Krantz, Gerald W. ¹

¹✉ Integrative Biology, Oregon State University, Corvallis, OR 97331, USA.

2023 - Volume: 63 Issue: Suppl pages: 29-38

Proceedings of the 9^th Symposium of the EurAAc, Bari, July, 12^th–15^th 2022

Keywords

Abstract

INTRODUCTION

Mycotrupes LeConte

The geotrupid beetle genus Mycotrupes (Fig. 1) comprises five flightless, relict, allopatric species that occupy deep, well-drained sand ridges overlying porous limestone in peninsular Florida (Woodruff 1973) and a narrow, more northerly elevated sand hill zone separating the Atlantic Coastal Plain from the adjacent Piedmont in South Carolina and Georgia, a zone referred to as the Fall Line (Fig. 2). Mycotrupes species are efficient burrowers, often tunneling down through sand to depths exceeding six feet (Howden 1954, 1955). Their sandy habitat is mostly a xeric, open woodland in which the most abundant trees are turkey and bluejack oaks that originally served as the understory for a great pine forest that thrived there in earlier times. Clumps of seedling oaks and low shrubs surrounded by quantities of dead leaves, along with a scattering of grasses and various herbs, also are common there (Olson & Hubbell 1954). Mycotrupes species are generalist feeders that take advantage of virtually any available organic food substrate in their heterogenous environment: dung, decaying fungi, plant litter, and even exposed soft tissue of acorns. As noted by Beucke (2009), reliance on a particular food source where its availability from year to year or season to season often is unpredictable would be a risky strategy for a genus whose members are flightless and consequently restricted in their searching capacity. According to Howden (1955, 1963), flightlessness in Mycotrupes arose early in the development of the genus and is a consequence of metathoracic wing degradation, coupled with median fusion of the prothoracic elytrae.

The deep sand ridges that shelter Mycotrupes species are believed to be remnants of ancient shorelines laid down during the alternating flooding/emergence episodes of the Pleistocene Epoch (Cooke 1945, Fig. 3). These sand ridges are isolated from one another by areas of poor drainage, shallow sand, swamps, marshes, rivers, low-lying dry timberland, or dense vegetative hammocks. Barriers such as these apparently were enough to produce the vicariance events that led to allopatry of Mycotrupes populations and to their subsequent speciation.

Hubbell (1954) presented a compelling evolutionary scenario for Mycotrupes in which he considered Mycotrupes gaigei Olson & Hubbell (Fig. 1) to be the most aberrant member of the genus, and its paleogeographic niche in western peninsular Florida (Fig. 2) to be the site where the genus made its first appearance during the late Tertiary. Hubbell's conclusions were later evaluated during the course of a molecular phylogenetic study of Mycotrupes by Beucke (2009), whose findings were based on nucleotide sequence data derived from a 481 base pair fragment of the Cytochrome Oxidase I gene taken from all five Mycotrupes species. Beucke's parsimony analysis revealed that the two Fall Line species, Myco. retusus (LeConte) and Myco. lethroides (Westwood), are basal to the other three described members of the genus (Myco. gaigei, cartwrighti O. & H. and pedester Howden), from which Beucke concluded that the genus originated on or close to the Fall Line, possibly during the Tertiary. He also concluded that, at some point after the sea level had fallen well below the level of the elevated Fall Line for the last time in the late Pleistocene (Fig. 3), a southward dispersal of Myco. retusus gave rise to Myco. gaigei, cartwrighti, and pedester, along with a possible cryptic species in the cartwrighti lineage. Based on Beucke's findings, sea level changes generated by intermittent glaciation and melting events during the Pleistocene evidently played a major role in the evolution of Mycotrupes.

Geotrupacarus mycotrupetes (Krantz & Mellott)

Scarabaeoid beetles worldwide serve as hosts for a variety of mites, and Mycotrupes is no exception. Geotrupacarus mycotrupetes (Fig. 4), a mite originally described as a member of the genus Macrocheles by Krantz & Mellott (1968), is a large (\textgreater1,000 μm), distinctive phoretic form that attaches preferentially behind coxae I or in the gular area of Myco. gaigei in northwestern peninsular Florida. Like its beetle host, G. mycotrupetes is arenicolous and burrows with ease through sand substrates. In laboratory studies, it was observed to use its formidable burrowing capabilities in locating Myco. gaigei when the beetles and the mites were sequestered in separate wire mesh cages beneath the sand surface (Fig. 5), presumably in response to recognition of a kairomonal cue generated by the beetle host (Krantz & Royce 1994). Although it is clearly phoretic, the morphology and reproductive strategy of G. mycotrupetes point to a close phylogenetic relationship with early derivative, free-living macrochelid taxa best exemplified by the genus Nothrholaspis Berlese (Emberson 2010). Like Nothrholaspis, G. mycotrupetes lacks the subterminal bidentate tooth typically present on the cheliceral movable digit of more highly derived phoretic macrochelids, a structure coupled with an opposing ribbed platform on the fixed digit to form a complex for grasping a single hair of its host (Fig. 6). In addition, the lateral elements of the gnathotectum of G. mycotrupetes, like those of Nothrholaspis species, are broadly fused to a bifurcated central element (Fig. 4d) rather than being free and flaglike as in more highly derived forms. The female ventrianal shield (Fig. 4b) is narrow and oblong rather than being subtriangular or broadly rounded as in Nothrholaspis species (Emberson 2010), and the cribrum has narrow paranal extensions (Krantz, 2009) (overly abbreviated in Krantz & Mellott, 1968, Fig. 4b) that are more typical of early derivative lineages rather than being totally reduced to a narrow band of spicules confined to the posterior margin of the shield as in more highly derived macrochelids. Similar cribral extensions also occur in all postlarval immatures of G. mycotrupetes (Krantz 1990, Krantz & Royce 1992). Postepigynal platelets, again characteristic of more primitive lineages, are present in the female (Krantz 1998). Among the less obvious morphological features that define both described species of Geotrupacarus (G. mycotrupetes and peltotrupetes) are the infrequent and often obscure barbs that ornament the subcapitular and ventral shield setae. Their obscurity is a consequence of some barbs being so closely aligned to their given seta that they are easily overlooked, as sometimes occurred in the original species descriptions (Krantz & Mellott 1968). Finally, the reproductive strategy of G. mycotrupetes is more suggestive of primitive diplodiploidy or parahaploidy (sensu Norton et al. 1993) than of the arrhenotokous form of haplodiploidy common to most insect-associated phoretic macrochelids (Krantz & Royce 1994).

Overall, the primitive characteristics of G. mycotrupetes, coupled with its unusual phoretic proclivities, lends credence to the concept that phoresy has arisen more than once in the Macrochelidae (Krantz & Royce 1992), and at the same time raises the question as to whether a phoretic association with a non-vagile host like Myco. gaigei could involve something other than transport to a fresh food substrate.

Objectives

The major objectives of this study were to determine 1) whether G. mycotrupetes, originally described as phoretically specific on Myco. gaigei, occurs on any of the other four described species of Mycotrupes (viz., retusus, lethroides, cartwrighti, pedester); 2) whether other, heretofore undescribed, members of the genus Geotrupacarus occur on species of Mycotrupes other than gaigei; and 3) whether G. egeriei (Fig. 7), a winged, widely distributed geotrupid that co-occurs with G. mycotrupetes in Florida, and to which G. mycotrupetes is strongly attracted in laboratory settings, may have succeeded in expanding the range of G. mycotrupetes beyond Florida and the Fall Line.

Materials and methods

Although commonly observed in field collections, occurrence of G. mycotrupetes on Myco. gaigei tends to be erratic, which implies that verifying the presence of G. mycotrupetes on Myco. retusus, lethroides, cartwrighti or pedester, or confirming the presence of undescribed Geotrupacarus species on any of these beetles, would likely require access to relatively large numbers of specimens. Accordingly, requests for study material went out to four museums where significant geotrupid beetle collections were known to be located (see Acknowledgements for details). The recognized potential for G. egeriei to expand the range of G. mycotrupetes northward beyond Florida (see Objective 3, above) made G. egeriei an additional target of museum searches during the course of this study.

Results and discussion

More than 400 mite collections taken from all five described Mycotrupes species offered convincing support for the conclusion that G. mycotrupetes is phoretically specific to Myco. gaigei. No other species of Geotrupacarus were found on any of the 133 available specimens of Myco. retusus, lethroides, cartwighti and pedester, nor was there any evidence to suggest that G. egeriei had carried G. mycotrupetes beyond its normal Florida range. It should be noted here that available Myco. gaigei, Myco. cartwrighti and G. egeriei specimens (282, 73, 104) far outnumbered the more narrowly distributed and less often collected Myco. pedester, lethroides and retusus (28, 15, 17), leaving room for speculation as to whether additional collections of the latter three species might reveal a broader host distribution for G. mycotrupetes, or verify the presence of other species of Geotrupacarus.

Geotrupacarus mycotrupetes seems to have defied a major precept of phoresy in choosing a host beetle that is flightless and presumably unable to carry it to fresh food substrates. Also, the incidental recovery of other phoretic Macrocheles species on four of the five species of Mycotrupes (Myco. lethroides excepted) and of phoretic Eviphididae on three species of Mycotrupes (Myco. pedester and Myco. retusus excepted), leaves unanswered the question as to what benefit can be expected from a relationship between these highly derived phoronts and flightless, reclusive allopatric beetles that spend much of their lives in deep sand burrows. Clearly, there are factors involved in these relationships that have yet to be resolved.

The strong attraction of G. mycotrupetes to G. egeriei in laboratory settings (Figs. 8a, b) belies the virtual absence of the mite from field collections of G. egeriei beyond Florida. This seeming contradiction illustrates the overarching importance of niche integrity and habitat dimension in natural ecological systems. Moving beetles from their natural habitat to an alien laboratory environment is disruptive not only for the beetles, but for their acarine phoronts as well, and may account for the unexpected high boarding levels of G. mycotrupetes on Geotrupes egeriei (at most an incidental host under natural conditions) in mite boarding tests on beetle candidates in both individual and group choice experiments (Krantz & Mellott 1972).

In their natural habitats, scarabaeoid beetle species each occupy an n-dimensional universe in which they respond in given ways to biotic and abiotic signals inherent to that universe. Hutchinson (1957) referred to these n-dimensional universes as hypervolumes. Each scarabaeoid species maintains an insularity based on its hypervolume, an insularity that also provides the conditions for niche integrity of their phoretic acarine associates (Krantz 1991). Chemical signals in the form of beetle-generated kairomones are a particularly important dimension for phoretic acarines occupying the n-dimensional universe of their host. In the laboratory setting referred to earlier, it appears that attraction of G. mycotrupetes to a given beetle species was based primarily on recognition of a class of kairomones common to both Mycotrupes and Geotrupes (Krantz & Mellott 1972, Krantz 1998). A study of the chemical structure of this compound in Mycotrupes cuticle (Krantz et al. 1991) revealed that it corresponds in some respects to the major dihydroxy wax ester found in uropygial fluid, an oily substance produced in a gland near the anal vent of many birds and used by them to waterproof their feathers. Based on that study, the kairomonal attractant in the cuticle of Myco. gaigei was tentatively identified as a dihydroxy wax or its diol ester.

Finally, in regard to G. egeriei and the four other scarabaeoid beetle species whose levels of attractiveness to G. mycotrupetes in the laboratory were referred to by Krantz & Mellott (1972), the loss of niche integrity occasioned by transfer of test beetles from the field to a laboratory setting apparently left G. mycotrupetes with only one recognizable dimension to which it could respond—the chemical dimension. Future laboratory studies on phoretic responses of mites to prospective hosts should therefore consider niche integrity and dimension as major variables when creating experimental systems.

Acknowledgements

I acknowledge with pleasure the receipt of beetle specimens, alcoholic mite collections, and pertinent tabular data on mites taken from Mycotrupes species and from G. egeriei provided by curators of four major geotrupid collections in the US and Canada. Paul Skelley, Head Curator of the Florida State Collection of Arthropods in Gainesville, kindly sent data sheets and 62 alcoholic collections of G. mycotrupetes and other gamasines from all five Mycotrupes species, and E. Richard Hoebeke, Associate Curator and Collections Manager of the University of Georgia Collection of Arthropods in Athens provided 20 mite-laden Mycotrupes and Geotrupes egeriei beetles for study. Mite data on 53 Mycotrupes and 29 Geotrupes egeriei collections were generously provided by Frédéric Beaulieu and Wayne Knee, Acari Unit Curator and Curator Assistant at Ottawa's Canadian National Collection of Insects, Arachnids and Nematodes. I am grateful to François Génier, Curator of the Canadian Museum of Nature in Ottawa, who sent essential data on mites from 290 Mycotrupes and 71 G. egeriei specimens housed in CMN, a small subset of the vast geotrupid collection bequeathed to the Museum by the late Henry F. Howden, a world specialist on the Geotrupidae. My thanks also to Brett Ratcliffe, Curator of the University of Nebraska Beetle Collection, who provided mite specimens from G. egeriei during the early days of this project, and to Chris Marshall, Curator of the Oregon State Arthropod Collection in Corvallis, who shared information on pertinent museum collections and made the OSAC collection of geotrupids available to me for study. Finally, I thank the late Robert Woodruff, author of many fine works on Florida scarabs, for his advice and encouragement when I first delved into the complex and fascinating world of Florida scarabaeoids and their equally fascinating acarine phoronts.

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