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

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.

HISTORICAL

Chopard (1938) in his book La Biologie des Orthoptères reviewed much of the literature on cockroaches, but of the many biotic associations that exist he discussed only the commensal cockroaches, gregariousness, and familial associations. Asano (1937), who reviewed the natural enemies of cockroaches, mentioned about 10 groups of animals that attack cockroaches. Thompson (1951) in his Parasite Host Catalogue, which was based mainly on papers abstracted or noted in the Review of Applied Entomology, listed only 19 insect parasites of cockroaches. Eighteen of these were Hymenoptera which attack only cockroach eggs; the single dipteron listed (Sarcophaga lambens Wiedemann, supposedly parasitic on Pycnoscelus surinamensis) is not a parasite in this case, but deposits its eggs on the dead insects (see p. 229). Cameron (1955) listed as parasites and predators of the cockroach 24 species of hymenopterous egg parasites, 7 species of Ampulex which hunt nymphs and adults, 17 Protozoa, 13 nematodes, 5 bacteria, 2 mites, and a few other miscellaneous predators. In his classified list of the protozoan parasites of the Orthoptera of the world, Semans (1943) listed about 26 species from cockroaches. Linstow (1878, 1889) recorded 14 species of helminths from cockroaches. Van Zwaluwenburg (1928) listed 33 names of roundworms which are commensals or secondary parasites of cockroaches, but some of these names are synonyms. La Rivers (1949) extended this list with 13 additional species. Chitwood (1932) recognized 24 species of nematodes which are primary parasites (probably commensals) of blattids. Steinhaus (1946) gave many instances of biological relationships between cockroaches and bacteria, fungi, and yeasts, but the cockroaches were not discussed as an entity and the information is scattered throughout the book.

In surveying the literature on this subject we have collected a far more extensive list of animals and plants associated with cockroaches than one might have expected from an examination of any one of the previous papers on this subject. In our review of the medically important organisms associated with the Blattaria, we pointed out that in addition to many experimental associations cockroaches have been found to harbor, naturally, 4 strains of poliomyelitis virus, about 40 species of pathogenic bacteria, the eggs of 7 species of pathogenic helminths, and to serve as intermediate hosts of 12 other species of helminths pathogenic for vertebrates; cockroaches have also been found to carry, on occasion, 3 species of Protozoa that are pathogenic to man and 2 species of fungi which are sometimes found associated with pathological conditions.

In addition to the above organisms of medical importance, we have compiled records of other organisms, nonpathogenic to vertebrates, which are naturally associated in some way with cockroaches. None of the following numbers can be considered absolute because some names may be synonyms. However, we believe that these figures are very close to the actual numbers of species that have been isolated because we have attempted to refer all obvious synonyms to the currently accepted name for each organism. On this basis there are about 45 species of bacteria, 40 fungi, 6 yeasts, 90 Protozoa, and 45 helminths that have been found associated naturally with cockroaches. Of the arthropods there are about 2 species of scorpions, 4 spiders, 15 mites, 4 centipedes, and 90 insects. Of vertebrates there are 4 species of fish, 16 amphibians, 12 reptiles, 20 birds, and 27 mammals. Besides these there are many records of experimental associations that have been contrived in the laboratory.

Some idea of the increase in our knowledge of the biotic associations of cockroaches, during the last 70 years, may be gathered from a comparison of the above figures with those of Miall and Denny (1886) who presented "...a long list of parasites which infest the Cockroach." This list included 2 bacteria, 6 Protozoa (some of the names are synonyms), 7 nematodes (some of these names are also synonyms), 1 mite, 1 wasp, and 1 beetle. In addition, they mentioned as other foes of the cockroach: monkeys, hedgehogs, polecats, cats, rats, birds, chameleons, and frogs.

METHODS

We have listed the organisms known to be associated with cockroaches systematically by phylum, class, order, and family. Within each family the organisms are listed alphabetically by genus and species. Under each organism the associated cockroaches are listed as natural or experimental hosts, vectors, or prey. Identified cockroaches are listed by the currently accepted name. Unidentified cockroaches are indicated by the word "Cockroaches." The name of each cockroach is followed by the country in which the observation was made, the authority for the record, and with a few exceptions[3] pertinent biological information, where this is known. Question marks following the names of organisms or countries indicate tentative or questionable identifications.