Onthophagus cavernicollis Howden and Cartwright, 1963

Slay, Michael E., Skelley, Paul E. & Taylor, Steven J., 2012, New Records ofOnthophagus cavernicollisHowden and Cartwright (Coleoptera: Scarabaeidae) from Ozark Caves, with a Review of Scarabaeoids Reported from North American Caves, The Coleopterists Bulletin 66 (3), pp. 187-199 : 188-192

Onthophagus cavernicollis Howden and Cartwright, 1963

Onthophagus cavernicollis Howden and Cartwright 1963: 32–35 .

“ Onthophagus n. sp. ”, Gardner 1986: 52.

Diagnosis. ( Figs. 2–6 ) Onthophagus cavernicollis can be distinguished by the following characters (modified from Howden and Cartwright 1963): Large robust body; length 7.5–11.2 mm, width 4.6–6.4 mm. Head and pronotum shiny with metallic green sheen; elytra entirely dull with uniformly dark blue or green tint; dorsal surface lacking setae. Clypeal carina in both sexes elevated in middle, when present. Frontal carina in dorsal view sinuate, convex anteriorly on each side. Head coarsely punctured. Pronotum with scattered punctures of 2 distinct sizes, large punctures 4 times diameter of smaller punctures, widely spaced on posterior disc, closer near tumosity and on anterior face. Protibia with few weak secondary teeth near base of exterior edge.

Male Major. ( Figs. 2 , 4 ) Clypeus broad, transverse; margin broadly arcuate anteriorly, shallowly emarginate at junction with gena; clypeal surface strongly reflexed anteriorly; clypeal carina vague to absent. Frontal carina extending almost to eye, raised to a blunt point at middle, lower at sides. Pronotum strongly convex with large, rounded anterior tumosity raised abruptly behind the anterior margins, ending on each side in a small raised ridge; below the ridge on each side is a distinct shallow concavity occupying most of the area near the anterior angles. Protibia elongate, inner margin curved, surface flattened, shallowly concave near apex, inner apex with small tooth.

Male Minor. ( Fig. 5 ) The specimen of “ Onthophagus n. sp. ” reported by Gardner (1986) was located in the USNM and studied. It proved to be a teneral male minor, morphologically identical to fully-colored male minors in our recent collections. Both of our male minors were part of a series including male and female majors. Their gender was confirmed by dissection.

Body smaller than male majors, length 7.5– 8.0 mm, width 4.6–4.8 mm. Clypeus semicircular; margin broadly arcuate anteriorly, weakly emarginate at junction with gena; clypeal surface weakly reflexed anteriorly; clypeal carina distinct, sharp, less well-developed than in female. Frontal carina similar to male major, raised in middle to a blunt point, lower at sides. Pronotum convex, weakly tumid anteriorly, lacking lateral ridge; concavity each side near anterior angles weak, indistinct. Protibia weakly elongate, inner margin curved, surface flattened, lacking shallow concavity near apex, inner apex angled at 90°. Three specimens studied.

Female Major. ( Figs. 3 , 6 ) Clypeus semicircular; margin feebly emarginate anteriorly, weakly emarginate at junction with gena; clypeal surface weakly reflexed anteriorly; clypeal carina strong, sharp, raised to blunt point in middle. Frontal carina wide, gradually elevated from middle to abrupt lateral ends that are nearer the eyes than the middle; raised ends are short, horn-like, transversely flattened projections. Pronotum strongly convex, tumid anteriorly, tumosity broadly rounded; lateral concavities each side of anterior tumosity small but distinct. Protibia shorter and broader than male, inner margin curved, surface weakly convex to obtuse inner apical angle.

7) Female minor.

Female Minor. ( Fig. 7 ) Body smaller than female major, length 9.0 mm, width 5.1 mm. Clypeus elongately semicircular; margin feebly emarginate anteriorly, weakly emarginate at junction with gena; clypeal surface weakly reflexed anteriorly; clypeal carina strong, sharp, raised to blunt point in middle. Frontal carina wide, gradually elevated from middle to abrupt lateral ends that are nearer the eyes than the middle; raised ends are weakly higher than at middle. Pronotum convex, weakly tumid anteriorly, tumosity broadly rounded; lateral concavities each side of anterior tumosity weak, indistinct. Protibia shorter and broader than male, inner margin curved, surface weakly convex to obtuse inner apical angle, not notably different from female major. One specimen studied.

Distribution and Label Data. Arkansas: [Boone Co.] Harrison, Waglers Cave, 13 Apr 1935 in bat dung, J. M. Valentine (Howden and Cartwright 1963, Holotype and allotype cited in USNM). Marion Co.: Square Cave, 22 July 2004, M. Slay and C. Bitting (100 Hand: collected from the twilight zone, 101 Hand: collected from the twilight zone) (2-FSCA). Newton Co.: Pentrance Cave, 24 October 2006, Wade Baker (1-FSCA). Washington Co.: 24 Apr 1938 (Howden and Cartwright 1963, 1 paratype [INHS]. Missouri: [unknown county]: “Cave - Central Mo.”, J. Peasely, Nov. 1972 (1-PKLC). Barry Co.: Currey Cave, 2 mi W Shell Knob Missouri, 29 July 1981, J. E. Gardner ( Gardner 1986; 1-USNM); 3.2 mi. S Roaring River on hwy. 112, T21N R27W S9 (SE1/4); 13-vi-1997, T.C.MacRae, nocturnally on Quercus velutina slash (1-WBWC). [Johnson Co.], Warrensburg, 9-14-72, Kathy Hudek (1-PKLC). McDonald Co.: Long Cave; ( Gardner 1986). Oregon Co.: Two Entrance Cave, 15 mi SE Alton Missouri, 9 July 1981, J. E. Garner; ( Gardner 1986; 1-USNM). [Phelps Co.], Hanley Cave, 6 Feb 1979, J. E. Gardner, MDC 184 (presented as “ Onthophagus n. sp. ” in Gardner 1986; 1- USNM). Pulaski Co.: Fort Leonard Wood Military Base, 23PU308, 13 May 2004, S. Taylor and M. Slay (510 Hand: on debris on normal breakdown block) (1-FSCA); Fort Leonard Wood Military Base, Flat Roof Cave, 10 May 2004, S. Taylor and M. Slay (377 Hand: dry dusty floor) (1-FSCA); Fort Leonard Wood Military Base, McCann Cave, 12 May 2004, S. Taylor and M. Slay (460 Hand: on underside of stone on normal soil floor, 463 Hand: dry soil and woodrat scat, 466 Hand: in woodrat feces on dry soil floor) (5-FSCA); Fort Leonard Wood Military Base, Miller Cave, 22 March 2003, M. Slay, S. Taylor, and V. Block (207 Hand: in pigeon guano) (1-FSCA); Fort Leonard Wood Military Base, Phreatic Cave, 24 October 2003, S. Taylor and M. Slay (039 Hand: in dry feces on floor, 041 Hand: normal soil floor) (2-FSCA); Fort Leonard Wood Military Base, Schmoeller Cave, 10 May 2004, S. Taylor and M. Slay (395 Hand: under stone with woodrat scat/fungus with normal moisture) (1-FSCA); Freeman Cave, 3.5 mi. ESE Fort Leonard Wood, 27 September 1984, J.E. Gardner (1-PKLC); Mark Twain National Forest, 14.5 mi. WSW of Rolla, Boiling Spring Saltpeter Cave, 16-May-2010, M. Sutton, deep twilight on the wall (1-FSCA). Shannon Co.: Blue Aerie Cave, 5.5 mi NE Mountain View, 2 May 1984, J. E. Gardner (1-UMRM, 1-PKLC). Stone Co.: Gentry Cave, MAY/03/1958, O. Hawksley (1-CMNC). Taney Co.: Back Door Cave, ( Gardner 1986). Texas Co.: Unnamed Cave No. 1., 10.5 mi NW Licking Missouri, 14 May 1980, J. E. Gardner ( Gardner 1986; 1- USNM); Unnamed cave #4, 11 mi. SNW Licking, 5 May 1980, J. E. Gardner (1-UMRM); FS Cave 135, 12 mi SNW Licking, 1 May 1980, J. E. Gardner ( Gardner 1986; 1-UMRM, 2-USNM). [Texas Co.], Liking [sic = Licking?], Bat Cave, 20 June 1956, Condé (Howden and Cartwright 1963, cited in Muséum National d’ Historie Naturelle, Paris; 1-CNIC). Oklahoma: Adair Co.: Christian School Study Cave, 5 mi. S Kansas, 07/11/1971, J.H. Black (1 CMNC); Cherokee Co.: [incorrectly labeled as Adair Co.], Tahlequah, 26 Sept 1954, O. C. Schomberg (Howden and Cartwright 1963, Black 1971, Wallace and Drew 1964; 1- CNIC). Delaware Co.: cave identified as DL-3, 27 July 2005, G. Graening, M. Slay, and W. Puckette (2-FSCA). Murray Co.: Little Crystal Cave, Turner Falls Park, January/15/ 1974, J. H. Black (Zunino and Halffter 1988; 1-CMNC, 1-TAMU). Texas: [no locality] (Howden and Cartwright 1963, 1 specimen cited in the Museum of Comparative Zoology, Cambridge, Massachusetts). Kendall Co.: vicinity Cave Without a Name, near Boerne, 30 July 1948, G. E. Ball (Howden and Cartwright 1963, 1 specimen cited as in American Museum of Natural History, New York, New York). Edwards Co.: Sumac Cave, April/02/1988, S. Tomsett (1-CMNC).

Remarks on Sexual Dimorphism. Onthophagus Latreille is a highly speciose genus, with over 2,000 described species ( Gill 2005; Tarasov and Kabakov 2010). It is very diverse in male secondary sexual characters, ranging from those with wildly modified male horns to species whose males can only be distinguished by genitalic morphology. Reasons for this diversity in Onthophagus and other dung beetles is the subject of many developmental and evolutionary studies too numerous to review in our presentation here (e.g., Arrow 1951; Emlen et al. 2005; Moczek 2011).

Male beetles often have reduced, female-like sexual ornaments (Rowland and Emlen 2009), and it is less common for females to possess male-like ornamentation as in some members of Coprophaneus Olsoufieff ( Arrow 1951; Edmonds and Zidek 2010). However, beetle species in which the female’ s secondary sexual ornaments are more elaborate than those of the male are quite rare (J. M. Rowland, 2012, personal communication). Examples of this within scarabs include Attavicinus monstrosus (Bates) (Philips and Bell 2008) , the Southeast Asian Onthophagus sagittarius (F.), and the Nearctic O. cavernicollis , discussed here.

Onthophagus cavernicollis males have reduced cephalic ornamentation and enlarged pronotal swellings that are characteristic of all members of the “ chevrolati group” (Zunino and Halffter 1988), but O. cavernicollis seems to be the only species where males lack horns while females have them. In addition, O. cavernicollis has both male and female majors and minors. Unfortunately, there are too few specimens of O. cavernicollis available to make any further statements. Analyses of such phenoplastic systems in Onthophagus may provide valuable insights into the mechanisms by which this and other groups have undergone extraordinary and apparently rapid diversification (J. M. Rowland, 2012, personal communication to PES).

Observations on the Life History of O. cavernicollis . Analysis of label data from the above specimens shows the species was collected in all four seasons and in 10 of the 12 calendar months (not collected in August or December). Only five of 32 collections with label information occurred outside caves. Of these five, one occurred in the spring, two in the summer, and two in the fall. Habitat information was recorded for one non-cave collection; one specimen was collected nocturnally in June from slash of Quercus velutina Lamarck (Fagaceae) , which indicates the species may leave the caves to disperse. For cave sites, Gardner (1986) reported collecting within the twilight and dark zone of caves. For our records, we also collected specimens from the twilight and dark zones of caves.

Of the 10 specimens examined by Howden and Cartwright (1963), eight were collected in bat guano, suggesting the species may be associated with guano in cave habitats. Black (1971) also reported O. cavernicollis from bat guano. Yet, recent collection data as well as comments by Gardner (1986) strongly suggest O. cavernicollis to be more frequently associated with eastern woodrats, Neotoma floridana (Ord) , than with bat guano. Gardner (1986) reports collecting specimens from under wood, beneath dung, and in woodrat scats and nests. We often collected specimens associated with woodrat scats or middens. However, in Miller Cave we collected specimens from bird droppings below a pigeon roost. Eastern woodrats are one of the more common vertebrates encountered in Oklahoma and Arkansas caves ( Graening et al. 2012), and we noted the presence of woodrats in 23 of 57 caves that were surveyed for invertebrates in Pulaski Co., Missouri. While dispersing, adult beetles may feed on bat guano. We strongly suspect the larval food is detritus or dung in eastern woodrat nests. However, no larvae are presently known.

Zunino and Halffter (2007) provide an excellent review of the use of caves and burrows by Onthophagus spp. , and they list three North American species that seem to be associated specifically with caves. Onthophagus verspertilio Howden, Cartwright, and Halffter and Onthophagus moroni Zunino and Halffter are reported from a few Mexican caves, while O. cavernicollis is known mainly from caves in the United States. These species were considered tentative troglobionts (= troglobites), or obligate cave species, by Zunino and Halffter (2007) because they were collected mainly from caves, appeared to be associated with large piles of bat guano, and were of the same phylogenetic group. The authors did express some doubt to this classification because of lack of documented reproduction in caves by these species. Only adults have been collected from caves, even with considerable effort by Zunino and Halffter (2007) to collect larvae of O. verspertilio and O. moroni . Our collections of O. cavernicollis suggest the species is not limited to bat guano, but is more commonly associated with woodrat scats and midden piles. Because woodrats also use surface locations (such as rock ledges and limestone outcrops) as latrines and nesting sites ( Wiley 1980; Clark et al. 1994), O. cavernicollis may also be found in these habitats. We did not inspect woodrat latrines or middens that occurred under bluffs or on rock ledges during our study. For now, we consider O. cavernicollis a facultative cave species (troglophile) rather than a troglobiont.

Zunino and Halffter (1988, 2007) discussed the “ chevrolati group, hippopotamus subgroup” of Onthophagus that have several unique morphological features along with sharing an apparent preference for living with rodents. Some species, like Onthophagus coproides Horn in the southwestern US and others in Mexico, show distinct preference for burrows of tusas or pocket gophers ( Rodentia : Geomyidae ). In the US, O. cavernicollis is structurally most similar to Onthophagus brevifrons Horn and Onthophagus subtropicus Howden and Cartwright from the southern and western US – species that prefer woodrat nests, especially nests in rock cavities. Because of the morphological similarities and observations discussed above, O. cavernicollis may have a more natural association with woodrats than other cave dwelling vertebrates.

The ecological, behavioral, and morphological progression of characters from surface nestdwelling species, through rodent burrow and crevice-dwelling species, to cave habitats is a logical sequence but remains phylogenetically untested. Additional study of rodent nests and burrows may yield new insights into the life histories and relationships of these possibly common but rarely seen species.

ADDITIONAL SCARABAEOIDEA COLLECTED OR REPORTED FROM NORTH AMERICAN CAVES

Perhaps the most comprehensive cave invertebrate survey that included scarab beetles was that of Gardner (1986) from caves in Missouri. In the study, 14 species were reported, including undescribed species of “ Aphodius ” and “ Onthophagus ”, along with information on the situations where the beetles were collected ( Gardner 1986). The “ Aphodius n. sp. ” was recently described ( Gordon 2006), while the “ Onthophagus n. sp. ” was found to be a male minor of O. cavernicollis . The following list is compiled from Gardner (1986) and other references, with the addition of our recently collected materials. Each species mentioned is briefly discussed with regards to its potential relationship to caves, most being accidentals or associated with vertebrates that live in burrows or crevices. Only two, O. cavernicollis and possibly Stenotothorax gardneri Gordon , may have more important relationships with caves.

Figures

Figs. 2–3. Onthophagus cavernicollis, dorsal habitus. 2) Male major; 3) Female major.

Figs. 4–7. Onthophagus cavernicollis, anterolateral view. 4) Male major; 5) Male minor; 6) Female major;