dorsal view of Form I holotypic male of Lacunicambarus chimera (OSUMC 10650). Photo by Guenter Schuster.

FIGURE 7. Form I holotypic male of Lacunicambarus chimera. (OSUMC 10650) (A–D, G–J, L–M); Form II morphotype (OSUMC 10651) (E, F); Allotype (OSUMC 10652) (K). Lateral view of cephalothorax (A); mesial and lateral views of Form I gonopod (B–D); mesial and lateral views of Form II gonopod (E, F); ischial hook (G); ventral view of merus (H); epistome (I); dorsal view of cephalothorax (J); annulus ventralis (K); dorsal view of antennal scale (L); dorsal view of chela (M). Photos by Guenter Schuster. Abbreviations: CP, central projection; MP, mesial process; U, umbo.

FIGURE 8. Dorsal view of juvenile Lacunicambarus chimera specimen from Pike County, Indiana (MGG-170812-03). Photo by Mael Glon.

FIGURE 9. Dorsal view of young adult Lacunicambarus chimera specimen from Pike County, Indiana (MGG-170812-03). Photo by Mael Glon.

FIGURE 10. Range map of Lacunicambarus chimera specimens examined (see Table 1 for details). Green dots indicate collection locality and the orange star represents the type locality of the species.

FIGURE 11. Sunburst chart adapted from Miller et al. (2014) showing occurrences of different life history stages (represented by different colors) by month in our specimens examined. Abbreviations: FI, Form I; FII, Form II.