Ann. Rev. Entomol 1979. 24:449-73 Copyright @ 1979 by Annual Reviews Inc. All rights reserved

BIOLOGY OF THE BRUCHIDAE +6178

B. J. Southgate

Biology Department, Pest Infestation Control Laboratory, Ministry of Agriculture, Fisheries, and Food, Slough SL3 7HJ, Berks, England

INTRODUCTION

Species of Bruchidae breed in every continent except Antarctica. The larg­ est number of live in the tropical regions of Asia, Africa, and Central and South America. Many species have obvious economic importance because they breed on grain legumes and consume valuable proteins that would otherwise be eaten by man. Other species, however, destroy seeds of an immense number of leguminous trees and shrubs, which, though they have no obvious economic value, stem the advance of the deserts into the marginal cultivated areas of the world. When this ecosystem is mismanaged by practices such as over­ grazing, then any organism that restricts the normal regeneration of seed­ lings will, in the long run, affect agriculture adversely. This has been demonstrated recently in some African and Middle Eastern semiarid zones (65). The present interest in the management of arid areas and in the introduc­ Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org

Access provided by Copyright Clearance Center on 11/01/20. For personal use only. tion of alternative tree species to provide timber, fodder, or shade has stimulated a detailed study of the ecology of some leguminous trees and shrubs that has revealed some deleterious effects of bruchid on the seeds of these plants (42, 43, 59). It has also emphasized the inadequacy of our knowledge of the and biology of these beetles. Simulta­ neously there has been a move to improve grain legume crops by breeding varieties that give heavier yields and are resistant to the pests and diseases that devastate current varieties. Thus ecologists, biochemists, agronomists, and plant breeders are already cooperating, and I hope this review will encourage entomologists to study the Bruchidae to gain a greater under­ standing of their ecology.

449 0066-4170/79/0101-0449$01.00 450 SOUTHGATE

THE TAXONOMIC STRUCTURE OF THE FAMILY BRUCHIDAE

The family Bruchidae at present consists of approximately 1300 species, grouped into 56 genera placed within 5 subfamilies. It is placed by most authorities in the superfamily Chrysomeloidea, and although some detect affinities with the Curculionoidea, Crowson (31), in particular, argues against that view. It comprises five subfamilies, Amblycerinae, Bruchinae, Eubaptinae, Kytorhininae, and Pachymerinae, as definedby Bridwell (15). To these, Luk'yanovich & Ter-Minasyan (68) add the subfamily Rhaebinae, represented by a single genus Rhaebus. Bridwell had excluded this although he had seen no specimens of it. In my opinion it fits into the Bruchidae, although it has some affinities with the Chrysomelidae. Its larvae develop within fruiting bodies, and although not of taxonomic significance, it is similar to the Bruchidae. Bottimer (10) accepted its exclusion, but Crowson (31) notes that it has close affinities with the Bruchidae and infers that it should be placed in the family. From the time of Linneaus up to the early 1900s, interest in the Bru­ chidae was limited to the description of considerable numbers of new spe­ cies, which were usually designated Bruchus. Bridwell (16), who made the first serious study of classification, constructed a key based on adult mor­ phology to the genera of bruchids found in America north of Mexico. Pfaffenberger& Johnson (75) made a limited generic classification based on larval morphology, especially on the presence or absence of ocelli and on the development of legs in the mature larvae, but they made no attempt to show any biological significance in these structures. At species level, the New World species have been extensively studied. Johnson and Kingsolver and co-workers (53, 56, 58, 100) have each as­ signed numerous species to genera that had been designated Bruchus by early workers such as Sharp. Less has been done on Old World genera such as Bruchidius, but Decelle (33) has separated and defined Conicobruchus

Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org and Tuberculobruchus. Bruchidius remains a heterogeneous group defined Access provided by Copyright Clearance Center on 11/01/20. For personal use only. by Schilsky (84) as having a conical thorax and a single spine on each hind femora. This spine may be almost invisible, or approximately 0.2 mm long. Species of the genus are found in Europe, Asia, and Australia, but King­ solver (62) evidently believes that the Australian species should be placed in some other genera. In my opinion the remaining African species, too, should be reassigned. A problem that arises when active taxonomic studies are in progress, especially in groups that have some economic importance, is the continued use of obsolete names. Applied entomologists are often unaware of new synonymies and of changed opinions about generic status, and names are THE BRUCHIDAE 4S 1

changed after papers are published. Therefore, in this paper I place the original name in parentheses after the currently accepted generic name whenever a species is mentioned, for example. (=Pachymerus) interstinctus.

Biotaxonomy The current interest of biochemists in the chemical composition of legume seeds has provided information that can be correlated with infestation and can generate ideas on the phylogenetic origins of the Bruchidae. Foodstuffs, ecology, and behavior may be adaptive, but they may also have some taxonomic value if they cause divergence of forms. Thus the inclusion of biochemical data about the seeds of many legumes should help the ecologist understand why some seeds are vulnerable to bruchids and how others combat attack, and perhaps gain insight into the evolution of species. Interesting associations occur between host plant groups and bru­ chid subfamilies. Thus the Bruchinae for the most part are associated with the family Leguminosae. whereas the Amblycerinae mostly attack other families (Table 1). The Eubaptineae and Pachymerinae attack mostly non­ leguminous plants. Host specificity of itself is not a valid criterion on which to base taxonomic differentiation. but it is a useful addition to the more conventional methods. Johnson (54) has suggested affinitiesbetween species of Acanthoscelides and Abutiloneus idoneus because they both breed in the Malvaceae. Likewise his analysis of the host relationship of the Acanthosce­ !ides produces some groupings that would not be made from a purely morphological analysis. Janzen (48) suggests that host species divergence is based less on physical characteristics. such as the seed type, pod structure, and shape or nature of the seed coat, than on nutritional characteristics of the seed. This hypothesis has been examined only for a few New World genera and could well be extended to the Old World. Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org

Access provided by Copyright Clearance Center on 11/01/20. For personal use only. GEOGRAPHICAL DISTRIBUTION

The early bruchid taxonomists lumped all the species into a few large genera, so no distribution pattern could be discerned. Now that our in­ creased knowledge enables us to differentiate the species into more distinct genera, it is evident that except for the very few species dispersed by commerce, almost all the genera are limited to either the Old or the New World. Bottimer (10) admirably defines the five subfamilies comprising the Bru­ chidae, along with the seven tribes into which two of the subfamilies are split. About three quarters of the genera are still placed in the subfamily 452 SOUTHGATE

Table 1 Plant families other than Leguminosae attacked by Bruchidaca

Bruchidae

Subfamily Tribe Genus Plant family attacked / Amblycerinae Amh/ycerus Anacardiaceae (51) Boraginaceae (51, 102) Euphorbiaceae (51) Malpighiaceae (51) Malvaceae (51) Nyctaginaceaeb Sterculiaceae (55) Tileaceae (61) Verbeneaceae (61) Vitaceae (57) Spermophagus Boraginaceae (102) Convolvulaceae (2, 45, 102) Malpighiaceae (102) Malvaceae (88, 102)

Bruchinae Acanthoscelidini Ahutiloneus Malvaceae (16) Acanthoscelides Anacardiaceae (18) Cistaceae (54) Lythraceae (54) Malvaceae (25,54) Onagraceae (54) Rhamnaceae (54) Sterculiaceae (55) Tiliaceae (51)

Althaeus Malvaceae (16)

Bonaerius Malvaceae (17)

Caryedes Euphorbiaceae (102)

Cosmobruchus Asteraceae (14)

Dahlibruchus Asteraceae (14)

Lithraeus Anacardiaceae (18)

Neltumius Rhamnaceae (25)

Stator Bixaceae (52) Myrtaceae (52)

Bruchidius CistaceaeC

Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org Megacerini Megacerus Convolvulaceae (25) Access provided by Copyright Clearance Center on 11/01/20. For personal use only. Eubaptineae Eubaptus Acanthaceae (95)

Kytorhinineae Kytorhinus Zygophyllaceae (2)

Pachymerinae Caryedon tini Caryedon Apiaceae (� Umbeliferae) (2,89) Combretaceae (78) Pachymerini Pachymerus Palmae (13, 102) Pandanaceae (13)

Caryoborus Palmae (13, 102) Caryobruchus Palmae (13)

Caryotrypes Pandanaceae (36)

a Numbers in parentheses indicate reference. bOata on specimen in the British Museum of Natural History. C B. J. Southgate, unpublished information. THE BRUCHIDAE 453

Bruchinae, which is split into four tribes. Of these, two are exclusively Old World origin, one is exclusively from the New World, and one very large New World tribe, the Acanthoscelidini, has a few Old World species in one genus, as discussed below. The Kytorhininae includes the only other genus not exclusively found in one or the other hemisphere, Kytorhinus, an Old World genus with one American species that has a distribution stretching from Alaska into the midwest. The small subfamily Pachymerinae com­ prises two tribes from the Old World and one from the New. The Eubap­ tinae comprises a single American genus, and the Amblycerinae, which has not yet been divided into tribes, includes three American and one Old World genera. Among the Old World species that have reached the Americas in seeds are those of the successful genus Callosobruchus, and one species of Carye­ don, C. serratus (Olivier). Pests of stored pulses that have spread from South America include Zabrotes sub/asciatus (Bohemann) and Acanthosce­ fides obtectus Say. One record difficultto explain at present is the discovery in West Africa of an undescribed species of Acanthoscelides that breeds on seeds of Indigo/era arrecta in two widely separated regions (79). We do not know if this species is an introduction or a remnant of an ancient link between Africa and South America. One species of Acanthoscelidini [Pseudopachymerina spinnipes Erich. (=Pseudopachymerus lallemanti Marseul)1, a South American species, is found over most of the Mediter­ ranean region and in Africausually associated with Acacia/arnesiana (34). Specialists in Leguminosae accept this plant to be of South American origin, so it is probable that the bruchid was introduced with the seeds, just as Bruchidius ater (Marsham) was introduced into the US with the ornamen­ tal broom Sarothamnus scoparius. Bruchus pisorum (L.), which attacks the growing garden pea, was also introduced into North America and has rea(.;hed pest status in the northwestern US. Recent revisions of New World genera have led to a greater under­ standing of the limitations on distribution of genera arising from host. For Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org

Access provided by Copyright Clearance Center on 11/01/20. For personal use only. example, according to a recent revision by Johnson & Kingsolver (56), the genus Sennius is restricted to Cassia spp. of the Americas, and Stator is restricted mainly to members of the Caesalpinioideae and Mimosoideae indigenous to the New World (58). They also show how some genera spread widely through a continent, with individual species adapting to a variety of plant families. Amblycerus, for example, is found throughout the New WorId and attacks the seeds of 12 plant families (51, 61). In the Old W orId, consideration of distribution has been limited to works describing the spe­ cies found in countries such as the USSR (68), France (45), and India (97). Smaller-scale works have dealt with Algeria (36), Israel (20), Egypt (86), Nigeria (78), and Japan (29). 454 SOUTHGATE

Australia has a very poor bruchid fauna. Kingsolver (62) mentions only 12 species from the region, including that described by Bohemann (7). I doubt if Bruchus quadriguttatus, recorded by Bohemann, is either indige­ nous or a true species. It is possibly synonymous with Bruchus quinquegut­ tatus, a Mediterranean species that breeds in vetch and peas and probably was transported to the region in storage by early mariners. The paucity of bruchids obviously cannot be attributed to the absence of suitable host plants, for the genus Acacia is present in large numbers. However, Evans, Qureshi & Bell (39) have recently analyzed a number of Acacia seeds. Those from Australia differ considerably in the secondary compounds they contain from species grown in other parts of the world. Furthermore, Australian Acacia spp. grown in southernAfrica are immune from attack by bruchids that heavily damage indigenous species, so it is possible that few Australian leguminous plants are susceptible to the Bru­ chidae.

HOST PLANT RELATIONSHIPS

The larvae of Bruchidae feed and develop only in seeds. A record of a Bruchus spp. being bred from bud galls Duvana dependens (DC.) (Anacar­ daceae) (60) and a heresay record of the larvae of an unnamed species living in the stems of an umbelliferous plant (14) are both dubious. Since these beetles breed exclusively in seed, it is essential to collect all possible host plant seed pods to get reliable breeding records and new hosts (9). One of the few bruchids indigenous to Britain is recorded from the flowers of Helianthemum (40). The host of this species is unrecorded, but Helianthemum chamaecistus grows on basic grassland in close proximity to many plants of prostrate legumes, so its flowers may provide a ready source of pollen for the adults, although eggs are not laid on it. I have collected numerous pods of the legumes growing near this plant and have

Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org bred adults from Lotus corniculatus. Access provided by Copyright Clearance Center on 11/01/20. For personal use only. It is evident that the species of Spermophagus are associated with the Convolvulaceae, but a few records (see Table 1) for this genus are associated with other plants families. Srivastava & Bhatia (92) record three Spermo­ phagus spp., S. tesselatus Mots., S. albofasciatus GyU., and S. convolvuli Thunb., that infest seeds of Hibiscus cannabinus, together with an unde­ scribed Spermophagus sp. from okra seeds (Hibiscus esculentus L.). Dutt (38) adds "roselle" Hibiscus sabdarifJa as a host species of S. tesselatus. In Europe, Spermophagus sericeus Geoffr.is known to breed only on seeds of Convolvulus arvensis and Calestegia sepium (L.) Roem & Schult. The host seeds for most species are Leguminosae (Table 2). Some 83 genera of the 482 listed by Hutchinson (47) are attacked. The rest are Table 2 Genera of the Legunimosae recorded as host to the Bruchidaea

Family Genus Family Genus

Caesalpinaceaeb Bauhinia Linn. Fabaceae (cont.) Hedysarum Linn. Caesalpinia Linn. Indigofera Linn. Cassia Linn. Kerstingiella Harms Cercis Linn. Lablab Savi Gleditsia Linn. Lathyrus Linn. Gymnocladus Lam. Lens Moench. Parkinsonia Linn. Lespediza Mich. Piliostigma Hoehst. Lonchocarpus Tamarindus Linn. H. B. &K. Mimosaceae Acacia Mill. Lotus Linn. Albizia Durrazz. Lupinus Linn. Dicrostachys Medicago Linn. Wright & Arnott Mucuna Adans. Inga Scop. Nissolia Jacq. Mimosa Linn. Onobrychis Adans Parkia R. Bf. Orobus Linn.

Pithecellobium Mart. (= Lathyrus Linn.) Prosopis Linn. Oxy tropis DC Fabaeeae Abrus Adans. Pachyrrhizus Rich. Aeschynomene Linn. ex DC. Arachis Linn. Petteria A. Gray Astragalus Linn. Petalostemon Cajanus DC. L. C. R ich. Calopogonium Desv. Phaseolus Linn. Calpurnia E. Mey. Piscidia Linn. Canvalia DC. Pisum Linn. Caragana Lam. Pseudarthria Wright Centrosema Benth. & Arnott Clitoria Linn. Pueraria DC. Colutea Linn. Rhychosia Lour. Coronilla Linn. Robinia Linn. Cracca Linn. Sarothamnus (L.)

(= Tephrosia Pers.) Wimmer = Cy tisus Crotolaria Linn. Linn. Cyamopsis DC. Sesbania Scop. Cytisus Linn. Sophora Linn. Dalbergi Linn. Spartium Linn. Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org Access provided by Copyright Clearance Center on 11/01/20. For personal use only. Desmodium Desv. Sphenostylis Dioc1ea H. B. & K. E.Mey. Dolichos Lam,. Stylosanthes Swartz Eriosema DC. Tephrosia Pers. Errazurizia Phil. Thermopsis R. Br. Erythrina Linn. Trifolium Linn. Galactia P. Br. Ulex Linn. Glycine Linn. Vicia Linn. Glycyrrhiza Linn. Vigna Savi Halimodendron Fisch ex DC. Voandizia Thou.

aThis information has been extracted from the literature and from data labels attached to specimens known to be authentic identification of the host. bFrom the subfamily Caesalpinioideae. The subfamily Brachystegioideae at present has not been recorded as being attacked. 456 SOUTHGATE

recorded from seeds of 24 other families, though for most only a single plant species is associated with one genus (Table 1). Zacher (102) includes 11 other families in his list of hosts, but these have not been confirmed by more recent captures. More species from the New World than from the Old have been recorded from nonleguminous plants. Thus Amblycerus spp. have been bred from 11 other plant families and Acanthoscelides spp. from 5. The American genera Abutiloneus and Bonaerius are each restricted to a single nonleguminous plant. In the Old World Caryotrypes (35) infests Pandanaceae only, whereas in the New World Pachymerus infest Palmae as well. Of the other Old World genera, Caryedon spp. breeds widely in other families. Although they develop principally in Mimosaceae and Ca­ esalpinaceae in Africa and Asia, they also infest Combretaceae in Africa south of the Sahara (78) and the seeds of Ferula and Liseae (Apiaceae = Umbelliferae) in southwestern Asia and the western Mediterranean (2, 68, 89). The variability of seed pod form infested by the Bruchidae indicates the need for further behavioral studies as the situation is complex and by no means clear-cut. The strong association with the main plant family Leguminosae implies that the links are either behavioral or biochemical. Applebaum & Birk (1) and Janzen, Juster & Bell (52) have demonstrated that larval development is controlled mainly by the level of secondary compounds contained in the seed. Bell & Janzen (6) suggested that L-dopa (3,4-dehydroxyphenylalaine) also prevents attack in some seeds. Some bruchid species have devised means of dealing with very large amounts of potentially toxic substances, as demonstrated by Rosenthal, Dalhman & Janzen (81) with Caryedon brasiliensis in the seeds of Dioc/ea megacarpa. Larva of this bruchid develop normally in seeds that contain more than 80/0 (dry weight) L-canavanine. 'Considerable effort has been devoted to the biochemistry of economic crops to develop resistance to damage by bruchids. Working with Calloso­

Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org Roy Bhat (82) examined the levels of trypsin inhibitors Access provided by Copyright Clearance Center on 11/01/20. For personal use only. bruchus chinensis, & in seeds of varieties of Lathyrus sativus, a plant whose seeds are highly susceptible to attack by this . One variety with a low trypsin inhibitor content showed low beetle attack, whereas the varieties with much higher levels were attacked at the 1000/0 level after 75 days. They concluded that a significant correlation existed between trypsin inhibitor content and sus­ ceptibility to insect attack. In a related species of bruchid, , Janzen, Juster & Bell (52) demonstrated that some of the non­ protein amino acids are highly toxic at the 0.1 % level when added to the diet of C maculatus, but L-homarginine is an exception, as low levels (0.10/0) have a salutory effect on the larvae. THE BRUCHIDAE 457

The external covering of the seed plays an important role in protecting the seed from attack. The majority of bruchids lay their eggs externally on the pod, and the young larva has to penetrate the pod wall to reach the seed. Features that might prevent the development of a bruchid larvae within a seed are as follows: (a) The pod, capsule, or seed may be too hard for the newly hatched larva to penetrate; (b) the pod or seed may be physically too small or of an inconvenient shape for the larva to reach full size; (c) the seed or pod may contain too little food to support a larva; (d) the seed may contain toxins or other substances in the cotyledons or its enveloping testa that inhibit the development of larvae; and (e) there may be too few suitable hosts within the region, or seed production may not coincide with the presence of a mature adult. Bridwell (12) experimentally induced Bruchus pruinius to oviposit and breed on seeds of Samanea saman (monkeypod), a plant not normally attacked in the field. Its seeds are surrounded by a syrupy substance not easily penetrated by small larvae. However, the sticky pulp surrounding the seeds of Tamarindus indica (tamarind) is easily penetrated by larvae of Caryedon serratus (01.), and the species has invaded and become estab­ lished in most of the regions to which this tree has been taken by man. When seeds are large enough, one or more seeds within a pod can support more than one larva each, as in the case of Stator limbatus or Status pruinius on Acacia berlandieri (53). On the other hand, a larva may need to use two or more seeds during the course of development, this being achieved by connecting seeds together with a silk tube as recorded by Johnson (53) for Merobruchus julianus Hornon the same host plant. Com­ plete destruction of all the seeds in a single pod of Crotalaria spp. by Bruchidius strangulatus (79) and up to eight seeds of Cassia baubinioides by larvae of Sennius morosus (23) has been recorded. Stored products species apart, and contrary to the opinion of Center & Johnson (24), the size of a bruchid is not correlated with the size of the seed

Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org in which it developed; it is influenced more by the nutritional content of the Access provided by Copyright Clearance Center on 11/01/20. For personal use only. seed and its suitability.

THE DEVELOPMENT OF THE BRUCHID

The life history of the Bruchidae follows that normally exhibited by Co­ leoptera. However, many facets of each individual stage still are not com­ pletely understood. The main areas in which detailed information is particularly lacking are host finding and the flightpattern of adults and the length of larval/pupal period, particularly with reference to prepupal or pupal diapause. The importance of this group in the seed destruction of 458 SOUTHGATE

plants of the arid and semiarid regions makes knowledge of their life history essential if the ecology of these regions is to be fully understood.

The Egg The egg, a flattened ovoid, is protected by a covering excuded at the time of oviposition, which fixes the egg firmly to the substrate. The majority of species attach a single egg directly onto the surface of the pod or seed. The newly hatched larva eating through the egg shell immediately penetrates the wall of the pod or seed to find its food. If oviposition is delayed until the pod has dehisced, eggs may be laid directly on the seed coat. One species, Stator limbatus, lays on the seed of Cercidium floridum by taking advan­ tage of the exit holes made in the pods by amicus (70). Teran (94) figures the two separate "hyaline" covers of the egg of Ca­ ryedes germaine Pic, an unusual species in which the outer cover is smaller in area than the inner one. Presumably this is an adaptation to some peculiarity of its ecology. The shape of the egg varies somewhat. That of Zabrotes subjasciatus Horn is more circular than usual, whereas those of Sennius morosus and Sennius simulans (23) are anchored by strands of secretion radiating from the egg chorion. I have seen the same egg form in Specularius su/caticollis on seeds of Cajanus cajan (pigeon pea). These eggs appear to be vulnerable to physical damage, but this may be unimportant as they hatch very quickly. The majority of the Amblycerinae and Bruchinae lay their eggs singly,

but Pseudopachymerina spinnipes Erichson (= Pseudopachymera lallemanti) lays eggs in clusters along the suture of the pod of Acacia jarnesiana, with some of them overlapping (94). Prevett (78) observed that Caryedon jasica­ tum always laid its eggs on the single seeded pod of Combretum lamprocar­ pum in a group. Since the exposed eggs were invariably attacked by trichogrammatid parasites and the covered one was not, he concluded that this was a protective adaptation against parasites for this species. Exposed Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org

Access provided by Copyright Clearance Center on 11/01/20. For personal use only. eggs also face physical hazards, such as parasites and desiccation. Mitchell (70) states that (Mylabris amicus) also deposits eggs one upon another, but he suggests that it does so only when under stress, estimating that parasites and desiccation together take 80% of the eggs of M. amicus and those that survived were those covered up. Prevett (78) notes that Caryedon albonotatum covers the eggs with fecal material. He found that not a single egg from a sample of 57l laid on pods of Acacia niloticus was parasitized, although evidence indicated minor predation. Some Acanthoscelides spp. do not stick their eggs to the pod or seed. These may lay eggs on a green pod in a hole bitten in the outer tissue (87, 101) or within the dehiscent pod (67, 87), or they may scatter eggs among THE BRUCHIDAE 459

harvested seed, as in Acanthoscelides obtectus. It is essential for the freshly hatched larva to find easily utilizable food close at hand.

The Larvae Since the adult females in the majority of bruchid species attach the egg directly to the seed or pod, the larvae need only to bore through the shell and pod wall to reach food. The emerging larva is furnished with an H-shaped plate of sclerotized chitin. Kunhi Kannan (64) has shown that this plate coupled with the legs and a well-developed anal sphincter enable the first-instar larva to gain leverage in its attempts to make its way out of the egg. The mechanism of eclosion is described by Pfaffenberger& Johnson (75). Most freshly hatched larvae burrow through the pod wall and enter the first available seed. The larvae of some species appear to be more selective and some crawl past several seeds before entering one, but the basis of choice is not known. The point at which the larva penetrates the pod and the construction of the pod may determine the seed to be attacked. For example, the pods of Acacia nilotica are strongly compartmented by septa with a single seed in each compartment. Thus the seed available is the one in the compartment over which the egg is laid. If there are no septa the larvae can, and often do, feed in several seeds or may complete development within a single seed, some two, three, or even four seeds away from the point of entry. Some species always destroy many seeds, as for example Sennius morosus and Sennius simulans in Cassia baubinioides (23), Merobruchus julianus in Acacia berlandieri (53), Conicobruchus (Bruchidius) stran­ gulatus (79) in the green pods of Crotolaria goreensis, Crotolaria comosa, and Crotolaria senegalensis, and Conicobruchuscitricosus in Croto/aria spp. (87). It is not clear if this multiple seed feeding confers any advantage other than ensuring sufficient food for the larva to reach maturity. Center & Johnson (23) suggest that the accumulation of larval silk by Sennius moro­ sus, caused by binding the seeds together, ensures that unattached seeds do

Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org not fall on the forest floor and expose the insect to microbial attack there. Access provided by Copyright Clearance Center on 11/01/20. For personal use only. Janzen (49) reported that bruchids in Scheelea palm seed lying on the ground were killed by pathogens. This risk is greatest in a rain forest habitat. In the semiarid zone in northern Nigeria, the larvae of Caryedon spp. leave pods to pupate beneath the surface of the soil (78). This habit is also alluded to by Skaife (87) for Caryedon (=Pachymerus) interstinctus, but his statement that it forms its cocoon among the undergrowth suggests a superficial pupation site rather than one beneath the surface. An account of how the larva reaches the ground has not been published, but they may well need to drop to the ground on a silken thread, as the majority of the host plants retain the pods on the tree for a considerable period. 460 SOUTHGATE

Larvae that remain within the seed to pupate prepare for adult emergence by eating as close to the surface as possible without actually breaking through, and thus constructing a window of thin outer integument. If the seed pod is of a nondehiscent form, then the larva proceeds to this point and the adult is left to bite its way out from the pod after emerging from the seed. The larvae of those species that leave the seed to pupate do not always migrate to the soil, but spin a cocoon on the outside of the seed, as figured by Bagdasaryan (2) for Caryedon liseae (=Caryedon pal/idus), which feeds in the seed head of Lisea heterocarpa, or within the pod, as in the case of Caryedon serratus in Arachis hypogeae (groundnut).

The Pupae There are three characteristic types of pupation sites: (a) The larva pupates within the larval feeding cell; (b) it constructs a cocoon attached to or within the seed or pod; or (c) it pupates in a cell below ground or among fallen leaf litter. Apart from the economic species there is little published on pupae of bruchids. Most of the crops attacked are Fabaceae, and in the field the pods of these ripen on the plant and then dehisce to scatter the seed. The species of Callosobruchus, Acanthoscelides, and Zabrotes all pupate within a single seed after constructing a window in the testa. Most of the genera known to construct cocoons for pupation are Pachymerinae, but some Old World Bruchinae also do so, such as Bruchidius strangulatus, a species that attacks Crotalaria in West Africa. The time spent in the pupa is relatively short, from 7-28 days for the storage species of Callosobruchus and Acanthoscelides and about 3 weeks for Caryedonserratus bred in groundnuts at 25°C and 60% relative humid­ ity (RH) (76). In the life cycle studies of the related Careydon serratus subsp. palaestinicus on Acacia spirocarpa and Acacia tortilis made by Dona­ haye, Navarro & Calderon (37), the majority of the adults emerged after remaining in the pupal cocoon for 150 days if kept at controlled conditions

Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org of 26°C, 70% RH, whereas at unspecified room temperatures 45 out of a Access provided by Copyright Clearance Center on 11/01/20. For personal use only. total of 86 emerged after 120 days and the remainder entered a prepupal(?) diapause from which they emerged after more than 2 years. Working with the same species, but breeding this insect in Prosopis farcta pods, Belinsky (5) found that a prepupal diapause occurred for 2-3 months at 25°C and 50% RH, and 3-4 months at 30°C and 70%RH. The same behavior possi­ bly occurs in the tropics to enable a species to maintain populations when fresh pods are not available; an intimation of this is made by Skaife (87) for Caryedon (=Pachymerus) interstinctus. I have observed emergence of a species of Tuberculobruchus from pods of Acacia albida 18 months after collection in Ethiopia, but no experimental evidence was available to ascer­ tain the stage at which the arrested development took place. THE BRUCHIDAE 461

The Adult With such a wide-ranging distribution as is found in the Bruchidae, a variety of adult behavioral adaptations are to be expected. Among the paleartic species, the adult spends the winter in hibernation and lays eggs in the spring when a suitable host plant is available. This life-cycle pattern is found among species from the Mediterranean regions and the southern us. Under tropical conditions, the appearance of active adults also depends on the climate and on the host plant being in the suitable stage of growth. Many bruchids require pods to be on the host tree; these appear in the dry season on some and in the rainy season on others. In this situation adult aestivation may take place. Skaife (87) sites the emergence of adults from seed of Acacia horrida from July to October when fresh pods for oviposition are unavailable for a further 4-6months. Detailed knowledge of the behav­ ior of the adult beetle is available for few species other than those attacking grain legumes. Mathwig (69) noted that Amblycerus robinae adults were nocturnally active, whereas the majority of bruchids are most active at the high temperatures most usual around midday in the tropics. Adults can be observed arriving and leaving flower heads. These species are positively phototropic, but the nocturnal activity of A. robinae studied by Mathwig apparently was governed by chemotactic response to the pods for oviposi­ tion. The high humidity probably makes it easier to detect odors from the pods. Too little is known about when these beetles lay eggs and how they choose the site. However, the majority of bruchids are diurnal. I have observed Bruchus rufipes ovipositing on pods of Vida spp. at midday in Yugoslavia and have frequently found Spermophagus sericeus in the Mediterranean region dur­ ing the day on the flower heads of umbelliferous plants, such as Daucus sp., feeding on pollen and copulating. Similar observations have also been made by Bagdasaryan (2) in Armenia for the same species on the flowers of Trigonellajoenum-graecum, Convolvulus arvensis, and Lisaea heterocarpa. Visits to the flowers of Convolvulus arvensis not only enable the beetle to Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org

Access provided by Copyright Clearance Center on 11/01/20. For personal use only. feed on nectar and pollen to enhance maturation, but also bring it close to maturing seed capsules on which it can lay eggs. Adults of Bruchus pisorum also visit pea flowers (Pisum sativum) for pollen feeding prior to oviposition (66).

DAMAGE

The Effect of the Bruchid on the Germinating Seed and Seedling Survival in Noneconomic Species Most of the bruchid species studied have been able to generate exeedingly high levels of infestation even when only one or, at most, two generations 462 SOUTHGATE

were passed on the host. Thus Halevy (43) recorded Bruchidius albosparsus in Israel attacking 64% of Acacia gerrardii subsp. negevensis and 99% of Acacia tortilis subsp. tortilis seeds, respectively. Lamprey, Halevy & Maka­ cha (65) record 95.6 and 99.6% infestation of seeds of A. tortilis subsp. spirocarpa by Bruchidius spadiceus after 1 year in storage in the Serengeti Game Reserve in Tanzania. Wickens (99) records a 51 % infestation of Acacia albida by two species of Bruchidius, B. silaceus and B. spadiceus, in the Sudan, and Mathwig (69) reports 86% destruction of seeds of Gled­ itsia tricanthos by Amb/ycerus robiniae in Kansas. Solbrig & Cantino (88) and Swier (93) give the level of infestation of mesquite (Prosopis ve/utina) in Arizona by bruchids as 70%, some 63% being caused by Algarobius prosopis and the remaining 7% by Mimosestes amicus and Neltumius arizo­ nensis. The effect of seed destruction on the survival of a plant species is of obvious importance, especially where seedlings are subjected to severe cli­ matic stresses and trampling by . No serious study has undertaken to measure the effect of bruchids on germination or subsequent survival of seedlings, apart from the investigation on Acacia raddiana, Acacia gerrardii subsp. negevensis, and Acacia tortilis by Halevy (43), and on A. raddiana and A. tortilis by Karschon (59). These workers have shown that some infested seed germinates in spite of damage to the cotyledons. For example, according to Halevy (43) A. gerrardii had a 64% infestation and 6% germinated, whereas in A. raddiana 72% were infested and I % germinated. Seeds such as some Acacia spp. that have a hard, water-resistant testa and need to pass through the gut of a herbivore, or be subjected to fire or scarification, may benefit from the boring of a first-stage larva. The entry hole of the larva would allow the ingress of water and a little damage to the cotyledon would not hamper germination seriously, provided the seed was not exposed to microorganisms for too long a period. The balance that exists between nongetmination and germination with survival is an ex­ tremely delicate one, and an in-depth knowledge of the ecosystem is re­

Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org quired, as highlighted by Lamprey, Halevy & Makacha (65), if the ecologi­ Access provided by Copyright Clearance Center on 11/01/20. For personal use only. cal balance of the region is to be maintained. It is unfortunate that so little attention has been given to ultimate survival of seedlings of the noncrop legumes. Halevy (43) published figures of the germination rates of unselected seeds of Acacia raddiana over a period of 350 days, but no information is given on the fate of bruchid-infested seeds or on the survival of seedlings. Until information of this nature is available, it is impossible to assess the overall effect of bruchid damage to seed on the environment and the regeneration of forest regions. With cultivated grain legumes (Vigna, Phaseo/us, etc), where many stresses have been removed, the chances that a lightly infested seed will survive are greatly enhanced. Using Pisum sativum infested by Callosobru� THE BRUCHIDAE 463

chus maculatus, M. T. Mahdi (personal communication) has shown that germination is correlated with the number of emergence holes in the seed and with the rate of growth and seedling vigor (i.e. the greater the number of holes, the slower the germination and the greater the reduction in seed­ ling vigor). Booker (8) notes that seeds of Vigna unquiculata with more than three holes have little chance of survival. The size of the seed and the portion remaining after feeding by the bruchid larva determine seedling survival. A single larva of Callosobruchus maculatus, the most widespread of the economic bruchids, infesting a seed of Vigna unquiculata (cowpea) will remove about a quarter of the cotyledon of an average-sized seed. When it infests the smaller seed of Phaseolus radiatus it consumes virtually all of the cotyledons, thereby removing all possible chance of germination by the seed.

Loss Due to Bruchids in Grain Legume Crops Some 20 species belonging to 6 genera attack grain legumes grown, stored, and eaten by man and therefore have been studied more than any of the remaining species (4, 8, 46, 67). One or two of these other species have also been studied in detail to gain ecological knowledge. Pulses grown by man have been infested by Bruchidae since the dawn of agriculture. There is evidence of infestation of lentils (Lens culinarisMed.) fr om the Egyptian Ptolemaic period (19) and of Vida /abae L. in antiquity (85). Nowadays, representatives of the genus Bruchus that attack crops oviposit on the young pod, and larvae feed in the ripening or freshly ripened pods on the plant. One important species of Bruchidius that attacks cow­ peas, B. atrolineatus, does likewise. Adults of these species that emerge fr om seeds after harvest are unable to breed further on these seeds. The remaining economic species belong to the genera Callosobruchus, Acan­ thoscelides, Zabrotes, and Caryedon. All breed successfully in harvested seed. The ability of the storage Bruchinae to pass through many succeeding generations on the same seeds until the food reserves are exhausted is well Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org

Access provided by Copyright Clearance Center on 11/01/20. For personal use only. known, and the amount of damage caused to harvested crops has been well documented (4, 8, 22, 63, 77). Some storage species can attack the crop in the field, but the initial infestation seldom reaches 1-2%, although 7.8 -9.9% has been recorded in the Phillipines (4). Preharvest infestation is very serious because it multiplies dramatically in storage and in 6-8months has reached a level of 80% (22). The present storage species have their origins in populations that infest plants that do not necessarily constitute food for man. In a number of instances the infestation levels of these wild popUlations are comparatively low. Caryedon serratus (01.) is one such species. On its natural hosts of Pilliostigma sp., Cassia sieberiana (DC.), and Tamarindus indica L. infestations are comparatively low. When this species infests groundnuts (Arachis hypogea) the infestation reaches pest 464 SOUTHGATE

proportions. Corby (30) reports this insect damaging groundnut crops in pest proportions in 1936, and Roubaud (83) makes the first record of the insect on this host, but the serious increase of acreage of this crop did not take place until the late 1940s, early 1950s. With the possible suggested time period for the introduction of the groundnut to Africa being in the early 16th century, the developmental period for the insect to reach serious pest proportions is some 500 years. Against this must be placed the very rapid growth of the groundnut industry in West Africa since World War II, which undoubtedly accelerated the problem. The uprise of a future pest problem of the same type could be avoided by a greater understanding of the bionomics of each possible species that may become involved. Damage is not restricted to the food they eat because seeds harboring any stage of development are unpalatable. Venkatrao et al (98) record 6231 fragments of (Bruchidae) and uric acid levels of 5117 mg/IOOg of grains of Phaseo/us mungo after 6 months of storage. The uric acid level of the control material was 0.3 mg/IOOg for the same period. The holes in seeds left when adults emerge are a nuisance in the canning industry. The distinction between "field" and "storage" species with their particu­ lar life-cycle characteristics may have climatic origin. Species that inhabit regions with cold or arid periods often survive, because one stage, usually the adult, passes it in a resting stage. These often have an annual cycle related to the plant host. Adult flight after hibernation when pollen and nectar are available enables the female to lay eggs on the host. Species from equable climates where suitable food is always available do not need to hibernate. Seed stores provide a habitat that is readily utilized by species capable of continuous breeding, and these often multiply until the food reserves are exhausted. Before man began to store seed, food caches were small, so adults that normally do not live very long needed to survive until food could be found. Utida (96) suggested one way in which a storage species, Callosobruchus macu/atus (F.), may have improved its chances of Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org

Access provided by Copyright Clearance Center on 11/01/20. For personal use only. discovering suitable host seeds. He postulated the appearance of an abnor­ mal "flight" form initiated by high environmental temperatures that occur both when seed is naturally available and when high densities of infestation develop in seeds. More recently, Utida (96a-96c), Sano (83a), and others (4a, 32) have attempted to elucidate the function of this form and the circum­ stances in which it appears. de Carvalho & Machado (32) defined, and Spirina (91) confirmed, morphological forms that they linked with typical or atypical behavior of the nonactive and active forms. Utida (96) and Caswell (21) state that the flight form laid few eggs. Gill, Kanwar & Bawa (41) record that the male internal reproductive organs mature late, suggest­ ing that it is a form of adult diapause. de Carvalho & Machado (32) state that it lays 20.0 eggs per female as against 70.6 by the normal. It seems that THE BRUCHIDAE 465

this strain of bruchid is able to flya considerable distance to reach a suitable host, and that consequently maturation of the ovaries is delayed and the reserves available for eggs are reduced. There is no convincing evidence of a similar phenomenon in other storage bruchids. The appearance of new pest species must be anticipated quickly. In 1969 Kingsolver (60a) described a new species, Acanthoscelides zetek;, attacking pigeon peas [Cajanus cajan (L.) Millsp.] in Panama that has since been recorded widely in the Caribbean with infestations in stored products reach­ ing 40% in a few months (K. U. Buckmire, personal communication). In East Africa, an infestation of pigeon peas by Specularius sulcaticollis Pic has been recorded growing at the Mawapa Experimental Station in the coastal region of Kenya (90). Since this genus is mainly associated with Erythrina species, association with a food crop gives some cause for alarm.

P ARASITOIDS

Bruchidae are attacked in all developmental stages by parasitoids belonging to 10 families of and 1 of Diptera. The egg stage is very vulnerable because they are usually laid on the surface of the ripening pod. Bridwell (11) noted that when the trichogrammatid egg parasite Us­ cana semifumipennis Girault was present, only six larvae reached maturity from 3000 eggs of Caryedon (=Caryoborus gonagra) serratus 01., and he attributed most of the mortality to it. This genus of parasitoid, which is found in both the Old and New Worlds, is probably a species complex. Belinsky (5) bred two geographically isolated color forms from Caryedon serratus subsp. palaestinicus. The slightly smaller yellow form, confined to the Dead Sea region, laid as many as four eggs within a single egg of Caryedon, whereas the larger black form, widespread elsewhere in Israel, laid only one or two eggs therein. All the eggs can develop to maturity. She inferred that the yellow color form was caused by high temperature, as they were all found in the hottest region. Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org

Access provided by Copyright Clearance Center on 11/01/20. For personal use only. Uscana spp. were recorded by Prevett (78) in Caryedon spp. that attack Combretum spp. in Nigeria. The majority of the remaining hosts recorded for this genus are economic species, but they do not appear to attack the eggs of Callosobruchus after harvest. A related trichogrammatid species, Chaestostricha mukherjii Mani, has been recorded from the eggs of Callosobruchus analis (F.) (26). This lays only a single egg in each egg, or at least only a single adult emerges. Chatterji (26) infers that if more than one egg is laid, one larva destroys the rest. Little attention has been given to larval, prepupal, and pupal parasitoids other than to record their breeding on a particular species. The development of Anisopteromalis (Aplastomorpha) calandrae Howard and of Dinarmus 466 SOUTHGATE

(Bruchobius) basalis Rond. in Callosobruchus maculatus, Callosobruchus chinensis, and Callosobruchus analis has been studied under experimental laboratory conditions (27, 28, 71-73). Parnell (74), studying the population dynamics of insects on broom, Cytisus (=Sarothramnus) scoparius (L.) Wimmer, in England. recorded 56.4 and 48.4% parasitism, respectively, of Bruchidius ater by Habro­ cytus sequester in the 2 years of the study. Although these attacks reduced the number of bruchid reaching maturity on young broom plants, they were even more effective in older established plantations where the populations had stabilized. Here larval mortality was much higher, and since this fol­ lowed destruction of eggs by parasites and mite predators, the bruchid populations fell to very low numbers. This 2-year study admirably illus­ trates the need for long-term observations on natural populations to under­

stand the effectof the parasitoids. Thus the levels of 3. 54-9. 40% parasitism recorded by Rogers & Garrison (80) for Horismenusproductus (Ashmead) on Acanthoscelides collusus Fall. in Texas for one season may be the highest attainable under these conditions, but a series of observations over a period of 10 or more seasons could prove that levels of parasitism fluctuate widely. Only one dipterous parasite has been recorded to date from the Bru­ chidae. Exoprosopa minops (BombJidaceae) emerged from a cocoon of Caryedon serratus subsp. palaestinicus collected in the Negev region of Israel by Donahaye, Navarro & Calderon (37). Mites of the Pyemotesventricosus complex can destroy bruchid cultures if they are present and escape detection when the material is brought into the laboratory (54, 87). but their status has never been thoroughly investi­ gated in the field. I have seen many pinned adult bruchids, mainly African in origin, from collections in which the space beneath the elytra was packed with dead Pyemotes adults.

BRUCHIDS AS POSSIBLE CONTROL AGENTS Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org Access provided by Copyright Clearance Center on 11/01/20. For personal use only. The intense destruction of seeds of some plants reduces the numbers of seedlings beyond that needed to maintain the plant population. This will be convenient when man wants to control the plant and inconvenient when he wishes to preserve it. Bruchids have already been suggested for use in this way as an agent of biological control by Rogers & Garrison (80), who proposed the regulation of the seedling numbers of Amorpha jruticosa L. by encouraging the attack of their seed by Acanthoscelides col/usus Fall. Bridwell (12) remarks on the considerable destruction of pods of Acacia jarnesiana in Hawaii by an immigrant species, Caryedon serratus 01. This plant is a troublesome spiny shrub imported from South America that occupies large areas of pasture, so a biological control agent obviously THE BRUCHIDAE 467

would be welcome. Another bruchid, Mimosestes (Bruchus) sallaei, attacks seeds of this plant, but neither Bridwell (12) nor Hinckley (44) states if it has deleterious effects on the survival of seedlings. Work on the ecology of Prosopis spp. in semiarid areas. of North and South America have provided data on the damage to seeds by bruchids of the genera Algarobius and Neltumius and on the numbers of seeds ger­ minating and becoming established (42, 88). The species principally studied has been Pr osopis juliflora (SW) DC., a tree capable of reaching 20 m in height in fa vorable areas. A smaller shrub species, Prosopis [a reta (Banks et Sol) MacB., with a maximum height of 4 m is being studied in Israel by Belinsky (5), with the deliberate intent of controlling it as a weed on cultivated land. This plant has four bruchid species that attack its seeds: Bruehidius quinqueguttatus (01.), Bruehidius seminarius (L.), an unidenti­ fied Bruehidius, and Caryedon serratus subsp. palaestinieus Southgate. Since this last species destroyed so many seeds, a study of its life history on P. [a reta was made (5). Although this paper draws no conclusions for this Caryedon sp. as a possible control agent, the three to fo ur generations per year it maintains must exercise a fair. degree of control with an average of 31 eggs per female at 30°C. The life history of this bruchid on Acacia tortilis subsp. spirocarpa had already been studied by Donahaye, Navarro & Calderon (37). The beetle has also been recorded fr om Acacia raddiana but was never numerous on either Acacia sp. In experiments in which gravid females of the bruchid were offered a choice of seeds of A. raddiana and P. [a reta, most of the eggs were laid on the latter. This Caryedon sp. is subject to attack by three species of parasite, one that attacks the egg, Useana semijumipennis, two that attack the last two larval stadia, Rhaeono­ tus acieulatus and Eurytoma sp. Although the latter do not reduce the damage to the attacked seed, they interfere with the overall biological control of the plant by diminishing beetle numbers. The possibility of controlling forest weeds in Pakistan with a Callosobru­ ehus sp. is being investigated (3). An undescribed Callosobruehus sp. spe­

Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org . cHic to Pueraria tuberosa has been found, so its biology is being stunied by Access provided by Copyright Clearance Center on 11/01/20. For personal use only. workers at the Pakistan Station of the Commonwealth Institute of Biologi­ cal Control, with a view toward its possible use in biological control. As for any biological control program, the basic need is to study all aspects of the life of the bruchid, especially how it finds the host, when it feeds on more than one plant, and what determines its choice.

PROMISING LINES OF FUTURE BRUCHID RESEARCH

The current trend and mounting interest in the grain legumes as potential sources of protein fo r developing countries has given impetus to the study 468 SOUTHGATE

of the role played by bruchids in seed destruction and contamination of human food. The greater part of this interest has been stimulated by the study of the biochemical interactions between the beetles and the seeds they attack. The increase in knowledge of the free amino acid content of the seeds of various groups will enable entomologists to predict the possibility of attack. This presupposes that other biological requirements for oviposition and larval development are favorable. At the present time there is still a lack of knowledge of the life-history and behavioral responses of a number of the economic species, not to mention those marginal species that apparently exert some control over the regeneration of important trees and shrubs in various regions of the world. The ecological balance briefly explored by Lamprey, Halevy & Makacha (65) in Tanzania and the Middle East, and Mathwig (69) in Kansas, has shown that bruchids are one of the factors concerned with the control of regeneration of leguminous trees in the semiarid zones of Africa and North America. A better understanding of their part in the ecology of these regions could help to stem the spread of these unproductive areas. It is not only here that a greater understanding is required. The majority of legumi­ nous trees in the, at present, productive forested areas of Africa, Asia, and South America have bruchid attack in their seeds. During the course of time these have reached equilibrium with their environment. The interference of man in the little-understood biological complex could engender a serious break in the cycle, thus starting a decline in the forest ecosystem. Janzen (48, 50, 51) has made numerous suggestions in this respect as a result of his studies in Costa Rica. Further studies on the relationship between the bruchids and the amino acid levels of the seed, such as that initiated by Applebaum & Birk (1), are required to give a greater understanding of the tolerance of the larvae to apparently toxic substances. This coupled with studies on the host finding mechanism of the adults could help in the breeding of resistant crops. From recent published observations it is becoming increasingly obvious

Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org that the stored product species are not alone in their ability to produce more Access provided by Copyright Clearance Center on 11/01/20. For personal use only. than one generation on the same seeds (54), but the criteria that governthis feature in the noneconomic species is little understood. Several factors could be responsible, the most obvious of which is the removal of the seeds by mammals and birds from the area of production (48). Other factors that require investigation in connection with this are the degradation of amino acid levels in the seed, the moisture content of the seed, and its enveloping pod, together with the nature of the pod and whether it is dehiscent or otherwise. The possible movement of bruchids into new areas of host association must be borne in mind if agricultural development is to continue. The THE BRUCHIDAE 469

legumes, as a readily available source of protein, are at present the subject of much concern to agronomists, plant breeders, and particularly to such organizations as the International Institute of Tropical Agriculture, where grain legume programs feature strongly in the research program. Bruchids are only a part of the large numbers of species that attack grain legumes, as is evident from the paper by Singh & van Emden (86a) in this publication, but they are the one group that attack the crop both in the field and in storage. Modification of the amino acid content by gene manipulation to provide a less toxic material suitable for human or consumption, without elaborate pretreatment, may be to the advantage of the bruchids, particularly by the transference of species not at present of pest status. This has occurred in the past by the simple means of bringing a potential new host into an environment, as in the case of the introduction of the groundnut (Arachis hypogea) into West Africa mentioned elsewhere in this paper. Foresters and agriculturalists alike must be made aware of the potential seed destruction by these insects and the part they play in the ecology of the developing world. However, the entomologist must be conscious of the lack of information at present available on host plants and biology of this group and must remedy these omissions if any further advances are to be made.

ACKNOWLEDGMENTS

I would like to thank R. W. Howe of this laboratory for critical reading of the manuscript and making suggestions for its improvement.

Literature Ci ted

1. Applebaum, S. W., Birk, Y. 1972. Natu­ 4a. Bawa, S. R., Kanwar, K. C., Gupta, R. ral mechanisms of resistance to insects K. 1972. Interspecific hybridization and in legume seeds. In Insect and Mite Nu· the abnortnal strain of Callosobruchus trition, ed. J. G. ROdriguez. Amster­ maculatus. Ann. En tomoL Soc. Am. dam: North Holland. 702 pp. 65:1241-42 2. Bagdasaryan, B. A. 1941. The seed bee­ 5. Belinsky, A. 1976. A survey of the en­ tles of the Artnenian SSR and their tomofauna of Prosopis fa rcta in Is rael.

Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org relationships with plants, particularly with sp ecial reference to Ca ryedon ser­ Access provided by Copyright Clearance Center on 11/01/20. For personal use only. Leguminosae. Na uchn. Tr. Erevan. 60s. ratus. MSc thesis. Tel Aviv Univ., Is­ Univ. 16:309-74 rael. 82 pp. 3. B8Ioch, G. M., Ahmed, M., Arir, M. I. 6. Bell, E. A., Janzen, D. H. 1971. Medical 1974. Annual report of investigations and ecological considerations of L­ on the natural enemies of dwarf mistle­ Dopa and 5-HTP in seeds. Na ture toe (Arceuthobium spp.) and other for­ 229:136-37 est weeds common to Pakistan and 7. Bohemann, C. H. 1829. Novae Coleop­ the United States, 1973. Rawalpindi, terorum species. No uv. Mem. Soc. Pakistan: Commonw. Inst. BioI. Con­ 1 : 103-18 trol. 37 pp. 8. Booker, R. H. 1965. Pests of cowpea 4. Bato, S. M., Sanchez, F. F. 1972. The and their control in Northern Nigeria. biology and chemical control of Cal­ Bull Entomol Res. 55;663-672 losobruchus chinensis (Linn.) Philipp. 9. Bottimer, L. J. 1961. New United States EntomoL 2:167-82 records in Bruchidae with notes on host 470 SOUTHGATE

plants and rearing procedures. Ann. En­ parasites of Bruchus analis Fabr. In­ tomol Soc. Am. 54:291-98 dian J. EntomoL 15:382-83 10. Bottimer, L. J. 1968. Notes on Bru­ 27. ChatteIji, S. 1954. Notes on Bruchobius chidae of America north of Mexico with laticeps Ashm. parasitic on Bruchus a list of World Genera. Can. Entomol. chinensis Linn. Indian J. Entomol. 100:1009-49 16:77-78 II. Bridwell, J. C. 1918. Notes on the Bru­ 28. Chatterji, S. 1954. Studies on the chidae and their parasites in the Hawai­ biology of Aplastomorpha calandrae ian Islands. Proc. Hawaii. Entomol. Soc. Howard parasitic on some storage pests. 3:465-505. Proc. Zool. Soc. 8:11-23 12. Bridwell, J. C. 1919. Some additional 29. Chujo, M. 1937. Some additions and re­ notes on Bruchidae and their parasites visions of bruchidae from the Japanese in the Hawaiian Islands. Proc. Ha waii. Empire. Trans. Natl. Hist. Soc. Formosa Entomol. Soc. 4: 15-20 27:189-201 13. Bridwell, J. C. 1929. A preliminary �e­ 30. Corby, H. D. R. 1941. Report ofa study neric arrangement of the Palm Bruchlds of a pest (Pachymerus longus Pic) caus­ and Allies with descriptions of new spe­ ing damage to groundnuts in the Wur­ cies. Proc. Entomol Soc. Wash. 31: kum District of the Muri division of 141-60 Adamawa. Nigeria Dept. Agric. No. 14. Bridwell, J. C. 1931. Bruchidae infest­ 8402. with ing seeds of Compositae descrip­ 31. Crowson, R. A. 1953. Th e Na tural tions of new genera and species. Proc. Classification o/ the Fa milies o/ Coleopt­ Entomol. Soc. Wa sh. 33:37-42 era. Hampton, Middlesex: E. W. Clas­ 15. Bridwell, J. C. 1932. The subfamilies of sey. 187 pp. the Bruchidae. Proc. Entomol. Soc. 32. de Carvalho, J. P., Machado, M. U. M. Wash. 34:100--06 1967. A entomofauna dos productos ar­ 16. Bridwell, J. C. 1946. The genera of bee­ mazenados. Contribuicao para 0 estudo ties of the family Bruchidae in America do Callosabruchus maculatus (Fab­ north of Mexico. J. Wa sh. Acad. Sci. 36:52-57 ricius). Bolm Soc. Port. Cienc. Na t. Ser. 2a 11:133-240 17. Bridwell, J. C. 1952. A new genus of 33. Decelle, J. E. 1951. Contribution a l'e­ Bruchidae affecting Hibiscus in Argen­ tude des Bruchidae du Congo beIge. tina. J. Wa sh. Acad. Sci. 42:49-51 Rev. Zool Bot. A/r. 45:172-92 18. Bridwell, J. C. 1952. Notes on Bru­ 34. Decelle, J. 1956. La Bruche sud­ chidae affecting the Anacardiaceae, in­ Americaine des Acacias: Pseudo­ cluding the description of a new genus. pachymerina sp innipes Erichson. Bull. J. Wash. Acad. Sci. 42:124-26 Ann. Soc. R. Entomol Belg. 102:109-16 19. Burleigh, R., Southgate, B. J. 1975. In­ 35. 1968. sect infestation of stored Egyptian Len­ Decelle, J. Nouveaux Genres et Especes de Carydontini d' Afrique et de tils in Antiquity. J. Archaeol Sci. 2:391-92 Madagascar. Bull Ann. Soc. R. En­ tomol Belg. 104:413-26 20. Calderon, M. 1962. Bruchidae of Israe!. Riv. Parassitol. 23:207-16 36. de Luca, Y. 1962. Contribution aux 21. Caswell, G. H. 1960. Observations on Bruchides d'AIgerie. Leurs hOtes� an abnormal fo rm of Ca llosobruchus leurs parasites�leurs stations. Mem. maculatus (F.). Bull Entomol. Res. Soc. Hist. Nat. A/r. No. 7, 114 pp. 50:671-80 37. Donahaye, E., Navarro, S., Calderon, Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org Access provided by Copyright Clearance Center on 11/01/20. For personal use only. 22. Caswell, G. H. 1961. The infestation of M. 1966. Observations on the life cycle Cowpeas in the western regions of Ni­ of Caryedon gonagra (F.) on its natural geria. Trop . Sci. 3:154-58 hosts in Israel, Acacia spirocarpa and A. 23. Center, T. D., Johnson, C. D. 1972. torti/is. Trop. Sci. 8:85-89 Comparative life histories of Sennius. 38. Dutt, N. 1961. Jute pests. Silver Jubilee Environ. Entomol. 2:669-72 No. Indian J. Entomol pp. 59-71. 24. Center, T. D., Johnson, C. D. 1974. Co­ 39. Evans, C. S., Qureshi, M. Y., Bell, E. A. evolution of some seed beetles and their 1977. Free amino acids in the seeds of hosts. Ecology 55:1096-103 Acacia species. Phytochemistry 16: 25. Center, T. D., Johnson, C. D. 1976. 565-70 Host plants and parasites of some 40. Fowler, W. W. 1890. Coleoptera o/ the Arizona seed-feeding insects. Ann. En­ British Isles, Vol. 4. London: Reeve. tomal. Soc. Am. 69:195-201 411 pp. 26. Chatterji, S. 1953. Biological notes on 41. Gill, J., Kanwar, K. C., Bawa, S. R. Chaetostricha mukherjii Mani�gg 1971. Abnormal "Sterile" strain in Cal- THE BRUCHIDAE 47 1

losobruchus maculatus. Ann. Entomol. North and Central America. Tech. Bull. Soc. Am. 64:1186-88 US Dep. Agric. No. 1462. 135 pp. 42. Glendening, G. E., Paulsen, H. A. Jr. 57. Johnson, C. D., Kingsolver, J. M. 1975. 1955. Reproduction and establishment Ecology and redescription of the of Velvet Mesquite as related to inva­ Arizona grape bruchid Amblycerus vitis. sion of semi-desert grasslands. Te ch. Coleopt. Bull. 29:321-31 Bull. US Dep. Agric. No. 1127. 50 pp. 58. Johnson, C. D., Kingsolver, J. M. 1976. 43. Halevy, G. 1974. Gazel1es and seed bee­ Systematics of Stator of North and Cen­ tle. Isr. J. Bot. 23:120-26 tral America. Tech. Bull. US Dep. 44. Hinckley, A. D. 1960. The Klu Beetle, Agric. No. 1537. 101 pp. Mimosestes sallaei (Sharp), in Hawaii. 59. Karschon, R. 1975. Seed germination of Proc. Hawaii. Entomol. Soc. 17:260-69 Acacia raddiana Savi and A. tortilis 45. Holfmann, A. 1945. Fa une de Fra nce­ Hayne as related to infestation by bru­ Coleopteres Bruchides et Anthribides. chids. Bet Dagan, Israel: Div. Sci. Paris: Lechevalier. 184 pp. Pubis. Leaflet no. 52. 9 pp. 46. Howe, R. W., Currie, J. E. 1964. Some 60. Kieffer, J. J., Herbst, P. 1905. Uber laboratory observations on the rates of Gallen und Gallenerzeuger aus Chile. development, mortality and oviposition Z. Wiss. Insekt. BioI. 1:63-66 of several species of Bruchidae breeding 60a. Kingsolver, J. M. 1969. A new species of Neotropical seed weevil affecting Pi­ in stored pulses. Bull. Entomol. Res. 55:437-77 geon Peas, with notes on two closely 47. Hutchinson, J. 1964. Th e Genera of related species. Proc. Entomol. Soc. Wa sh. 71:50-55 Flo wering Plants Dicotyledons, Vol. I. Oxford: Oxford Univ. Press. 516 pp. 61. Kingsolver, J. M. 1970. A synopsis of 48. Janzen, D. H. 1969. Seed-eaters versus the subfamily Amblycerinae Bridwel1 in seed size, number, toxicity and dis­ the West Indies with descriptions of new species. persal. 23:1-27 Trans. Am. Entomol. Soc. Evolution 96:469-97 49. Janzen, D. H. 1971. The fate of Scheelea 62. Kingsolver, J. M. 1971. Description of fruits beneath the parent tree: rostrata a new seed beetle from Australia. predispersal attack by bruchids. J. Prin. J. 10:179-82 15:89-101 Aust. Entomol. Soc. Palm Soc. 63. Koura, A., EI Halfawy, M., Shehata, T., 50. Janzen, D. H. 1973. Comments on host­ Darkal, 1971. Preference of the specificityof tropical herbivores and its W. Cowpea Weevil Callosobruchus macu­ relevance to species richness. Taxonomy la tus F. to some legume seeds and and Ecology, ed. V. H. Heywood, pp. weight loss due to the insect infestation. 201-11. New York: Academic Agric. Res. Rev. Ca iro 49:35-40 51. Janzen, D. H. 1978. The interaction of 64. Kunhi Kannan, K. 1923. The function seed predators and seed chemistry. Col­ of the prothoracic plate in Mylabrid loques Int. Cent. Na tL Rech. Sci. (Bruchid) larvae. Bull. Dep. Agric. 265:415-28 Mysore Entomol. Ser. 7:1-47 52. Janzen, D. H., Juster, H. B., Bell, E. A. 65. Lamprey, H. F., Halevy, G., Makacha, 1977. Toxicity of secondary compounds S. 1974. Interactions between Acacia, to the seed-eating larvae of the Bruchid bruchid seed beetles and large her­ beetle Callosobruchus maculatus. Phy­ bivores. East Afr. WildL J. 12:81-85 tochemistry 16:223-27 66. Larson, A. 0., Brindley, T. A., Hin­ 53. Johnson, C. D. 1967. Notes on the sys­ man, F. G. 1938. Biology of the pea Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org

Access provided by Copyright Clearance Center on 11/01/20. For personal use only. tematics, host plants and bionomics of weevil in the Pacific Northwest with the Bruchid genera Merobruchus and suggestions for its control on seed peas. Stator. Pan. Pac. EntomoL 43:264-7 1 Te ch. Bull. US Dep. Agric. No. 599. 54. Johnson, C. D. 1970. Biosystematics of 48 pp. the Arizona, California, and Oregon 67. Larson, A. 0., Fisher, C. K. 1938. The species of the seed beetle genus Acan­ and the Southern Cowpea thoscelides Schilsky. Un iv. California weevil in California. Te ch. Bull. US Publ. EntomoL 59:1-1 16 Dep. Agric. No. 393. 71 pp. 55. Johnson, C. D., Kingsolver, J. M. 1971. 68. Luk'yanovich, F. K., Ter-Minasyan, M. Descriptions, life history, and ecology E. 1971. Fauna of the USSR: Coleop­ of two new species of Bruchidae infest­ tera: Seed Beetles. Akad. Na uk SSSR ing Guacima in Mexico. J. Kan. En­ Zool. Inst. Fa una SSSR 24 tomol. Soc. 44: 141-52 69. Mathwig, J. E. 1971. Relationships be­ 56. Johnson, C. D., Kingsolver, J. M. 1973. tween Bruchid beetles (Amblycerus robi­ A revision of the genus Sennius of niae) and honey locust trees (Gleditsia 472 SOUTHGATE

triacanthos). PhD thesis. Kansas State 82. Roy, D. N., Bhat, R. V. 1975. Variation Univ., Manhattan. 169 pp. in neurotoxin, trypsin inhibitors and 70. Mitchell, R. 1977. Bruchid beetles and susceptibility to insect attack in vari­ seed packaging by Palo Verde. Ecology eties of Lathyrus sativus seeds. Environ. 58:644-5 1 Physiol. Biochem. 5:172-77 71. Okamoto, K. 1971. The synchroniza­ 83. Roubaud, E. 1916. Les insects et la de­ tion of the life cycles of Callosobruchus generscence des Arachides au Senegat chinensis L. and its parasite Anisop­ Ann. Mem. Co m. Etudes Hist. Sci. Afr. teromalus calandrae How. Jp n. J. Ecol. Occ. Fra ncaise. 76 pp. 20:233-37 83a. Sano, I. 1967. Density effect and envi­ 72. Okamoto, K. 1971. The reproduction ronmental temperature as the factors curve of the host in a host-{,arasite in­ producing the active form of Ca lloso­ teracting system and a parasite free sys­ bruchus maculatus. J. Stored Prod. Res. tem. Jp n. J. Ecol. 21:197-203 2:187-95 73. Okamoto, K. 1972. Synchronization of 84. Schilsky, J., in KUster. 1905. de Kafer life-cycles between C. chinensis (L.) and Europa s. NUrenberg: Bauer und Raspe its parasite Anisopteromalus calandrae 85. Schulze-Motel, J. 1972. Die Ar­ How. II. The relationship between de­ chiiologischen Reste der Ackerbohne, velopment of parasite and developmen­ Vida fa bae L. und die Genese der Art. tal stage of the host. Jp n. J. EcoL Kulturpjlanze 19:321-58 22:238-44 86. Shomar, N. F. H. 1963. A monographic 74. Parnell, J. R. 1966. Observations on the revision of the Bruchidae of Egypt population fluctuations and life histo­ (U.A.R.). BulL Soc. EntomoL Egypt 47:141-96 ries of the beetles Bruchidius ater and 86a. Singh, S. R., van Emden, H. F. 1979. Apion fu scirostre on Broom (Sarotham­ Insect pests of grain legumes. Ann. Rev. nus scoparius). 1. Anim. Ecol. 35: 157-88 Entomol. 24:255-78 87. Skaife, S. H. 1926. The bionomics of the 75. Pfaffenberger, G. S., Johnson, C. D. Bruchidae. S. Afr. J. ScL 13:575-88 1976. Biosystematics of the first-stage 88. Solbrig, O. T., Cantino, P. D. 1975. Re­ larvae of some North American Bru­ productive adaptations in Prosopis. J. chidae. Te ch. Bull US Dep. Agric. No. Arnold Arbor. 56:185-210 1525. 75 pp. 89. Southgate, B. J. 1971. On the identity of 76. Prevett, P. F. 1953. Studies on the Caryedon pallidus (Olivier) and the de­ fe cundity and longevity of the groundnut scription of two new Ca ryedon spp. Bruchid, Ca ryedon fu scus Goeze, and Bull. Entomol. Res. 60:409-14 the external morphology of the im ma­ 90. Southgate, B. J., McFarlane, J. A. 1978. ture stages. BSc thesis. Imperial Coil. Host records of Sp ecularius species Sci. Technoi., London. 54 pp. with notes on the infestation of Pigeon 77. Prevett, P. F. 1961. Field infestation of Peas (Cajanus caja n (L.» by these bee­ cowpea (Vign a unguiculata) pods by tles. East Afr. Agric. For. J. 42:In press beetles of the families Bruchidae and 91. Spirina, T. S. 1974. The comparative Curculionidae in Northern Nigeria. morphology of the male and female Bull Entomol Res. 52:635-45 genitalia in the two fo rms of the four­ 78. Prevett, P. F. 1966. Observations on spotted cowpea beetle Callosobruchus biology in the genus Caryedon Schoen­ maculatus (F.). EntomoL Rev. Wa sh. herr in Northern Nigeria, with a list of 53:22-27 Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org Access provided by Copyright Clearance Center on 11/01/20. For personal use only. parasitic Hymenoptera. Proc. R. En­ 92. Srivastava, B. K., Bhatia, S. K. 1957. tomol. Soc. London Ser. A 41:9- 16 Occurrence of Sp ermophagus sp. as a 79. Prevett, P. F. 1967. Notes on the pest of okra seed. Indian J. Entomol. biology, fo od plants and distribution of 19:216-,17 Nigerian Bruchidae with particular ref­ 93. Swier, S. R. 1974. Comparative seed erence to the northern region. Bull. En­ predation strategies of Bruchids attack­ tomol. Soc. Nigeria 1 :3-6 ing mesquite in the Sonoran Desert. 80. Rogers, C. E., Garrison, J. C. 1975. Proc. North Cent. Branch Entomal. Soc. Seed destruction in Indigobush Amor­ Am. 29:157 pha by a Seed Beetle. 1. Range Manage. 94. Teran, A. L. 1962. Observacianes sabre 28:241-42 Bruchidae del Noroeste Argentino. 81. Rosenthal, G. A., Dahlman, D. L., Acta Zool. Lilloana 18:21 1-4:4 Janzen, D. H. 1976. A novel means for 95. Teran, A. L. 1964. Alfunas novedades dealing with L-canavanine a toxic en el genero Eubaptus Lac. Acta Zool. metabolite. Science 192:256-,58 Lilloana 20: 177-86 THE BRUCHIDAE 473

96. Utida, S. 1953. "Phase" dimorphism 97. Vazirani, T. G. 1976. A contribution to observed in the laboratory population the knowledge of Oriental Bruchidae. J. of the cowpea weevil Ca llosobruchus Bombay Na tl Hist. Soc. 72:740-57 quadrimaculatus. Jp n. J. Appl Zool. 98. Venkatrao, S., Nuggehalli, R. N., Pin­ 18:161-68 gale, S. V., Swaminthan, M., Subrah­ 96a. Utida, S. 1956. "Phase" dimorphism manyan, V. 1960. Effect of insect infe­ observed in the laboratory population station on stored field bean and black of the cowpea weevil Callosobruchus gram (Phaseolus mungo). Food Sci. maculatus. 2nd Rep: Differential effects 9:79-82 of temperature, humidity and popula­ 99. Wickens, G. E. 1969. A study of Acacia tion density upon some ecological char­ albida Del Mimosoideae. Kew Bull acters of the two phases. Res. Pop. Ecol. 23:181-202 3:93-104 100. Whitehead, D. R., Kingsolver, J. M. 96b. Utida, S. 1965. "Phase" dimorphism 1975. Biosystematics of the North and observed in the laboratory population of Central American species of Gibbobru­ the cowpea weevil Callosobruchus chus. Trans. Am. Entomol. Soc. 101: maculatus. IV. The mechanism of in­ 167-225 duction of the flight form. Jp n. J. Ecol. 101. Zachariae, G. von 1958. Das Verhalten 1965: 193-99 des Speisebohnenkafers Acanthoscelides 96c. Utida, S. 1968. The influence of the obtectus Say im Freien in Norddeutsch­ parental condition on the production of land. Z Angew. Entomol. 43:345-65 the flight form in the population of Cal­ 102. Zacher, F. 1951. Die Nahrpflanzen losobruchus maculatus. Jp n. J. Ecol. der Samenkafer. Z Angew. Entomol. 18:246-49 33:210-17; 460-80. Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org Access provided by Copyright Clearance Center on 11/01/20. For personal use only. Annu. Rev. Entomol. 1979.24:449-473. Downloaded from www.annualreviews.org Access provided by Copyright Clearance Center on 11/01/20. For personal use only.