Introduction
This review aims to provide a checklist of the species of Sub-Saharan African Melolonthinae that have been recorded as pests in agricultural and forestry crops (Table 1 supplementary material), and draws attention to groups most in need of revision from a pest management perspective. Additionally, it provides comprehensive review and bibliography of all traced literature (especially taxonomic) specific to the melolonthine white grubs and chafers of the Region. It is hoped that this will facilitate white grub research in Sub-Saharan Africa via enhanced access to information, and the reduction of duplicated research efforts. Based on this synthesis, recommendations relevant to white grub and chafer taxonomy in Sub-Saharan Africa are proposed. To constrain the size and scope of the review, it covers only the subfamily Melolonthinae, with the remaining scarab subfamilies that contain species of economic concern being dealt with in forthcoming studies.
The larvae (white grubs) and adults (chafers) of five subfamilies of Scarabaeidae (Aphodiinae, Dynastinae, Cetoniinae, Melolonthinae and Rutelinae) include species that feed on the roots, stems, fruit or foliage of many crops, and therefore may be sporadic forestry and agricultural pests (Table 1 supplementary material). Colloquially, these larvae are known as white grubs, cane grubs or curl grubs when they damage agricultural crops in different regions of the World. White grubs are readily identified by their ‘C-shaped’ bodies and sclerotized head capsules, while the more variable adults generally have an ovoid body shape and lamellate antennae (Richter, Reference Ritcher1958, Reference Ritcher1966). Related scarab families, for example dung beetles (Scarabaeinae), have similar larvae, but as these groups are beneficial recyclers, they are generally not referred to as white grubs.
Melolonthine scarab beetles have a complete life-cycle (holometabolous); a fertilized female lays eggs, these hatch into the first of three larval stages or instars, the final (or third) instar enters a pre-pupal stage before pupation, from which adults emerge when environmental conditions are conducive (Ritcher, Reference Ritcher1958, Reference Ritcher1966). The duration of the larval stage can vary from 1 to 3 years depending on the environmental conditions and species’ life cycle (Ratcliffe, Reference Ratcliffe1991). However, species with 2–3 year life-cycles often have adults active each year due to an overlapping of generations. The phenology of the adults is unknown for most species, but based on adult phenological data compiled from museum records for Asthenopholis (Harrison, Reference Harrison2009) and Pegylis (Harrison, Reference Harrison2014b ), adults from these genera are present in varying numbers throughout summer each year.
Species distributions are dependent on a variety of factors. Some white grubs have a narrow distribution (stenotopic, e.g. Asthenopholis subfasciata (Harrison, Reference Harrison2009) and Macrophylla spp.), while others have a wider distribution (eurytopic, e.g. Pegylis sommeri (Harrison, Reference Harrison2014b )). Soil type, texture and moisture content can play an important role in the distribution of certain white grub species (Cherry & Allsopp, Reference Cherry and Allsopp1991; Allsopp et al., Reference Allsopp, Klein and McCoy1992; Logan, Reference Logan1997). Females of some white grub species are flightless, e.g. Macrophylla pubens (Omer-Cooper et al., Reference Omer-Cooper, Whitnall and Fenwick1941, Reference Omer-Cooper, Whitnall and Fenwick1941–1942, Reference Omer-Cooper, Whitnall and Fenwick1948; Fenwick, Reference Fenwick1947), and this has implications for control strategies and the geographic extent of an outbreak. The adult activity period can be quite narrow (just a few days after rain) for some species of chafer (Harrison, personal observations) or extend over a longer time period, i.e. weeks and months for Pegylis sommeri (see phenology figs in Harrison (Reference Harrison2014b )).
Pest status of scarabs
In large numbers the feeding activity of white grubs and chafers in crops reduces yields and facilitates secondary microbial infections through the damaged plant cuticle (Smith et al., Reference Smith, Petty and Villet1995; Miller et al., Reference Miller, Allsopp, Graham and Yeates1999). For example, in southern Africa, white grubs have been recorded as sporadic subterranean pests on tree-seedlings, sorghum, sugarcane, pineapples, potatoes and turf grass (see Table 1 supplementary material for a complete list). Additionally, the adult chafers are often defoliators (e.g. Pegylis spp.) in forest plantations, fruit orchards, vineyards and rose gardens (Table 1 supplementary material). At least 50 different species of commercially grown plants have records of Melolonthinae being destructive to parts of these plants (Table 1 supplementary material).
Introduced alien species
Most, if not all, African melolonthine scarab pests are endemic to parts of Africa, and no introduced scarab pest species are recorded for South Africa (Picker & Griffiths, Reference Picker and Griffiths2011). However, as this is a broad and general information source, it by no means rules out the possibility of there being alien scarabs in Sub-Saharan Africa. A possible exception is Phyllophaga smithi (Arrow, Reference Arrow1912), which was originally described as Phytalus smithi from the Caribbean (Barbados and Trinidad) and introduced into Mauritius (Evans, Reference Evans2003). This species was recorded (Katagira, Reference Katagira, Macdonald, Reaser, Bright, Neville, Howard, Murphy and Preston2003: 74) from Tanzania and mentioned as a sorghum stem-borer in eastern Ethiopia (Tefera, Reference Tefera2004). However, there is no published confirmation of this introduction in the primary literature for sugarcane pests known from Tanzania, but the African endemic Cochliotis melolonthoides is well established as a sugarcane pest in Tanzania (Jepson, Reference Jepson1956; Carnegie, Reference Carnegie, Carnegie, Dick and Harris1974a , Reference Carnegie b ). Consequently, the Katagira (Reference Katagira, Macdonald, Reaser, Bright, Neville, Howard, Murphy and Preston2003) and Tefera (Reference Tefera2004) records of P. smithi occurring on the African mainland may be based on the exotics being confused with an African species of Schizonycha, which is quite similar to Phyllophaga (=Phytalus) Arrow (Reference Arrow1912).
Conservation of localized endemic species
Localized endemics are of particular conservation importance. For example, Asthenopholis subfasciata can become an important sporadic pest of pineapples in the Eastern Cape of South Africa (Petty, Reference Petty1976, Reference Petty1977a , Reference Petty b , Reference Petty1978, Reference Petty1982, Reference Petty1990, Reference Petty1994, Reference Petty, van den Berg, de Villiers and Joubert2001, Petty et al., Reference Petty, Stirling, Bartholomew, Peña, Sharp and Wysoki2002). However, it is endemic to South Africa and is also one of only seven known species of Asthenopholis (Harrison, Reference Harrison2009). As a localized endemic and part of the country's biodiversity, we need to control it responsibly when it reaches localized pest levels. Another example of a localized endemic that can become a sporadic pest species is Pseudachloa leonina on golf greens near Pretoria, South Africa (A. Schoeman, Reference Haddad, Dippenaar-Schoeman and Pekár2005, personal communication).
Access to information
Fragmentary, unsynthesized information relating to scarabs as pests in African crops reduces the efficiency of research on economically important species. For example, the paucity of information on Eucamenta eugeniae, originally described as a pest of clove (Eugenia caryophyllata) from Zanzibar (Arrow, Reference Arrow1932; Andre Moutia, Reference Andre Moutia1941). But a recent paper (Conlong & Mugalula, Reference Conlong and Mugalula2003) omitted these early publications and reported E. eugeniae only as a new pest of sugarcane in Uganda.
Information relating to the same insect taxon, but disguised due to an incorrect identification is another problem. For example, the incorrect identification of Pegylis sommeri (previously Hypopholis) as Macrophylla ciliata (Herbst) as a pest of pineapple in South Africa (Petty, Reference Petty1976, Reference Petty1977b , Reference Petty1978, Reference Petty1990, Reference Petty, van den Berg, de Villiers and Joubert2001; Petty et al., Reference Petty, Stirling, Bartholomew, Peña, Sharp and Wysoki2002) resulted in the redescription of the larvae of P. sommeri (Smith et al., Reference Smith, Petty and Villet1995), which had previously been described (Prins, Reference Prins1965). Misidentification resulted in a duplication of effort, lack of efficient control strategies, crop destruction and reduced economic benefits.
The importance of having named pests
The success of an integrated pest management (IPM) program for melolonthine white grubs depends strongly on accurate identification of larvae and adults (Danks, Reference Danks1988). Species level identification is important because life cycles of white grub species vary from 1 to 3 years and susceptibility to insecticides varies for species (as demonstrated in Australian cane grubs; Allsopp et al., Reference Allsopp, McGill and Bull1995). Correct diagnosis relies upon available taxonomic expertise, published research, trained systematists, and access to museum specimens, voucher specimens and type material. In contrast to more developed countries (e.g. the USA, Australia and New Zealand) southern Africa in our view lags behind by a number of years in scarab taxonomic research on melolonthine white grub identification and research.
In a discussion on white grub identification (Omer-Cooper et al., Reference Omer-Cooper, Whitnall and Fenwick1941, Reference Omer-Cooper, Whitnall and Fenwick1941–1942) the authors state that, ‘… very little work has been done on these insects in South Africa, and with the present state of our knowledge we would not be prepared to say in all cases which are pests and which are not’. Later (Sweeney, Reference Sweeney1967) added that ‘Few published papers deal with the morphology and taxonomy of larval Scarabaeoidea in southern Africa, and the larvae of many species are undescribed’. However, recent taxonomic work by Ahrens (Reference Ahrens2007a , Reference Ahrens b ), Conlong & Mugalula (Reference Conlong and Mugalula2003), Dittrich-Schröder et al. (Reference Dittrich-Schröder, Conlong, Way, Harrison and Mitchell2009), Goble et al. (Reference Goble, Costet, Robene, Nibouche, Rutherford, Conlong and Hill2012) and Harrison (Reference Harrison2004, Reference Harrison2009, Reference Harrison2014a , Reference Harrison b , this review) is a positive advancement in melolonthine research in the Region.
Morphological identification of melolonthine larvae and adults
To morphologically describe a scarab larva, the chitinous head capsule is softened in lactic acid or a weak solution of KOH and disarticulated from points of natural articulation of structures (Dittrich-Schröder et al., Reference Dittrich-Schröder, Conlong, Way, Harrison and Mitchell2009). Ritcher (Reference Ritcher1966) provided numerous illustrations and descriptions of disarticulated scarab head capsules. This requires association of the larva with a named adult and formal description in a published paper. African melolonthines in which larvae have been described and illustrated (Table 2 supplementary material), include a small percentage of the known melolonthine diversity.
Adult identification also relies on the beetle species having been described in a validly published paper. Insect drawers of African Melolonthinae sorted only to subfamily in museum collections are testament to the lack of taxonomists dealing with this diverse group of beetles. Consequently, in many cases one can at best identify a pest melolonthine to genus level only, and even here good taxonomic keys for generic diagnoses (e.g., Péringuey, Reference Péringuey1904; Lacroix, Reference Lacroix2010) are the exception rather than the rule.
An ideal scenario would be as follows: a taxonomist is presented with larvae and adults of Pegylis sommeri and asked to identify these. In this particular instance, the larvae could be identified using Prins (Reference Prins1965) and the adults using Harrison (Reference Harrison2014b ). Adult specimens of Asthenopholis can be identified using Harrison (Reference Harrison2009), but the larva of only one species of this genus has been described, i.e., A. subfasciata in Smith et al. (Reference Smith, Petty and Villet1995), leaving the larvae of the remaining six species unassociated with their adults via the taxonomic literature.
Molecular diagnostic techniques
A frequently encountered problem with white grub outbreaks is determining the white grub species. Identification is especially important because control action must be immediate to prevent further losses. Molecular DNA barcoding techniques allow for the DNA of grubs or adults to be matched with DNA sequence data (e.g., archived Genbank sequences) and possible retrieval of an identification based on these data. Once a match is retrieved the morphology of the grubs can be described in order to facilitate accurate and efficient identification in the future. This process can be used to develop identification tools. For example, Dittrich-Schröder et al. (Reference Dittrich-Schröder, Conlong, Way, Harrison and Mitchell2009) compiled an identification key to the scarab beetle larvae attacking sugarcane in South Africa. Using molecular methods and associating grubs with adults, tools for identification of chafers were developed for use on the Nepalese fauna (Ahrens et al., Reference Ahrens, Monaghan and Vogler2007a , Reference Ahrens, Zorn, Dhoj, Keller and Nagel b ). This research is best done by a collaborating team of molecular biologists, beetle taxonomists and crop specialists.
IPM options for white grubs and chafers
IPM of white grubs and chafers is a review topic of its own, and consequently only brief mention is included here. Control options include various forms of chemical control, cultural methods, parasitic Diptera (flies), Hymenoptera (wasps), fungi and tillage methods. Smit (Reference Smit1964), Annecke & Moran (Reference Annecke and Moran1982) and Visser (Reference Visser2005, Reference Visser2009) provide general coverage of IPM methods relevant to the African context for many of the taxa included in this review.
Taxonomic review of the Melolonthinae with published records of significance to Sub-Saharan African forestry and agricultural crops
The world melolonthine fauna is presently divided into 28 extant tribes and 12 subtribes (Smith, Reference Smith2006), of which six tribes and nine subtribes are known to occur on the African mainland. Sub-Saharan Africa includes taxa from six tribes and six subtribes as presented below. All known Sub-Saharan African Melolonthinae recorded in the literature as having the potential to become sporadic pests in agricultural and forestry crops are reviewed (table 1). Included in table 1 are taxonomic details (generic and specific description dates and authors) and thus this information is not repeated in the text. However, taxa not included in the checklist (table 1) are referred to in the text including their author and publication date.
Table 1. Checklist of Sub-Saharan African melolonthine white grubs and leaf chafers (Scarabaeidae: Melolonthinae) of potential significance to forestry and agricultural crops. This list is based on the literature sources cited in Table 1 supplementary material.
1 Misidentified as Adoretus tessulatus (Rutelinae) in Petty's earlier papers.
2 An incorrect identification has placed this species name in the literature as a pest of pineapple; the correct species identification is Pegylis sommeri (see Harrison, Reference Harrison2014b ). Petty (Reference Petty1978) provides a clear photograph of P. sommeri, but identified as Macrophylla ciliata.
3 Von Schmutterer (Reference Schmutterer1964) refers to this species as S. vastatrix Chiar. (Chiaromonte). Paul Schoolmeesters (personal communication) drew our attention to its first description in Paoli (1934); no mention is made to this species in Pope (Reference Pope1960) or Lacroix (Reference Lacroix2010).
4 To a non-specialist the genera Phyllophaga and Schizonycha are morphologically similar. The former is not known from Africa, while the latter is (see Pope, Reference Pope1960).
5 Incorrectly referred to as Macrophylla ciliata (Herbst, 1790).
6 Afrolepis Decelle, 1968 (replacement name for preoccupied Oligolepis Brenske, 1903).
7 ‘Williams (Reference Williams1985) records A. minor (as A. subfasciata) to have a limited distribution in the Nokwane (Mhlume) and S.I.S. (Swaziland Irrigation Scheme) sugarcane farms in Swaziland. Carnegie (Reference Carnegie1988) mentions A. minor and A. subfasciata as sugarcane pests in Swaziland and Emoyeni, KwaZulu–Natal. White grubs of A. subfasciata (Anonymous, 1992) are reported from sugarcane fields from the Mhlume area (Vuvulane) in Swaziland. However, the present study establishes that these are misidentifications. Asthenopholis subfasciata does not occur in Swaziland or KwaZulu–Natal (i.e., Port Natal = Durban), save for a few old and questionable records. Asthenopholis minor is more likely to be a sporadic pest of sugarcane in these regions.’ Harrison (Reference Harrison2009).
8 Sweeney (Reference Sweeney1967) includes A. subfasciata for Swaziland (Mhlume). After revising Asthenopholis Harrison (Reference Harrison2009) suggests that the Swaziland (Mhlume) specimens are most likely attributable to A. minor.
9 Currently valid genus name is Maladera Mulsant & Rey, 1871 (Dirk Ahrens, personal communication).
10 Swain & Prinsloo (Reference Swain and Prinsloo1986) list this species as Maladera tesselata (Péringuey), but we follow Dalla Torre (Reference Dalla Torre1912) and include it here as Autoserica tessellata Péringuey, 1904.
11 Currently valid genus name is Maladera Mulsant & Rey, 1871 (Dirk Ahrens, personal communication).
12 This species was originally described in Serica (Dirk Ahrens, personal communication).
13 The taxonomic position of Lepiserica in relation to Maladera requires investigation (Dirk Ahrens, personal communication).
14 Swain & Prinsloo (Reference Swain and Prinsloo1986) list this species as Maladera carneola (Péringuey), but we follow Dalla Torre (Reference Dalla Torre1912) and include it here as Neoserica carneola Péringuey, 1892.
15 Currently valid genus name is Triodontella Reitter, 1919 (Dirk Ahrens, personal communicaiton).
16 Spelt as T. aerugineus in Sweeney (Reference Sweeney1967), but as T. aeruginosus in Dalla Torre (Reference Dalla Torre1912).
Also summarized are melolonthine species, crop attacked, life stage involved, country of origin and the source reference (Table 1 supplementary material). Thus, if not specifically mentioned below, the life stage, larva or adult, involved in the damage is included in Table 1 supplementary material.
Tribe ABLABERINI Blanchard, 1850
For garden flowers, Annecke & Moran (Reference Annecke and Moran1982) list adults of Ablabera pellucida as feeding on carnations. Adults of Camenta innocua appears to occur in most major centers in South Africa (JduGH, personal observations) and can be found at night feeding on a variety of garden plants, with roses, being one of those most seriously damaged (JduGH, personal observations). The larvae of what was possibly C. innocua caused significant damage to raspberry seedlings in the George and Hermanus areas of South Africa (Tim Sobey Nov. 2012, personal communication). Oberholzer (Reference Oberholzer1959a , Reference Oberholzer b ) described the third instar larvae of C. innocua from specimens collected in Johannesburg, South Africa, but he did not indicate any pest status for the species.
In the interests of taxonomic stability, Ahrens (Reference Ahrens2007a ) designated types for various African genera in the Ablaberini, including Ablabera Dejean, 1833; Eucamenta Péringuey, Reference Péringuey1904; Hybocamenta Brenske, 1898; and Paracamenta Péringuey, Reference Péringuey1904. Neither Ablabera nor Camenta have been recently revised, making species level identification in these genera difficult or impossible, especially bearing in mind the large number of undescribed taxa within the Ablaberini. The syntype of C. innocua is a single female (Dirk Ahrens, personal communication), making the unequivocal identity of this species currently impossible in the absence of the male genitalia necessary for identification.
Tribe DIPLOTAXINI Kirby, 1837
Peacock (Reference Peacock1913), looking at insect pests of cacao or cocoa bean (Theobroma cacao L.) in southern Nigeria, recorded Apogonia nitidula together with various other scarabs, but included these in a list of taxa with doubtful significance (associated with the crop but not showing signs of being an actual pest). Lepesme & Paulian (Reference Lepesme and Paulian1944) recorded the same species on Coffea robusta in Gabon, but they provided no further details about the association. In work applying to species from neighbouring South Asia Islam et al. (Reference Islam, Ahmed and Joarder1984) included species of Apogonia among the insect pests associated with green gram (Vigna radiata L.) from Bangladesh, India. Of the beetles studied by Islam et al. (Reference Islam, Ahmed and Joarder1984), Apogonia were responsible for consuming the largest leaf area.
Bezděk (Reference Bezděk2004a ) provided a catalogue of Diplotaxini of the Old World and a detailed revision on the African monotypic genus Ceratogonia Kolbe, 1899 (Bezděk, Reference Bezděk2004b ). He provided synonymic notes for Apogonia cupreoviridis Kolbe, 1886 and A. nigroolivacea Heyden, 1886 (Bezděk, Reference Bezděk2008), and notes on the synonymy and geographic distribution of Apogonia niponica Lewis, 1895 (Bezděk, Reference Bezděk2009). Lacroix (Reference Lacroix2008a , Reference Lacroix b ) described new genera and species of Diplotaxini, and Lacroix & Bezděk (Reference Lacroix and Bezdĕk2009) proposed replacement names for Metagonia Kolbe, 1899 (nec Simon, Reference Simon1893).
Tribe HOPLIINI Latreille, 1829
In South Africa, these beetles are colloquially referred to as monkey beetles (Picker & Midgley Reference Picker and Midgley1996). Smit (Reference Smit1964) recorded adult Hopliini burrowing into garden Compositae (Asteraceae), especially marigolds in Pretoria, South Africa. Prins (Reference Prins1965) listed Monochelus calcaratus, which he refered to as the small wattle chafer, as a wattle defoliator. Prins (Reference Prins1965) also described its larva, the only description of an African Hopliini larva (known to us). For garden flowers, Annecke & Moran (Reference Annecke and Moran1982) recorded Eriesthis stigmatica and Heterochelus connatus feeding on carnations, and E. vestita feeding on dahlias. Swain & Prinsloo (Reference Swain and Prinsloo1986) listed species of Heterochelus feeding on Acacia mearnsii, and Monochelus calceratus feeding on Acacia decurrens, A. mearnsii and A. melanoxylon. Gess (Reference Gess1968), Myburgh et al. (Reference Myburgh, Rust and Starke1973, Reference Myburgh, Starke and Rust1974), Myburgh & Rust (Reference Myburgh and Rust1975) and Coetzee & Giliomee (Reference Coetzee and Giliomee1985) investigated insects associated with Protea flowers as both pests damaging the flowers and insects likely to be exported with flowers due to their biological associations with the Protea. Myburgh & Rust (Reference Myburgh and Rust1975) provided a list of 34 ‘free-living pests in protea flower-heads’, including the following monkey beetles: Anisonyx nasuus, Heterochelus rufimanus, and a species of Platychelus. Coetzee & Giliomee (Reference Coetzee and Giliomee1985), in a study specific to Protea repens (L.), listed adult Diaplochelus longipes as a floral visitor. Dombrow (Reference Dombrow2006b ) described two new species of Diaplochelus sent abroad with consignments of exported Protea from South Africa to Poland and the USA.
Due to the charismatic morphological diversity of the southern African Hopliini, this tribe has received greater taxonomic attention than any other in the Region. Dombrow, in particular, has revised many of the southern African genera (a list of his known papers is provided). These papers included taxonomic revisions of Eriesthis (Dombrow, Reference Dombrow1997c , Reference Dombrow2002b ), Heterochelus (Dombrow, Reference Dombrow2001c ) and Diaplochelus (Dombrow, Reference Dombrow2006b ). Schein (Reference Schein1958) studied South African Heterochelus and his paper included a key (pp. 256–257) to the genera and subgenera of Heterochelina (= Hopliina).
Subtribe HOPLIINA Latreille, 1829
Swain & Prinsloo (Reference Swain and Prinsloo1986) included adults of Hoplia sordita as feeding on Acacia mearnsii. We are not aware of any other references relating to the biology or pest status of Hoplia species in Sub-Saharan Africa, but there is extensive literature on the non-African Hoplia. For example, Ansari et al. (Reference Ansari, Adhikari, Ali and Moens2008) examined the susceptibility of Hoplia philanthus (Füessly) larvae and pupae to entomopathogenic nematodes in Belgium, while Zhang et al. (Reference Zhang, Ma, Yang, Byers, Klein, Zhao and Luoe2011) examined the attractive responses of Hoplia spectabilis Medvedev to un-baited yellow or white cross-pane funnel traps in China.
Tribe PACHYDEMINI Burmeister, 1855
Omer-Cooper et al. (Reference Omer-Cooper, Whitnall and Fenwick1941) noted that southern Africa turf (golf courses) is a human-made habitat often composed of the indigenous grass (Cynodon dactylon Pers.), and thus its pests are endemic, opportunistically making use of an abundant food resource. The damage caused by white grubs when they feed on grass roots, completely ‘scalps’ the roots and can result in death of the grass, especially following a dry period. Larvae of species of Macrophylla are potential pests of golf greens in the Eastern Cape of South Africa (Omer-Cooper et al., Reference Omer-Cooper, Whitnall and Fenwick1941).
Omer-Cooper et al. (Reference Omer-Cooper, Whitnall and Fenwick1941, Reference Omer-Cooper, Whitnall and Fenwick1941–1942, Reference Omer-Cooper, Whitnall and Fenwick1948) provided notes on the biology of species of Macrophylla, where the females of atleast some of the species appear to be flightless. Fenwick (Reference Fenwick1947) redescribed the male of M. pubens and provided the first description of its flightless female based on specimens collected on the Humewood Golf Green near Port Elizabeth, South Africa. Schoeman (Reference Schoeman, Way and du Toit1996) recorded that white grubs in turfgrass are ‘usually patchily distributed, unpredictable and capable of doing severe damage before they are detected’. Due to the incorrect identification of Hypopholis sommeri (now Pegylis sommeri) as Macrophylla ciliata and published as M. ciliata in Petty's earlier papers, the larva of M. ciliata (but actually P. sommeri) was described by Smith et al. (Reference Smith, Petty and Villet1995). However, this is actually a redescription of the larva of P. sommeri (see Prins, Reference Prins1965). Consequently, we are not aware of any descriptions of southern African Pachydemini larvae (here we exclude Sparrmannia flava covered by Evans (Reference Evans1989) and Scholtz (Reference Scholtz1988), due to the preferred placement of Sparrmannia in the Melolonthini).
Evans (Reference Evans1988a ) reviewed the taxonomy and systematics of southern Africa Pachydemini and revised some genera (Evans, Reference Evans1987a , Reference Evans b , Reference Evans c , Reference Evans1988b ). Lacroix provided descriptions of many new African Pachydemini genera and species in 14 papers (Lacroix, Reference Lacroix1997, Reference Lacroix1999, Reference Lacroix2001, Reference Lacroix2003, Reference Lacroix2004, Reference Lacroix2005a , Reference Lacroix b , Reference Lacroix2006a , Reference Lacroix b , Reference Lacroix c , Reference Lacroix d , Reference Lacroix2008e , Reference Lacroix2008 f, Reference Lacroix2011) and a catalogue (Lacroix, Reference Lacroix2007).
Tribe MELOLONTHINI Leach, 1819
Subtribe MELOLONTHINA Leach, 1819
Swain & Prinsloo (Reference Swain and Prinsloo1986) included Psilonychus groendahli on Acacia mearnsii in a list of phytophagous insects on forest trees and shrubs in South Africa. Specimens of Psilonychus were collected in pheromone traps set to catch the lepidopterous pest Helicoverpa armigera (African Bollworm) from chicory fields in the Eastern Cape of South Africa (Midgley et al., Reference Midgley, Hill and Villet2008, Midgley, personal communication). There are eight described species of Psilonychus and Harrison (in preparation) plans to revise this genus, making its species and what we know about them accessible to other entomologists.
The adults of three Sparrmannia species (S. acicularis, S. flava and S. transvaalica) were recorded in the vicinity of pistachio nut trees in the Prieska area of the Northern Cape of South Africa by Louw (Reference Louw2001). However, only S. flava caused economic damage by defoliating trees, thereby forcing them to produce new leaves. It is suspected that this regrowth reduced the ultimate nut yield of trees (Louw, Reference Louw2001). Haddad et al. (Reference Haddad, Dippenaar-Schoeman and Pekár2005) and Haddad & Louw (Reference Haddad and Louw2006) recorded the spider groups present in pistachio orchards in South Africa and noted their potential as biological control agents for pistachio pests. Sparrmannia species are caught in spiders’ webs (Harrison, personal observations) and thus one can expect that both large sedentary and orb-weaving spiders would catch and feed on Sparrmannia adults. Scholtz (Reference Scholtz1988) investigated the breeding biology of S. flava in the arid Kalahari and noted that, under desert conditions, the life cycle is 1 year in duration. Larvae are able to maximize feeding after rain and then become dormant until rain allows them to feed again. Quite unique for the melolonthines, or perhaps just unrecorded due to the absence of studies on African arid chafers, is the larval behaviour of foraging at night on the soil surface for antelope dung, which is then taken below the soil surface, rehydrated and fed upon by these larvae. Evans (Reference Evans1989) summarized what is known about the biology of Sparrmannia. All species appear to feed on plants as adults, but there is a lack of established host plant records, even from mass swarming observations. Of the 24 known species, two appear to be diurnal while many other species have been collected at light traps at night. Mating swarms of S. transvaalica have been observed at dusk, and in the morning and late afternoon (Harrison, personal observations). Evans (Reference Evans1989) provided a detailed and thorough revision of the 24 known species of Sparrmannia and a description of the second instar larvae of S. flava.
Subtribe SCHIZONYCHINA Burmeister, 1855
Larvae of Entyposis impressa were recorded by Mansfield-Aders (Reference Mansfield-Aders1920) feeding on the roots of caladiums and castor oil plants. Lacroix & Montreuil (Reference Lacroix and Montreuil2012) revised Entyposis and recognized nine species in the genus. Male Entyposis are unusual among melolonthines in that they have indented dynastine-like pronota including small pronotal horns making it easy to recognize this genus of African melolonthines.
Von Schmutterer (Reference Schmutterer1964), in an overview of the insect pests on southern Somalian crops, noted larvae of a species of Schizonycha feeding on banana plant roots. Büttiker & Bünzli (Reference Büttiker and Bünzli1957) included Schizonycha profuga, S. citima and Hecistopsilus molitor in their survey of the more important leaf chafers on tobacco in Zimbabwe. Tarr (Reference Tarr1958) examined the relationship between feeding by species of Schizonycha grubs on Dolichos Bean (Dolichos lablab) seedlings, resulting in wilt and often followed by stem blight. They discuss how various chemical seed dressings can reduce losses. In a list of phytophagous insects in South Africa, Swain & Prinsloo (Reference Swain and Prinsloo1986) listed S. fimbriata as associated with Acacia mearnsii. Larvae of S. fimbriata caused damage to soya beans in KwaZulu-Natal (Hittersay, Reference Hittersay2005). In the Trans Nzoia district of Kenya, changes in the intercropping practices to enhance soil nutrition resulted in an increase in the abundance of root-feeding chafer (Schizonycha spp.) grubs (Medvecky et al., Reference Medvecky, Ketterings and Vermeylen2006, Reference Medvecky, Ketterings and Nelson2007; Medvecky & Ketterings, Reference Medvecky and Ketterings2009). Apparently, the enhanced soil nutrition may have benefitted white grubs developing in the soil. In a review of the insect pests associated with yam production and storage, Korada et al. (Reference Korada, Naskar and Edison2010) included unnamed species of Schizonycha larvae as boring into and feeding on the tubers during the pre-harvest period. Hajek et al. (Reference Hajek, McManus and Delalibera Júnior2005) in their ‘Catalogue of introductions of pathogens and nematodes for classical biological control of insects and mites’ listed Paenibacillus popilliae (Dutky) (Bacillaceae) as having been released in 1956 in Kenya for the control of Schizonycha spp. In this instance, P. popilliae was not recovered after release (Hajek et al., Reference Hajek, McManus and Delalibera Júnior2005). Schizonycha is the African equivalent to the diverse Phyllophaga Harris of the New World. Pope (Reference Pope1960) revised the southern African species of Schizonycha, and at that time recorded over 300 described species, with 292 of these being from Africa, and 120 being from southern Africa. Undoubtedly, many undescribed species remain, complicating efforts for routine identification of this important pest containing genus. Lacroix (Reference Lacroix2010) provided a World checklist of 349 species for Schizonycha.
Subtribe PEGYLINA Lacroix, 1989
Harrison (Reference Harrison2014a ) provides a phylogeny for the Pegylina while Harrison (Reference Harrison2014b ) provides detailed coverage of the natural history, pest status, larval description, parasites and previous chemical control of South African Pegylis species. Lacroix (Reference Lacroix2008c , Reference Lacroix d ) described new species of Pegylis and included all known species of Pegylis in his 2010 book.
Subtribe LEUCOPHOLINA Burmeister, 1855
Lepesme & Paulian (Reference Lepesme and Paulian1944) recorded larvae of Afrolepis pygidialis feeding on the roots of Coffea excelsa in Gabon, provided a brief description of the larvae and pupae of A. pygidialis, and a key to the species in the genus. Decelle (Reference Decelle1968) proposed Afrolepis as a replacement name for Oligolepis Brenske, 1903 as the latter generic name was already occupied within the vertebrates. Lacroix (Reference Lacroix2010) provided redescriptions, a key to species, and maps for the five known species of Afrolepis.
Harrison (Reference Harrison2009) provides detailed coverage of the natural history and pest status of Asthenopholis, revises the genus and recognizes seven species of Asthenopholis from these countries: South Africa (five spp.), Lesotho (one), Swaziland (one), Kenya (one), Tanzania (two) and Uganda (one).
The larvae of Cochliotis melolonthoides are considered an important pest of sugarcane in Tanzania (Jepson, Reference Jepson1956). Lacroix (Reference Lacroix2009a ) provided a revision of the four known species of Cochliotis, including the description of a new species from Somalia. Cochliotis species are known from Kenya, Tanzania and Somalia (Lacroix, Reference Lacroix2009a ). Jepson (Reference Jepson1956) discussed the biology, larvae (including third instar head capsule and rastal pattern illustrations) and adults of C. melolonthoides. Additionally, Jepson (Reference Jepson1956) included recommendations for the cultural, biological and chemical control of C. melolonthoides larvae, which are pests of sugarcane in Tanzania. Hajek et al. (Reference Hajek, McManus and Delalibera Júnior2005) listed Paenibacillus popilliae (Dutky) (Bacillaceae) as having been released in 1968 in Tanzania for the control of C. melolonthoides. It is possible that P. popilliae became established, but the presence of an indigenous milky disease confounded conclusive results.
Taylor & Smithers (Reference Taylor and Smithers1959) recorded Eulepida mashona as a pest of Ley pasture in Zimbabwe. ‘In ley farming, the field is alternately used for grain or other cash crops for a number of years and ‘laid down to ley’, i.e., left fallow, used for growing hay or used for pasture for another number of years. After that period it is again ploughed and used for cash/field crops’ (Wikipedia, 2015). Towards the end of the growing season in Zimbabwe, Wilson (Reference Wilson1963, Reference Wilson1972) mentioned that larvae of E. mashona can damage maize plants when the cobs begin to ripen in March. In their list of phytophagous insects on forest trees and shrubs, Swain & Prinsloo (Reference Swain and Prinsloo1986) included E. mashona as associated with Acacia mearnsii. Gomez (Reference Gomez1988) included E. mashona in the list of ‘indigenous and traditional foods in Zimbabwe’. From an IPM perspective eating E. mashona would reduce high populations of this chafer and also provide rural communities with free nutrients. However, Tagwireyi et al. (Reference Tagwireyi, Ball, Loga and Moyo2000) reported a case of cantharadin poisoning presumably caused by ingestion of a blister beetle (Meloidae) by a 4-year-old child in Zimbabwe. The cause of the ingestion is thought to be due to mistaken identification of the edible Eulepida mashona with the blister beetle Mylabris distincta Thomas. Lacroix (Reference Lacroix2008f , Reference Lacroix2009a , Reference Lacroix b , Reference Lacroix c , Reference Lacroix d , Reference Lacroix e , Reference Lacroix2011) revised various genera of Leucopholina. Lacroix (Reference Lacroix2010) covered the 26 known species of Eulepida (including descriptions of three new species); he also provided descriptions, keys, distribution maps and line drawings, including the male genitalia for all 26 species.
Tribe SERICINI Kirby, 1837
Subtribe SERICINA Kirby, 1837
In Nigeria, Pseudotrochalus concolor is associated with the following plant species: Bixa orellana, Citrus acida, Citrus limonia, Gossypium hirsutum, Haematoxylon campechianum, Quisqualis indica, Spondias lutea and Zea mais (Golding, Reference Golding1927, Reference Golding1937). Certain genera of African Sericinae (Ahrens, Reference Ahrens2007a ) are currently being revised (Ahrens personal communication).
Subtribe TROCHALINA Brenske, 1898
In southern Nigeria, Peacock (Reference Peacock1913) recorded several species of Trochalus together with other scarabs on cacao or cocoa beans (Theobroma cacao L.), but he placed these taxa on his list of doubtful significance (associated with the crop but not an actual pest). Hargreaves (Reference Hargreaves1937) recorded T. carinatus, T. gibbus and T. pilula as feeding on avocado, Cola nitida and cotton in Sierra Leone. Swain & Prinsloo (Reference Swain and Prinsloo1986) included T. byrrhinus and T. fulgidus in their list of phytophagous insects of forest trees and shrubs in South Africa for Acacia mearnsii.
Conclusion
Identification of melolonthine white grubs and adult chafers unlocks published information on these taxa and creates the necessary nomenclatural foundation for research into the biology and ecology of the species. This review provides a foundation for taxonomic research on this agriculturally important pest group. Research is required in all areas relating to African white grub and leaf chafers in order to improve our ability to make species level pest identifications, understand their biology and implement IPM strategies when required. It is important to conserve these same species as they are also African endemics and an integral part of the continent's rich biodiversity. Recent work by Ahrens, Bezděk, Conlong, Dittrich-Schröder, Goble, Harrison, Lacroix and Way (see reference list) indicates a positive trend to more taxonomic and applied research being undertaken on South African and southern African scarab pests.
Recommendations
Based on this review of the literature from 1889 (Ormerod & Janson, Reference Ormerod and Janson1889) to the present, the following recommendations can be made to improve the continuity of information relating to African scarab pest taxonomy and associated research in future. These include:
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• inclusion of the following key words in paper titles/keyword lists to facilitate electronic literature searchers, i.e., ‘white grub, leaf chafer, Scarabaeidae, Melolonthinae, Africa and scarab pest’;
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• clear indication of the methods used to establish larvae-to-adult conspecificity, when identifications are provided, e.g., adults bred from larvae, larvae and adults found in association with one another, or via molecular matching techniques;
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• a clear statement of the person responsible (and their professional affiliation) for taxon identifications, e.g., ‘Riaan Stals of the ARC-PPRIFootnote 1 ’; and
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• information on the national museum/research institution in which the vouchers on which the identification is based have been deposited, e.g., ‘ARC-PPRI or SANCFootnote 2 ’.
The supplementary materials for this article can be found at http://www.journals.cambridge.org/BER
Acknowledgements
The authors extend their gratitude to these people and organizations for their contributions to this paper: Darren J. Mann, Gudrun Dittrich-Schroder, Mike Way, Paul Schoolmeesters, Petr Šípek and Tarryn Goble for providing literature; Riaan Stals and Beth Grobbelaar (ARC-PPRI) for access to their extensive pest related beetle reprint collection; Kevin Balkwill allowed JduGH to attend a number of writing retreats at WITS’ Pullen Nature Reserve, where much of the review was written; Irene and Mick Jackson provided funding for the upgrade of facilities at Pullen N.R. making the Jackson Field Station such a pleasant research environment; The WITS Faculty Research Committee and WITS SPARC covered JduGH's research costs. Marcus Byrne (WITS, RSA), Mary Liz Jameson (Wichita State University, USA), Connal Eardley (ARC-PPRI), Simon van Noort (SAMCFootnote 3 ) and Brett Hurley (FABIFootnote 4 ) provided valuable comments to an earlier version of the paper; Dirk Ahrens provided his knowledge and insight into the current taxonomy of the Ablaberini, Sericini and Trochalina. Most importantly, JduGH thanks his family and especially Margaret A.C. Harrison for their love, support and patience while completing his PhD.
