Mantidflies: Chimeras of the Insect World

The Chimera of Arezzo, an Etruscan effigy of the monster

Now it's time to post on creatures that I've wanted to discuss for along time: mantidflies. I was immensely gratified when I finally collected one (Dicromantispa sayi) this past June. These insects are uncommon and little-known outside of the entomological community, which is a pity, given their strangeness–both in their chimerical morphology and weirdo ontogeny.

How is a mantidfly akin to the Chimera–a monstrous fire-breathing beast of Greek myth? This fictitious creature had the body (and head) of a lion, a serpentine tail with a snake's head at its tip, and a dorsal goat's head to boot: consequently, the name has become a byword in biology for an organism assembled from unrelated parts. Mantidflies (Mantispidae) certainly look as though they were haphazardly crafted in this fashion: they have the abdomen, wings, and thorax of a lacewing attached to the head, pronotum, and forelegs of a mantis. This confusion of insect bodies is compounded in Climaciella brunnea, a common North American species, since it does a very passable impersonation of a paper wasp (Polistinae), as seen below.

A Louisianan C. brunnea, photographed by Gayle Strickland

Mantidflies' marked likeness to their namesakes is the result of convergent evolution–the two insects could not be more unrelated, as one can readily see from mantispid ontogeny (more about that later). But, as one would surmise from those ferocious grabbing chelae, the members of the Mantispidae are predators just as the mantises (although small ones: 2-3.5 cm.). To determine mantidflies' true provenance we must disregard their body-parts from the mesothorax forward. Excluding those, it is obvious that the mantidfly is a member of the order Neuroptera, along with antlions, dustywings, owlflies and all manner of lacewings. Among the other families of this order (collectively called "net-winged insects"), the Mantispidae are most akin to the beaded lacewings (Berothidae) and thorny lacewings (Rhachiberothidae–formerly sunk into the Berothidae; Tjeder, 1959), with which they comprise the Mantispoidea. Both these lacewings are rather more conventional than their mantidfly cousins, although beaded lacewing larvae (or those in the sole North American genus) are odd in that they haunt termitaries, preying on the resident termites with the Fart of Death (actually a blast of deadly gas from anal glands; Johnson & Hagen, 1981). This would be a good place to engage in some middle-school fun at beaded lacewings' expense, but I'll refrain.
 

Lomamyia sp., the only genus of beaded lacewing found in the United States; picture by Randy Hardy

Neuropterans are holometabolous: that is, their metamorphosis is complete (proceeding from larva to pupa to adult). That alone establishes the Mantispidae's un-relation to the order Mantodea, the constituents of which are nymphs (not larvae) when young (and thus hemimetabolous), even if a systematist ignored the obvious neuropteran affinity demonstrated by mantidflies' fossil record and wing venation. It is the particular mantispid mode of metamorphosis that completes their surreal persona. Ontogenetically speaking, however, the four mantidfly subfamilies differ substantially; so a description of each would probably be germane before I treat their metamorphoses.

The Symphrasinae are the most plesiomorphic of the foursome (since it's politically incorrect to call them "primitive") (Lambkin, 1986); thorny lacewings were once classified as mantidflies due to a noticeable similarity (Willmann, 1990). In line with their basal status, symphrasines have a short prothorax; they are presently restricted from South America north to the southwestern United States, although they had a presence in Germany in the Paleogene Period (Wedmann & Makarkin, 2007). To continue: the Drepanicinae are roughly as advanced as the Symphrasinae; they range throughout Australia and South America, but are known as fossils from the mid-Cretaceous of Kazakhstan (Makarkin, 1990). Unusually, the genus represented from that locality (Gerstaeckerella) is extant (Enderlein, 1910). The Calomantispinae are known only from Central America (north into the San Fernando Valley) and eastern Australia (all of Queensland, New South Wales, Victoria, and Tasmania), and have no fossil record; whilst the Mantispinae are by far the most widespread and diverse of the subfamilies, found in all the regions in which the other subfamilies are present (except Argentina and Tasmania) plus the rest of the world north to about 50°N (Wedmann & Makarkin, 2007) and lived on the Isle of Wight during the Paleogene Period (Jarzembowski, 1980).

A Plega sp. (Symphrasinae) making rude tarsal gestures at the photographer (Marcela Freerks)

Now that we've gotten all of that under finger, I'll get on with the interesting stuff. The larvae of Calomantispinae–those that are known–have a lifestyle typical of net-winged insects: that of mobile predators. Symphrasines and mantispines are the ones that "grow outside of the box", as it were (drepanicines' young remain unknown). The life-cycles of the mantidflies in the Symphrasinae remains poorly-studied; but what we do know shows us that as larvae they are parasitoids of bees and wasps (both solitary and social; Buys, 2008; Hook et al., 2010). Some have also been implicated as attackers of moth, fly, or beetle pupae (Parfin, 1958). How the larvae reach their hosts remains uncertain. They could, of course, be laid as eggs thereupon by their mothers, but the fact that intrusions into beehives by adult Plega hagenella are promptly foiled by the resident (and potential host) stingless bees (Meliponini) suggests that symphrasine larvae may have to seek hosts on their own (Maia-Silva et al., 2012): as do the mantispines (also parasitoids), which are comparatively well-studied.

The hypermetamorphic stages of Mantispa sp., as shown in Introduction to Entomology (1933); not to scale

Members of the Mantispinae begin life as minuscule (~1 mm.), slender, active larvae termed planidia–from the Greek for "wandering" (Gordh & Headrick, 2003), since that is all a planidium does from the moment of its hatching. The objective of this wandering is a spider: locating and boarding such a creature is vital to the larva. Finding a suitable one is difficult (species differ in preference); at this point Morgan Freeman might solemnly intone that Many Will Not Survive, which would be absolutely true: mantidfly mothers lay something on the order of 1,000 eggs in each batch (Drees & Jackman, 1999), compensating for the tiny odds that any one planidium will reach its hairy eight-eyed destination. But that destination is not in and of itself the larva's prospective host.

A first-instar mantispine situated near a jumping spider's (Salticidae) pedicel; photograph by Jeff Kramer

What, then, is the purpose of a mantispine planidium's quest? Their relationship with the adult spiders is only phoretic*, for it is upon the contents of spiders' egg sacs that they feed. Naturally, only a female spider will produce what the larva requires; but if a planidium has the misfortune to board a male, all is not necessarily lost: like some kind of crawling STD, it can transfer to the male's mate during copulation (or cannibalization). In the meantime, the planidium may conceal itself by coiling around the juncture betwixt cephalothorax and abdomen (as seen above) or, if the spider molts, take shelter in the latter's book lungs, surviving by sucking blood from those organs for the time being (Redborg & MacLeod, 1983). Some species (D. sayi among them) may dispense with the hassle of spider phoresy and simply seek out and penetrate egg sacs directly (Redborg, 1998); but others are obligate spider boarders: they can only enter an egg sac while it is under construction (Redborg & MacLeod, 1983).

Ocnaea sp. (Acroceridae), female, photographed by Jeff Gruber

Regardless of how it accomplished the feat, a larva that has gained entrance to an egg sac molts, and undergoes a total morphological shift: one from a campodeiform (fast-running, flattened, and in possession of functional antennae) shape (fig. A in the illustration from John Henry Comstock's Introduction to Entomology) to a scarabaeiform (inactive and grub-like) one (B). Immersed in the embryonic spiderlings upon which it will subsist, the mantidfly has no further need for a planidial form (Imms, 1957). Hypermetamorphosis, as this change is termed, is a rarity among the holometabolous insects, appearing in 4 disparate orders aside from the Neuroptera; it is always an adaptation to a parasitoid ecology in situations where it is inconvenient for a mother to directly lay her eggs on the host (as the vast majority of parasitoids do). Mantidflies' fellow hypermetamorphic insects–such as wedge-shaped beetles (Rhipiphoridae) and small-headed flies (Acroceridae)–are nearly as fascinating this post's titular chimeras: but I will have to defer them to another day.

Happy New Year (if it is a happy one–which I doubt).



*That is, hitchhiking, as opposed to parasitic.
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Buys, S. C. (2008). Observations on the biology of Anchieta fumosella (Westwood 1867) (Neuroptera: Mantispidae) from Brazil. Tropical Zoology, 21, 91-95.

Drees, B. M. and Jackman, J. (1999). Field Guide to Texas Insects. Houston: Gulf Publishing Company.

Enderlein, G. (1910). Klassifikation der Mantispiden nach dem Material des Stettiner Zoologische Museums. Stettiner Entomologische Zeitung, 71, 341-379.

Gordh, G. and Headrick, D. H. (2003). A Dictionary of Entomology. Wallingford: CABI. 

Hook, A. W.; Oswald, J. D. and Neff, J. L. (2010). Plega hagenella (Neuroptera: Mantispidae) parasitism of Hylaeus (Hylaeopsis sp.) (Hymenoptera: Colletidae) reusing nests of Trypoxylon manni (Hymenoptera: Crabronidae) in Trinidad. J. Hymenopt. Res., 19, 77-83.

Imms, A. D. (1957). A General Textbook of Entomology. London: Methuen.

Jarzembowski, E . A. (1980). Fossil insects from the Bembridge Marls, Palaeogene of the Isle of Wight, southern England. Bulletin of the British Museum of Natural History (Geology), 33, 133-140. 

Johnson, J. B. and Hagen, K. S. (1981). A neuropterous larva uses an allomone to attack termites. Nature, 289, 506-507.

Lambkin, K. J. (1986). A revision of the Australian Mantispidae (Insecta: Neuroptera) with a contribution to the classification of the family I. General and Drepanicinae. Australian Journal of Zoology (Supplementary Series), 116, 1-142.


Maia-Silva, C.; Hrncir, M.; Koedam, D.; Machado, R. J. P. and Imperatriz-Fonseca, V. L. (2012). Out with the garbage: the parasitic strategy of the mantisfly Plega hagenella mass-infesting colonies of the eusocial bee Melipona subnitida in northeastern Brazil [electronic version]. Naturwissenschaften, 100, 101-105. Retrieved 1/6/13 from http://link.springer.com/content/pdf/10.1007%2Fs00114-012-0994-1 

Makarkin, V. N. (1990). Novye setchatokrylye (Neuroptera) iz verkhnego mela Azii. In: I. A. Akimov (ed.), Novosti Faunistiki I Sistematiki (pp. 63-68). Kiev: Naukova Dumka.

Parfin, S. I. (1958). Notes on the bionomics of the Mantispidae (Neuroptera: Planipennia). Entomological News, 69, 203-207. 

Redborg, K. E. (1998). Biology of the Mantispidae. Annual Review of Entomology, 43, 175-194.

Redborg, K. E. and MacLeod, E. G. (1983). Climaciella brunnea (Neuroptera: Mantispidae): a mantispid that obligately boards spiders. Journal of Natural History, 17, 63-73.

Tjeder, B. (1959). Neuroptera-Planipennia. The lace-wings of southern Africa. 2. Family Berothidae. In: Hanström, B.; Brinck, P. and Rudebec, G. (eds.), South African Animal Life Results of the Lund University Expedition in 1950-51 (vol. 6, pp. 256-314). Stockholm: Almqvist and Wiksell.

Wedmann, S. and Makarkin, V. N. (2007). A new genus of Mantispidae (Insecta: Neuroptera) from the Eocene of Germany, with a review of the fossil record and biogeography of the family [electronic version]. Zoological Journal of the Linnaean Society, 149, 701-716. Retrieved 1/6/13 from http://www.biosoil.ru/files/00004954.pdf 

Willmann, R. (1990). The phylogenetic position of the Rhachiberothinae and the basal sister-group relationships within the Mantispidae (Neuroptera). Systematic Entomology, 15, 253-265.

Mormotomyiids' Terrible Hairiness

There are many rare insects in this world of ours—species that have been collected only once, and have never been seen since. Due to their diminutive size or retiring habits or a simple dearth of investigation by Homo sapiens, we have no idea of their habits or distribution; and so we cannot know their true range or abundance. Thus, I would reason that many "restricted" insects are no doubt only rare in the eye of a human beholder.


(Rest assured that this essay will not take the form of an argument to the effect that, given our lack of understanding of the vast majority of insects, there is no need to protect them from anthropogenic destruction; and that any attempt to do so is most likely a wrongheaded effort by leftists to squelch free enterprise. Free enterprise, of course, being the only thing that makes life worth living, as I would sincerely claim if the American Enterprise Institute were paying me gobs of money.)

A. muwu, photographed by Alice Abela

But now that I've finished my digression towards the soapbox, I will reiterate that many insects appear unusual merely due to humans' blinkering by our large size. There are exceptions, however: if we understand an insect's habitat preferences and know that the said habitat is insular, we can safely extrapolate that insect's rarity. An exemplar of these would be Ammopelmatus kelsoensis (Stenopelmatidae), an arenophilous Jerusalem cricket known only from the isolated Kelso Dunes erg in the Mojave Desert ("Ammopelmatus kelsoensis"—Natural Diversity Database). (A similarly restricted congener is shown above.)

Another instance of a truly rare insect would be the primary subject of this post, the terrible hairy fly (Mormotomyia hirsuta), which is such a bizarre creature that it's placed in its own family (naturally dubbed Mormotomyiidae). Known only from a single crevasse cleaving a gigantic hilltop boulder (and a smaller, oblique nick in selfsame boulder) in northern Kenya (near Ukasi), this surreal creature has been seen only thrice since its discovery in 1933, and definitely not due to a lack of trying: seven attempts at collecting the terrible hairy fly have been mounted in the past 79 years, with only two of them having success.

A live Mormotomyia hirsuta

The dim, cave-like fissure is a roost for bats: and, where there are bats, there is guano. It is upon (and within) this that M. hirsuta's maggots feed (van Emden, 1950). This is hardly uncommon; guano is a very nutritious substance popular with all kinds of organisms, especially true fly larvae (Diptera): this is aptly demonstrated by the presence of no fewer than 6 families (not counting Mormotomyiidae) in the rich medium at Ukasi Hill (Kirk-Spriggs et al., 2011). What is unusual is mormotomyiids' adult appearance: very hirsute (hence the name), with proportionally longer leg setae in males; no ocelli; gangly, and uncannily recalling a windscorpion (order Solifugae); and (most importantly) flightless, with the wings reduced to bristly projections (Austen, 1936). The long hair of males probably serves a function in sexual selection, making them appear larger (and therefore hardier) to potential mates (Copeland et al., 2011). The terrible hairy fly's morphology shows heavy specialization for a troglobitic (cave-dwelling) lifestyle; that much is clear. However, the adults' precise relationship with the bats upon which they indirectly depend remains uncertain (Kirk-Spriggs et al, 2011). 

A Swiss bat fly (Nycteribiidae) on its host, photographed by Giles San Martin

Three families with a similar appearance—Streblidae, Nycteribiidae, and Mystacinobiidae—are notable here as points of comparison. The former two (sometimes classified as a single family; Petersen et al., 2007) are known as "bat flies", and are louse-like bloodsuckers of bats (duh): nycteribiids are rather more advanced in this respect, being blind, wingless, tiny-headed, and never parting with their hosts (Peterson & Wenzel, 1987); conversely, some streblid bat flies retain their wings and/or sight (Whitaker, 1988). Bat flies are also ovoviviparous (meaning that the female's eggs hatch in utero): yet another adaptation to obligate parasitism (Bequart, 1940). Mormotomyia's mouthparts, though, are unequivocally not designed for puncturing skin—they merely sponge up liquids (van Emden, 1950). Hence, the theory that the terrible hairy fly is a bat ectoparasite can be ruled out.

Mystacinobiids on their host (or, rather, symbiont); photograph by Rod Morris

Perhaps, then, the subject of this post is more comparable to the members of the Mystacinobiidae, another monotypic family of weirdo flies which also happen to be the only eusocial dipterans (Piper, 2007). They are found only in New Zealand, which, aside from wetas and Peter Jackson (you gotta love that country), is inhabited by an endemic species of short-tailed bat that plays host to these flies. Mystacinobia zealandica, however, is not a sanguivore (blood-eater); instead, it subsists on the bats' secretions and excreta (Holloway, 1976). The New Zealand bat fly even spends a good deal of its time off-host: and thus its relationship with the creatures whose "fundiment" (to quote Geoffrey Chaucer) it eats isn't parasitic, but phoretic. Might the terrible hairy fly also be a bat cleaner? Extrapolating from its delicate long-legged habitus, which contrasts with the leathery muscularity of the flies seen above, probably not: the creature is free-living; a dasher-over-rocks, rather than a climber-through-fur (Kirk-Spriggs et al., 2011).

Due to its peculiarity, the classification of Mormotomyiidae has been contentious, being included within two unrelated superfamilies: the Sphaeroceroidea (Austen, 1936; Griffiths, 1972; McAlpine, 1989) or Muscoidea (van Emden, 1950 and Pont, 1980). The two are unrelated, the latter belonging to the Calyptratae (a clade including blowflies, flesh flies, houseflies, etc.) and the former, Acalyptratae: a paraphyletic grab-bag consisting of all ptilinum*-bearing flies tha (aren<'t calyptrates. Study of the female genitalia (those dipterist perverts), by contrast, strongly indicates placement in the Ephydroidea (Acalyptratae; Kirk-Spriggs et al., 2011), along with the very familiar laboratory fruit fly (Drosophilidae): the only ephydroids that so much as superficially resemble the terrible hairy fly would be the bee lice (Braulidae), stocky, mite-like little (1.6 mm.) commensals of honeybees (see drawing below), formerly placed in the Carnoidea (Wiegmann, et al., 2011). Larvae grow up in the honeycomb (Ellis & Nalen, 2010); adults are freeloaders who cling to bees and steal food from their hosts' mouths.

Braula coeca, from John Henry Comstock's A Manual for the Study of Insects (1895)

But now we must return to the terrible hairy fly itself. Its sporadic presence despite repeated searching is probably owed to the fact that rain is required to keep guano amicable to M. hirsuta maggots: and it so happens that the climate of northeastern Kenya is arid (c. 381 mm. of precipitation annually around Ukasi; Wright, 1964), with rain brief and very seasonal (Copeland et al., 2011). Thus, adults only make a brief annual (or semi-annual) appearance, their life-cycle being swiftly carried out while the weather permits, and remaining for the most part within the moist microclimate sustained inside their shaded clefts. It's probable that their eggs are capable of long periods of estivation in the times between life-giving torrents. 

So it is amply demonstrable that the terrible hairy fly is a creature intensively adapted for life in a very specific habitat; and that it cannot survive outside of said habitat. Moreover, the fact that the fly is a delicate creature, ill-shaped for phoresy, means that it is incapable of dispersal to new locales. Dormant eggs being carried off in guano stuck to birds' feet (by analogy to the similar phenomenon among seeds) is probably the only means by which terrible hairy flies could escape their cleft; but even if this happened, the likelihood of those eggs arriving in a hospitable environ remains a long shot. Therefore, it is most likely that the population on Ukasi Hill is the only one on Earth, a deduction confirmed by genetic evidence which also indicates a recent population bottleneck (Copeland et al., 2011). 

Even though M. hirsuta's numbers are good at the moment, the species remains very vulnerable. And whether or not you feel that the terrible hairy fly deserves our protection, I heartily hope that the sight that g reeted their discoverer, H. B. Sharpe—that of the flies drifting gently down from the walls " ... like feathers", borne by their long hair—will remain to be witnessed by humanity (or those members of it who happen to care) for many years to come. 




*The ptilinum is an inflatable sac located in a number of flies' heads (rather like an airbag): it is used to force open the end of the puparium to permit the new adult's eclosion. Afterwards, the ptilinum deflates, withdrawing into the head; a suture above the antennae's bases marks the place where it originated. The flies that bear this suture comprise a monophyletic group called the Schizophora (a subdivision of the infraorder Muscomorpha). 
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Ammopelmatus kelsoensis. (n.d.). Sandra Shanks. Retrieved 12/18/12 from http://www.dfg.ca.gov/biogeodata/cnddb/pdfs/invert/Insects_-_Orthoptera/Ammopelmatus_kelsoensis.pdf

Austen, E. E. (1936). A remarkable semi-apterous fly (Diptera) found in a cave in East Africa, and representing a new family, genus, and species. Proceedings of the Zoological Society of London, 425-431.

Bequart, J. (1940). Moscas parasiticas pupiparas de Colombia y Panama. Acad. Colombiana Cienc. Exac. Fis. Nat., 3, 414-418.

Copeland, R. S.; Kirk-Spriggs, A. H.; Muteti, S.; Booth, W.; and Wiegmann, B. M. (2011). Rediscovery of the "terrible hairy fly", Mormotomyia hirsuta Austen (Diptera: Mormotomyiidae), in eastern Kenya, with notes on biology, natural history, and genetic variation of the Ukasi Hill population [electronic version]. African Invertebrates, 52(2), 363-390. Retrieved 12/18/12 from http://www.africaninvertebrates.org.za/Uploads/8ba3321a-9a13-45e5-aaea-f4de4d15f02e/Copeland_etal_2011_AfrInvertebr_52_2_RediscoveryMormotomyia_LR.pdf

Ellis, J. D. and Nalen, C. M. Z. Bee Louse—Braula coeca Nitzsch. 2010. Retrieved 12/18/12 from http://entomology.ifas.ufl.edu/creatures/misc/bees/bee_louse.htm 


Griffiths, G. C. D. (1972). The Phylogenetic Classification of Diptera Cyclorrhapha, with Particular Reference to the Structure of the Male Postabdomen. The Hague: W. Junk.

Holloway, B. A. (1976). A new bat-fly family from New Zealand (Diptera: Mystacinobiidae). New Zealand Journal of Zoology, 3, 279-301.

Kirk-Spriggs A. H.; Kotrba, M.; and Copeland, R. S. (2011). Further details of the morphology of the enigmatic African fly Mormotomyia hirsuta Austen (Diptera: Mormotomyiidae) [electronic version]. African Invertebrates, 52(1), 145-165. Retrieved 12/17/12 from http://www.africaninvertebrates.org.za/Uploads/bdee00bd-7b45-4a66-aa77-afa03eda1936/kirkspriggs_etal_2011_AfrInvertebr_52_1_Mormotomyia_LR.pdf

McAlpine, J. F. (1989). Phylogeny and classification of the Muscomorpha. In Borkent, A.; McAlpine, J. F.; Wood, D. M.; and Woodley, N. E. (eds.), Manual of Nearctic Diptera, vol. 2. Ottawa: Agriculture Canada , Biosystematics Research Center, monograph 28, pp. 1069-1072.

Piper, R. (2007). Extraordinary Animals: an Encyclopedia of Curious and Unusual Animals. Westport: Greenwood Publishing Group. 

Pont, A. C. (1980). Superfamily Muscoidea. 81. Mormotomyiidae. In Crosskey, R. W. (ed.), Catalogue of the Diptera of the Afrotropical Region. London: British Museum (Natural History), p. 713.

Petersen, F. T.; Meier, R.; Kutty, S. N.; and Wiegmann, B. M. (2007). The phylogeny and evolution of host choice in the Hippoboscoidea (Diptera) as reconstructed using four molecular markers. Molecular Phylogenetics and Evolution, 45(1), 111-112. 

Peterson, B. V. and Wenzel, R. L. (1987). Nycteribiidae. In McAlpine, J. F.; Peterson, B. V.; Shewell, G. E.; Teskey, H. J.; Vockeroth, J. R.; and Wood, D. M. (eds.), Manual of Nearctic Diptera, vol. 2, Minister of Supply & Services, Ottawa, monograph 28, pp. 1283-1301. 

Van Emden, F. I. (1950). Mormotomyia hirsuta Austen (Diptera) and its systematic position. Proceedings of the Royal Entomological Society of London (B), 19, 121-128.

Whitaker, J. O. (1988). Collecting and preserving ectoparasites for ecological study. In Kunz, J. H. (ed.), Ecological and Behavioral Methods for the Study of Bats. Washengton: Smithsonian Institution Press, pp. 459-675.

Wiegmann, B. M.; Trautwein, M. D.; Winkler, I. S.; Barr, N. B.; Kim, J.; Lambkin, C.; Bertone, M. A.; Cassel, B. K.; Bayless, K. M.; Heimberg, A. M.; Wheeler, B. M.; Peterson, K. J.; Pape, T.; Sinclair, B. J.; Skevington, J. S.; Blagoderov, V.; Caravas, J; Kutty, S. N.; Schmidt-Ott, U.; Kampmeier, G. E.; Thompson, F. C.; Grimaldi, D. A.; Beckenbach, A. T.; Courtney, G. W.; Friedrich, M.; Meier, R.; and Yeates, D. K. (2011). Episodic radiations in the fly tree of life. Proceedings of the National Academy of Sciences, United States, 108. 

Wright, J. B. (1964). Geology of the Ndeyini Area. (Report #69.) Ministry of Natural Resources, Geological Survey of Kenya. Nairobi: Government Printer.