SMITHSONIAN

MISCELLANEOUS COLLECTIONS

VOL. 141

"EVERY MAN IS A VALUABLE MEMBER OF SOCIETY WHO, BY HIS OBSERVATIONS, RESEARCHES,
AND EXPERIMENTS, PROCURES KNOWLEDGE FOR MEN"—JAMES SMITHSON

(Publication 4470)

CITY OF WASHINGTON
PUBLISHED BY THE SMITHSONIAN INSTITUTION
1961

PORT CITY PRESS, INC.
BALTIMORE, MD., U. S. A.

The Smithsonian Miscellaneous Collections series contains, since the suspension in 1916 of the Smithsonian Contributions to Knowledge, all the publications issued directly by the Institution except the Annual Report and occasional publications of a special nature. As the name of the series implies, its scope is not limited, and the volumes thus far issued relate to nearly every branch of science. Papers in the fields of biology, geology, anthropology, and astrophysics have predominated.

Leonard Carmichael,
Secretary, Smithsonian Institution.

SMITHSONIAN MISCELLANEOUS COLLECTIONS

VOLUME 141 (WHOLE VOLUME)

THE BIOTIC ASSOCIATIONS OF
COCKROACHES

(With 37 Plates)

By

LOUIS M. ROTH

AND

EDWIN R. WILLIS

Pioneering Research Division, United States Army
Quartermaster Research and Engineering Center
Natick, Mass.

(Publication 4422)

CITY OF WASHINGTON
PUBLISHED BY THE SMITHSONIAN INSTITUTION
DECEMBER 2, 1960

PL. 1
Blaberus craniifer, c. X 2. 1. (Photograph by Jack Salmon, Philadelphia Quartermaster Depot.).

SMITHSONIAN MISCELLANEOUS COLLECTIONS

VOLUME 141 (WHOLE VOLUME)

THE BIOTIC ASSOCIATIONS OF
COCKROACHES

(With 37 Plates)

By

LOUIS M. ROTH

AND

EDWIN R. WILLIS

Pioneering Research Division, United States Army
Quartermaster Research and Engineering Center
Natick, Mass.

(Publication 4422)

CITY OF WASHINGTON
PUBLISHED BY THE SMITHSONIAN INSTITUTION
DECEMBER 2, 1960

THE LORD BALTIMORE PRESS, INC.
BALTIMORE, MD., U. S. A.

[FOREWORD]

People having only casual interest in insects usually express amazement when they learn how much is known about this most numerous group of animals. However, while entomologists have good reason to take pride in the accomplishments of their contemporaries and predecessors, they are more likely to be appalled by how much remains to be learned. We are indeed ignorant of even the identity of fully half and probably much more than half the total number of insect species. Of those that have been described, we have reasonably complete information about the behavior and basic environmental relationships for only a comparative few. The great majority of the remainder are known only from specimens found in museum collections. Such information as we have about these species usually amounts to no more than date and locality of collection.

This is true of the cockroaches, which now include approximately 3,500 described species. Conservative estimates based on partially studied museum collections and the percent of new species found in recent acquisitions, particularly from tropical and subtropical countries, indicate that at least 4,000 species remain unnamed. Although the group is well known in general terms to nearly all entomologists, there is an almost complete void of information about all except the few domestic species and, to a progressively diminishing degree, some 400 others. Many details about the lives of even those that share man's habitations are not fully understood. This then is a rough measure of how little is known about cockroaches.

With the exception of mosquitoes and a few other comparatively small groups of insects on which work has been concentrated, it is doubtful if any other comparable segment of the world's insect fauna is better known. Already an estimated 800,000 kinds of insects have been described, and since this figure is generally regarded as less than half the actual total, think what this means in terms of knowledge yet to be assembled. No wonder entomology is a growing science with a promising future, but the magnitude of the task also presents a serious obstacle to progress. Progress can continue only if the scattered literature resulting from the diversified labors of hundreds of contributors is brought together and summarized in thorough and well-organized compilations that can serve as a solid basis for future research.

The present work is such a compilation, for it assembles what has been gleaned from approximately 1,700 sources, including correspondence with a large number of other workers. Original observations during some eight years of concentrated effort in U. S. Army Quartermaster research laboratories are a valuable supplement to what others have done, and with this background of experience the authors are especially well qualified to appraise previous work. Seldom has a compilation been done so thoroughly or a single large group of insects been the subject of such uninterrupted effort.

The contents gives the categories of subject matter treated and the introduction discusses the value of this assembled information and offers suggestions for future study. No longer are cockroaches regarded only as disagreeable pests; many species appear to be important, actually or potentially, as carriers of disease. Recognition of this importance has grown considerably, even in the period since World War II. Consequently, anything that increases our knowledge of the basic bionomics of cockroaches will be consulted widely for factual information and for clues to new approaches.

In spite of this extensive compilation, the limitations of present information about cockroach bionomics must be kept in mind. The cited observations of many writers were fragmentary, or their conclusions disagreed. But it is fundamental to scientific inquiry that we should know and attempt to evaluate the results of previous study, and that is what Drs. Roth and Willis have done. Fortunately, their review is readily available. Sometimes, a piece of work fails to be of maximum value because the results are not generally accessible to later students. For this reason I am especially glad that the Smithsonian Institution, by disseminating the results of the authors' labors, has this opportunity to exercise one of its traditional functions—that of diffusing knowledge.

Throughout the period of research by Drs. Roth and Willis at Natick, I was in frequent correspondence with them, and I admire their many accomplishments. Our warmest commendations should go not only to them personally but also to those in administration who encouraged their fundamental research and who aided in the financial support of this publication.

Ashley B. Gurney
Entomology Research Division
United States Department of Agriculture

[CONTENTS]

Page
Foreword[iii]
List of Plates[vii]
List of Illustrations[viii]
I.Introduction[1]
Historical[2]
Methods[4]
Future work[5]
Illustrations[7]
II.Species of cockroaches[7]
III.Ecological relationships[14]
Cave habitats[16]
Cavernicolous cockroaches[17]
Cockroaches from burrows[23]
Desert habitats[25]
Desert cockroaches[27]
Aquatic habitats[30]
Amphibious cockroaches[31]
Outdoor habitats[33]
Cockroaches from outdoor habitats[35]
Structural habitats[70]
Land-based structures[73]
Cockroaches associated with land-based structures[74]
Ships[82]
Cockroaches associated with ships[85]
Aircraft[87]
Cockroaches associated with aircraft[88]
IV.Classification of the associations[91]
V.Mutualism[96]
Bacteroids[96]
Cockroaches in which bacteroids have been found[99]
Bacteria[100]
Protozoa[101]
VI.Viruses associated with cockroaches[103]
VII.Bacteria associated with cockroaches[104]
VIII.Fungi and yeasts[127]
Fungi associated with cockroaches[129]
IX.Higher plants associated with cockroaches[139]
Damage to plants by cockroaches[162]
X.Protozoa associated with cockroaches[166]
XI.Helminths associated with cockroaches[190]
Helminths for which cockroaches serve as primary hosts[192]
Helminths for which cockroaches serve as intermediate hosts[203]
Helminths whose eggs have been carried by cockroaches[208]
XII.Arthropoda associated with cockroaches[210]
Arachnida[211]
Chilopoda[222]
Insecta[224]
Hymenoptera[234]
Predators and parasites of cockroach eggs[234]
Host selection by egg parasites[254]
Cockroach-hunting wasps[255]
Ants predaceous on cockroaches[266]
XIII.Vertebrata associated with cockroaches[268]
Pisces[268]
Amphibia[269]
Reptilia[272]
Aves[276]
Mammalia[283]
XIV.Checklist of cockroaches and symbiotic associates[290]
XV.Cockroaches as commensals[310]
Hosts of commensal cockroaches[310]
Checklist of commensal cockroaches with their hosts[315]
Obscure associations[316]
XVI.Cockroaches as predators[319]
Interspecies predation[319]
Intraspecies predation[322]
XVII.Associations among cockroaches[324]
Familial associations[325]
Gregariousness[330]
Intraspecies fighting[336]
Interspecies compatibility[337]
Interspecies antagonism[341]
XVIII.Defense of cockroaches against predators[343]
XIX.The biological control of cockroaches[348]
Invertebrates[349]
Vertebrates[353]
Acknowledgments[354]
References[356]
Index[441]

[LIST OF PLATES]

Plate Page
1 Blaberus craniifer, c. X 2. 1. (Photograph by Jack Salmon, Philadelphia Quartermaster Depot.). [a]
2 Blaberus craniifer, nymph. (Photograph by Jack Salmon.) [A-3]
3 Blaberus giganteus, c. X 2.2. (Photograph by Jack Salmon.) [A-4]
4 Blatta orientalis, c. X 3.8. A, Male. B, Female. (Photographs by Jack Salmon.) [A-5]
5 A-B, Blattella germanica, c. X 5.2. A, Male. B, Female.
C-D, Blattella vaga, c. X 5.2. C, Male. D, Female with oötheca. 		[A-6]
6 Byrsotria fumigata, c. X 2. A, Brachypterous male. B, Macropterous male. C, Female. [A-7]
7 A and B, Cariblatta lutea minima, X 10. A, Male. B, Female with partly formed oötheca. C, Ectobius pallidus, female with completely formed oötheca, X 8. (C, From Roth and Willis [1957].) [A-8]
8 A, Cryptocercus punctulatus, c. X 4.6. (Photograph by Jack Salmon.) B, Panesthia australis, X 2.8. [A-9]
9 Cutilia sp. near sedilloti, c. X 5. A, Male. B, Female. [A-10]
10 Diploptera punctata, c. X 5. A, Male. B, Female. [A-11]
11 Eurycotis floridana, c. X 2.8. A, Male. B, Female. (Photographs by Jack Salmon.) [A-12]
12 A-B, Gromphadorhina portentosa, c. X 1.5. A, Male nymph. B, Adult female. C, Coleolaelaps (?) sp., a mite from G. portentosa, c. X 32. (Glycerine jelly preparation and photograph of C by Dr. Barbara Stay.) [A-13]
12A Ischnoptera deropeltiformis, c. X 5.3. A, Male. B, Female. [A-14]
13 Leucophaea maderae, c. X 2.2. A, Male. B, Female. (Photographs by Jack Salmon.) [A-15]
14 Nauphoeta cinerea, c. X 3.4. A, Male. B, Female. [A-16]
15 Neostylopyga rhombifolia, c. X 3.4. A, Male. B, Female with partially formed oötheca. [A-17]
16 Panchlora nivea, X 4.5. A, Dead individual showing normal, pale green coloration. B, Dead individual showing the bright red coloration (very dark areas) characteristic of infection with Serratia marcescens. C, Living male. D, Living female. [A-18]
17 A, Parcoblatta pensylvanica, female with completely formed oötheca, X 4. B, Parcoblatta virginica, female with partly formed oötheca, X 7.3. [A-19]
18 Parcoblatta uhleriana, c. X 5.5. A, Male. B, Female with oötheca. [A-20]
19 Periplaneta americana, c. X 3. A, Male. B, Female. (Photographs by Jack Salmon.) [A-21]
20 Periplaneta australasiae, c. X 3.2. A, Male. B, Female. (Photographs by Jack Salmon.) [A-22]
21 Periplaneta brunnea, c. X 2.9. A, Male. B, Female. [A-23]
22 Periplaneta fuliginosa, c. X 2.9. A. Male. B. Female. [A-24]
23 Platyzosteria novae seelandiae, c. X 2.9. A. Male. B, Female with oötheca. [A-25]
24 Pycnoscelus surinamensis, c. X 3.7. A, Male from Hawaii. B, Macropterous parthenogenetic female from Florida. C, Brachypterous nonparthenogenetic female from Hawaii. D, Late instar nymph. (Photograph of nymph D, by Jack Salmon.) [A-26]
25 Supella supellectilium, c. X 6.3. A, Male. B, Female. [A-27]
26 Bacteroids from Blattella germanica. A, Part of abdomen showing mycetocytes in fat body, X 225. B, Lobe of fat body showing 3 mycetocytes, X 750. C, Single mycetocyte; bacteroids appear hollow as result of fixation in Carnoy's fluid, X 1725. D, Smear of fat body showing bacteroids in various stages, X 1800. (All preparations and photographs through the courtesy of Dr. Marion A. Brooks.) [A-28]
27 Fungi parasitic on cockroaches. A, Herpomyces arietinus growing on antennae, legs, body, and cerci of a nymph of Parcoblatta virginica, X 7. B, Herpomyces stylopygae on antenna of Blatta orientalis, X 35. (Reproduced from Richards and Smith [1955, 1956].) C, Herpomyces sp. [probably H. stylopygae] on antenna of B. orientalis, X 132. (Photographs B and C through the courtesy of Dr. A. G. Richards.) [A-29]
28 A-B, Gregarines (Diplocystis sp.?) from Blaberus craniifer. A, Organisms removed from intestine, X 50. B, Organisms removed from hemocoele, X 32. C, Gregarine cysts in feces of Leucophaea maderae, X 12. [A-30]
29 A, Undetermined mermithid that parasitizes Ectobius pallidus. X 9. The worm has partly emerged from the neck region of the cockroach. (Reproduced from Roth and Willis [1957].) B, Undetermined gordian worm that parasitized Eurycotis floridana shown beside its host, X 1.8. (Specimen courtesy of Dr. T. Eisner.) [A-31]
30 A, Heteropoda venatoria, a cockroach-hunting spider, slightly less than natural size, on bananas. (Reproduced from a Kodachrome transparency through the courtesy of Dr. B. J. Kaston.) B to E, Lycosa sp. (avida?) capturing and feeding on a nymph of Supella supellectilium in the laboratory, X 1.4. [A-32]
31 The centipede Scutigera coleoptrata capturing and feeding on cockroaches in the laboratory. A to E, Pursuit, capture, and eating of a nymph of Supella supellectilium, c. X 1.2. F, Centipede feeding on adult of Blattella germanica, X 1.8. [A-33]
32 The mantid Hierodula tenuidentata (?) devouring a nymph of Periplaneta australasiae, c. X 1.5. [A-34]
33 A, Prosevania punctata ♂ beside an oötheca of Periplaneta americana, X 5. B, Hyptia harpyoides with oötheca of Parcoblatta uhleriana from which it had emerged, X 5. C, Larva of a lampyrid beetle feeding on Parcoblatta virginica in the laboratory, X 4. [A-35]
34 Chalcid parasites of cockroach eggs. A, Anastatus floridanus ovipositing into an oötheca which is still being carried by Eurycotis floridana, c. X 4. B, Comperia merceti ovipositing into an oötheca of Supella supellectilium, c. X 13. C, Tetrastichus hagenowii ovipositing into an oötheca of Periplaneta americana, c. X 10. (C from Roth and Willis [1954b].) [A-36]
35 A, The wasp finds a cockroach. B, She stings the prey in the thorax. C, She then leads the disabled cockroach (antennae clipped) to her nest. D, The wasp's egg was placed on the coxa of the cockroach's right mesothoracic leg where it hatched. E, Portion of the host's abdomen removed to show feeding larva. F, New adult wasp emerging from dead host. (Reproduced from F. X. Williams [1942] from the color paintings of the late W. Twigg-Smith, through the courtesy of F. A. Bianchi.) [A-37]
36 Chemical defense of Diploptera punctata against predators; the spray pattern is displayed on KI-starch indicator paper. A, Spray pattern after right mesothoracic leg was pinched. B, Cumulative spray pattern after left mesothoracic leg of the same insect was pinched. C, The defensive glands of the cockroach on the left had been excised, and it is under persistent attack by ants from a laboratory colony of Pogonomyrmex badius (Latreille). The intact cockroach on the right was also attacked by the ants, but it discharged a spray of quinones and repelled the attackers. (From Eisner [1958], through the courtesy of Dr. T. Eisner.) [A-38]

[LIST OF FIGURES]

Fig. Page
1 Diagram illustrating the relationship between a mature plant of Herpomyces stylopygae and the integument of Blatta orientalis. (Reproduced from Richards and Smith [1956], through the courtesy of Dr. A. G. Richards.) [128]
2 Representative Protozoa associated with cockroaches. A, Monocercomonoides melolonthae, X 3094 (after Grassé). B, Coelosporidium periplanetae, X 1310 (after Sprague); trophozoite with spores and chromatoid bodies. C, Endamoeba blattae, X 273 (after Kudo); trophozoite. D, Lophomonas striata, X 330 (after Kudo). E, Lophomonas blattarum, X 660 (after Kudo). F, Retortamonas blattae, X 3094 (after Wenrich). G, Nyctotherus ovalis, X 175 (after Kudo). H, Gregarina rhyparobiae, c. X 52: mature trophozoite attached to intestinal wall of Leucophaea maderae. (Redrawn from J. M. Watson [1945].) I, Diplocystis schneideri, c. X 14.4 (after Kunstler). J, Gregarina blattarum, c. X 57 (after Kudo). K, Protomagalhaesia serpentula, X 36 (after Pinto). L, Gamocystis tenax, magnification not known (after Schneider). (All figures except H redrawn from Kudo [1954] after sources indicated.) [168]
3 Protozoa from the gut of the wood-feeding cockroach Cryptocercus punctulatus. A, Eucomonympha imla, female above, male below, c. X 375. (From Cleveland [1950c].) B, Barbulanympha sp. (From Cleveland [1953].) C, Urinympha talea, c. X 712. (From Cleveland [1951a].) D, Rhynchonympha tarda, c. X 450. (From Cleveland [1952].) E, Trichonympha okolona or T. algoa, c. X 390. (From Cleveland [1949].) (All drawings reproduced through the courtesy of Dr. L. R. Cleveland.) [175]
4 The cockroach mite, Pimeliaphilus podapolipophagus. (From Baker et al. [1956]; reproduced through the courtesy of Dr. E. W. Baker and the National Pest Control Association.) [221]
5 Evania appendigaster. Left, dorsal view, X 8. Right, side view, X 5. (Reproduced with permission. British Museum [Natural History], 1951, figs. 1A and 1B.) [238]
6 Ampulex canaliculata attacking Parcoblatta virginica. A, Female wasp stinging her prey, c. X 4.8. B, Wasp's egg attached to the coxa of the mesothoracic leg of the cockroach. C, Larva of A. canaliculata (about three-quarters grown) feeding on the internal organs of the host from the exterior, c. X 4. (Reproduced from F. X. Williams [1929], through the courtesy of Dr. F. X. Williams and F. A. Bianchi, Hawaiian Sugar Planters' Association.) [258]
7 Cockroach-hunting wasps. A, Dolichurus stantoni leading a nymph of Blattella lituricollis to her nest, c. X 4. (Reproduced from F. N. Williams [1919].) B, Podium haematogastrum attaching her egg to an Epilampra sp. while on the side of a termite mound that contains the wasp's nest, c. X 1.6. C, Epilampra sp. parasitized by P. haematogastrum showing the wasp's egg attached to the right fore coxa, c. X 3.2. (B and C reproduced from Williams [1928], through the courtesy of Dr. F. X. Williams and F. A. Bianchi.) [263]

THE BIOTIC ASSOCIATIONS OF COCKROACHES[1]

By Louis M. Roth and Edwin R. Willis[2]

Pioneering Research Division, United States Army
Quartermaster Research and Engineering Center
Natick, Mass.

(With 37 Plates)

With most of us collectors the life history of an insect begins in the net and ends in the bottle.

Hanitsch (1928)

[I. INTRODUCTION]

Recently we brought together much of the literature linking cockroaches with the transmission of certain organisms that cause disease in man and other vertebrates. In that paper (1957a) we concluded that cockroaches, being potential vectors of pathogenic agents, should not be regarded simply as minor annoyances. Obviously the associations of cockroaches with agents of vertebrate diseases are of more immediate importance than their relations with pathogens of lower animals or with nonpathogens. On the other hand, cockroaches are of general economic as well as medical importance, and their control is sought by many who are unaware of their medical significance. That the control of domiciliary cockroaches is far from satisfactory may be inferred from current entomological and pest-control journals in which new insecticides are continually advocated to replace others found to be inadequate. Possibly new approaches to the control of cockroaches are needed. Whether these lie in the direction of increased use of parasites and predators for the biological control of these insects remains to be seen. In any event, the more we know about any insect, especially its ecology, the greater the likelihood of achieving satisfactory control. In order to advance knowledge in any field of science, new research should proceed from the results of prior investigations when these exist. We hope that the observations and experiments cited herein may suggest areas for future research and exploitation.

To the best of our knowledge no previous publication has brought together the vast literature on the parasites, predators, commensals, and other symbiotic associates of the Blattaria. For this reason, we have tried to assemble observations on all such known associations. Undoubtedly we have overlooked some records, as, for example, those buried in papers dealing with other phases of cockroach biology. We hope that such inadvertent omissions will not seriously impair the usefulness of this compilation. Whatever its defects, this review should be a unified source of information for all who are interested in the biotic associates of cockroaches.

In addition to previously published information, this monograph also contains original records and observations on the associations of cockroaches that are reported here for the first time. Although some of the observations were made by us, others were made by colleagues who have graciously made their knowledge available to us in private communications.