Documenting museum records of West African Coccinellidae (Coleoptera) in Benin and Senegal

Abstract Background This work provides a preliminary inventory of West African Coccinellidae. This was based on the West African Coccinellidae (WAC) specimens in the holdings of insect collections at the Laboratoire de Zoologie des Invertébrés Terrestres at the Institut Fondamental d’Afrique Noire Cheikh Anta Diop (IFAN), Senegal and the Biodiversity Center at the International Institute of Tropical Agriculture (IITAB), Benin. New information A total of 129 species representing 11 tribes and 40 genera is reported, including one species of the subfamily Microweiseinae and 128 species of the subfamily Coccinellinae. The geographic distribution of collection localities is presented for these species. Cheilomenes lunata (Fabricius, 1775), Cheilomenes propinqua (Mulsant, 1850), Cheilomenes sulphurea (Olivier, 1791), Chnootriba elaterii (Rossi, 1794), Chnootriba similis (Thunberg, 1781), Exochomus laeviusculus Weise, 1909, Hyperaspis delicatula (Mulsant, 1850) and Hyperaspis pumila Mulsant, 1850 are the best represented species in these collections.


Introduction
Natural history museums play a critical role in science and education (Gropp 2018, Holmes et al. 2016. They contribute fundamental data, necessary for understanding the biodiversity of Earth across temporal and geographic ranges. Biological information derived from specimen data provides essential information supporting a wide range of basic and applied biological endeavours. Museum specimens often play an important role in the recognition of threatened taxa, allowing the scientific community to propose appropriate action (e.g. Thomson et al. 2018, Mikula et al. 2018. Other activities that benefit from specimen-based biological information include the monitoring of environmental change, protecting public health and safety and enhancing agriculture, to name a few (Suarez and Tsutsui 2004).
In agriculture, biological collections can provide vitally important information about pest species, including phenology, food preferences, behaviour, ecological associations etc. (Escalona et al. 2017). For invasive species, museum data can help to identify the point of entry, the date of introduction, the rate of expansion and the native distributional range, which is where natural enemies (potential biocontrol agents) might be found.
The full benefits of natural history museums can only be realised if these collections are known and accessible to the public and scientific communities worldwide, thereby enabling cooperation between local and distant scientists to explore and advance our knowledge of global biodiversity. Unfortunately, access to biological collections is limited for researchers in some regions, like Africa. Much of the available museum material of African origin is housed in natural history museums or private collections in Europe (Klopper et al. 2002, Miller andRogo 2001). There are some major African national or regional natural history museums. The majority of their holdings comprise subsets of material that was collected by missionaries, explorers and scientists from European institutions (Medler 1980, Scholtz andMansell 2017). There are some natural history museums in West Africa, but these have remained overlooked by the research community.
Coccinellidae Latreille, 1807, commonly known as ladybugs, are small beetles ranging from 0.8 to 18 mm (Seago et al. 2011). Although some coccinellids are phytophagous or fungivorous (Iperti 1999), nearly 70% of species are considered predaceous, preying on aphids, mealybugs, scale insects, thrips, leaf hoppers, mites and other soft bodied insects (Giorgi et al. 2009, Riddick 2017, Shah and Khan 2014, Ślipiński and Tomaszewska 2010 Although Africa is well known for its rich and charismatic vertebrate diversity, there is far less appreciation for the great diversity of other taxa there. It is estimated that 100,000 species of insects are currently known from the continent and conservative estimates put the total number of insect species there at about 600,000, yet few research collections of insects exist on the continent (Miller and Rogo 2001). While entomological research collections in some African countries (e.g. Algeria, Egypt, Ghana, Kenya, Libya, Malawi, Morocco, Mozambique, South Africa, Tanzania, Uganda and Zambia) have appeared for some time in registries of museums (e.g. Arnett et al. 1993, Evenhuis 2019, others remain virtually unknown to the outside world, especially those in French West African countries (Afrique Occidentale Française). This is true for the two largest reference collections of arthropods in West Africa, the Biodiversity Center at the International Institute of Tropical Agriculture (IITAB) in Benin and the Laboratoire de Zoologie des Invertébrés Terrestres at the Institut Fondamental d'Afrique Noire Cheikh Anta Diop (IFAN) in Senegal. These two important resources were absent from compilations of insect and spider collections of the world until just recently when they were added to a web-based listing of biological collections by Evenhuis (2019) following an enquiry by the senior author.
The Laboratoire de Zoologie des Invertébrés Terrestres (formerly Section Entomologie) was created in 1945 by André Villiers. It is housed in the Institut Fondamental d'Afrique Noire Cheikh Anta Diop (IFAN), Université Cheikh Anta Diop, Dakar in Senegal ( Fig. 1a-b). The IFAN insect collection was established to serve as a centre for entomological collection-based research in West Africa. With over 400,000 specimens, the IFAN insect museum is the largest insect collection in West Africa. Dr. Abdoul Aziz Niang, a specialist of Phlebotomine sandflies (Diptera: Psychodidae), is the current Curator and Director of the IFAN insect collection.
The International Institute of Tropical Agriculture (IITA) is a non-profit international research organisation founded in 1967. Headquartered in Ibadan, Nigeria, IITA is a member of the Consultative Group for International Agricultural Research. IITA has stations and hubs in Central, Eastern, Southern and West Africa (www.iita.org). The IITAB, IITA Biodiversity Center (formerly IITA insect centre or museum) is housed at the Benin Station of IITA in Calavi, Cotonou,. With over 365,000 specimens, the IITAB collection is the second largest insect collection in West Africa. Dr. Georg Goergen, Entomologist and Biosystematist, is the current Curator and Director of the IITAB.
The taxonomic impediment, which affects biologists around the world, impacts West African researchers especially hard. Most African scientists must rely on distant experts for the identification of insect specimens. Africa produces far fewer trained insect taxonomists than any other continent in the world (de Carvalho et al. 2005). This gap in taxonomic knowledge has also limited the assessment of biodiversity in Africa (Coleman 2015). Currently, the Biodiversity Center of IITA, Benin (IITAB) is one of the major insect identification hubs in Africa.
The IFAN and IITA insect collections are the two largest in West Africa, a region situated between the Tropic of Cancer and Equator, covering 6,140,000 km , approximately one 2 Figure 1.
Photos of the two largest West African insect museums: a. IFAN, outside view of the museum; b. IFAN, inside view of the museum showing insect boxes; c. IITAB, outside view of the museum; d. IITAB, inside view of the museum showing insect cabinets and drawers. fifth of Africa. More than 75% of the land consists of plains lying below an elevation of 300 m. The region includes 16 countries: Benin, Burkina Faso, Cape Verde, Côte d'Ivoire, Gambia, Ghana, Guinea, Guinea-Bissau, Liberia, Mali, Mauritania, Niger, Nigeria, Senegal, Sierra Leone and Togo. Additionally, the United Nations recognises Saint Helena (a United Kingdom Overseas Territory), Ascension and Tristan da Cunha as part of West Africa (Comité Inter-états de Lutte contre la Sécheresse dans le Sahel 2016, Kabo-bah and Diji 2018) (Fig. 2).
Given the importance of coccinellids and the patchy knowledge of their diversity in West Africa, we summarised data about the taxonomic holdings of this family in IFAN and IITAB insect collections with the goals of raising the visibility of those institutions and providing a preliminary inventory of West African Coccinellidae (WAC). This work represents part of ongoing research on the WAC by the senior author, who is currently developing a formal taxonomic catalogue of West African Coccinellidae.

Materials and methods
Museum specimens were studied at the IFAN and IITAB insect collections in West Africa. We photographed specimens and recorded label data (e.g. taxonomic determination, collection locality, collection date, associated plants, collector, determiner etc.).
The taxonomic names that were recorded on museum specimens were put in a database and updated to currently valid names using the systematics literature. Aberrations, Documenting museum records of West African Coccinellidae (Coleoptera) in ... variations and subspecies were not included in the database except when museum specimens were identified as such. References are provided, when appropriate, to clarify the current classification for species. In some cases, specimen determinations were made (by KH) using the literature along with examination of reference collections of authoritatively identified material at the Musée Royal de l'Afrique Centrale (MRAC), Museum für Naturkunde der Humboldt-Universität (ZMHB), Museum of Comparative Zoology (MCZ), National Museum of Natural History (NMNH) and University of Georgia Collection of Arthropods (UGCA). Annotations are given when an invalid determination on a specimen label has been updated to the currently valid taxonomic name.
Many museums and institutions kindly assisted this study by hosting visits, providing data or initiating loans of specimens for this and related studies. These collections and institutions include the following: The updated specimen database was used to produce the first list of West African coccinellid diversity (Table 1) and to explore general characteristics about the museum holdings. Valid taxonomic names and tribal placement follow Seago et al. (2011). Generic and species names are arranged alphabetically. The lists of synonyms provided below valid names are not exhaustive, but instead include only junior synonyms that have been used in literature regarding West African taxa or ones that appear on specimen determination labels in the focal collections.

Analysis
The taxonomically updated list of coccinellid species, present in the IFAN and IITAB collections, includes 129 species, representing 40 genera assigned to 11 tribes and two subfamilies following the classification of Seago et al. (2011). A total of 751 West African coccinellid specimens was recorded for the two collections. Of those, 385 specimens (68 spp., 30 genera) are deposited at IITA, while 366 specimens (84 spp., 31 genera) are at IFAN Table 1.
Most specimens (62%) were curated under currently valid names; however, 38% of specimens were labelled using junior synonyms. At IITA, 83% of the specimens were labelled using currently valid species names, while at IFAN, 39% of specimens were labelled using valid names.

Temporal distribution
Coccinellid material in the IFAN and IITA insect collections differ in temporal coverage (IFAN: 1900(IFAN: -1994IITAB: 1950IITAB: -2009 (Fig. 7). In the IFAN collection, the oldest specimens were all collected in 1900 and represent the following species: Both collections show a spike in growth of coccinellid holdings during one decade, but not the same one (Fig. 7). While 17% of the IFAN WAC specimens were collected between 1900 and 1944, the great majority (73%) were collected between 1945 and 1954. Only 5% of the specimens were added between 1955 and 1994. No new coccinellid material has been added since 1994. The IITAB WAC records indicate that 6% of specimens were collected between 1950 and 1979, 80% from 1980 to 1989 and 14% between 1990 and 2009. No new coccinellid material was added after 2009.

Discussion
Data records compiled from collection labels in the IFAN and IITAB insect collections show that both collections combined provide an historical record of West African coccinellid diversity spanning over a century. It is clear that much coccinellid diversity in this region remains unrecorded though.
Very little published information is available about African coccinellids. Fürsch (1992) reports 70 species from Western Uganda. In Algeria, 75 species were recorded (Lakhal et al. 2018). The West African region, with its surface area of 6,140,000 km , is nearly 26 times the size of Uganda (236,040 km ) and more than twice the size of Algeria.
West Africa, with its diverse ecosystems, landscapes, bioclimatic regions and vegetation (desert, rain forest, savannah), should support one of the highest diversities of coccinellids in all of Africa. The current total of 129 known coccinellid species from West Africa is surprisingly low for such a heterogeneous region. The two focal collections of this study, the largest biodiversity centres in West Africa, differ in their taxonomic coverage. The IFAN holds more West African coccinellid diversity (31 gen., 84 spp.) than IITA (30 gen., 68 spp.). One possible explanation for the higher taxonomic diversity at IFAN is that their coccinellid records span nearly a century  while records at IITA only range from 1950 to 2009. In addition, the holdings at IFAN were enhanced by many expeditions to other West African countries, especially Côte d'Ivoire, Liberia, Mali, Mauritania, Senegal and Togo (Paulian et al. 1983).
A species name can become invalid due to the discovery of an older valid name or due to subsequent reclassification of the species in a different genus. Even though there was more taxonomic diversity represented at IFAN, 61% of species names used in the collection have not been updated to the valid names used in the current classification. At IITAB, however, most coccinellid species names (83%) were current and valid. It should also be noted that the various researchers, who have served as curators of IFAN insect collection, were taxonomists. Even though their expeditions and fieldwork focused on insect biodiversity in general, their efforts were concentrated on their respective specialities. These researchers each left Africa after some time and were no longer involved in the curation of these collections (e.g. André Villiers: 1945-1956, Michel Condamin: 1950-1973and 1978-1988Roger Roy: 1958-1992, Bernadette Soltani: 1988, Aïssatou Dramé: 1988-1991, Sun Heat Han: 1992-1996. These are some of the potential reasons why the taxonomy of the coccinellid holdings at these museums was not current. The IITA arthropod collection plays a crucial taxonomic role by providing essential, authoritative insect identifications amongst other services (e.g. biodiversity monitoring, pest management control etc.). IITA research has contributed to the description of more than 120 arthropod species (Ortiz 2017). This position of the IITA helps to explain why the identifications of its WAC specimens are more current: the IITAB WAC collection is newer than the one at IFAN.
Considering the numbers of specimens, Exochomus (6%), Chnootriba (9%), Scymnus (13%), Cheilomenes (14%) and Hyperaspis (15%) are the most strongly represented West African genera in the two collections. Cheilomenes lunata, Cheilomenes propinqua, Cheilomenes sulphurea, Chnootriba elaterii and Chnootriba similis are the most commonly collected species. Whereas Cheilomenes lunata, C. propinqua and C. sulphurea are widespread aphid predators, Chnootriba elaterii and Ch. similis are serious herbivorous pests of major staple crops. All these species may have been collected more often because they are relatively large, more colourful than many other coccinellids in the region and are regularly occurring on many cultivated and wild plants. In contrast, the collection, preparation and identification of tiny, brown coccinellids, like Scymnus species, are more difficult and time consuming. Drab, minute coccinellids could have been abundantly collected in field samples, but might never have been prepared, identified and curated. As a result, these less conspicuous coccinellids could be greatly under-represented in museum holdings even though they might be very common and important in various agroecosystems.
Many predaceous species are represented in the holdings, such as Exochomus flavipes (Thunberg, 1781), Exochomus laeviusculus Weise, 1909, Stethorus jejunus Casey, 1899, Hyperaspis delicatula, H. pumila, Rodolia cardinalis (Mulsant, 1850 and Scymnus senegalensis Weise, 1913. Some of these species are poorly represented in these collections, but this is likely due to collection and preparation biases, rather than actual rarity in the region. Although these relative abundance numbers of specimens in the collections are not the result of systematic and long-term sampling efforts, the simple spatial and temporal records of occurrence for these species in the region provide important information that could facilitate entomological research and pest management programmes in the sub-region.
Records of material in both IFAN and IITAB show that more than 60% of WAC specimens were collected from five countries (Senegal, Nigeria, Benin, Liberia and Côte d'Ivoire). These countries might have experienced more collecting effort because they either house the museums (Benin and Senegal) or because they are neighbouring countries where museum expeditions could be easily conducted (Côte d'Ivoire, Liberia, Nigeria). Benin, Côte d'Ivoire, Nigeria and Senegal have been agricultural research and trade centres in West Africa since the colonial period (Paulian et al. 1983). IFAN (Senegal), IITA (Benin, Nigeria) and ORSTOM (Côte d'Ivoire) were originally established to promote scientific research before the 1950s. Studies conducted through those organisations have continued to be published in more recent years (Chazeau and Couturier 1985, Fürsch 1991a, Saethre et al. 2011, generating specimens for the museums.
The collecting efforts that built these museum holdings were haphazard, not the result of long-term, systematic monitoring efforts in the region. More than 23% of IITAB WAC specimens were collected from the IITA Station in Ibadan, Nigeria, while 17% of IFAN WAC were collected in Dakar, Senegal. Despite the high historical value of both collections, the geographic record is uneven. Some countries were far more heavily sampled over the years than others.
The coccinellid material housed in both collections is diverse, but there is a surprising lack of overlap in taxa between the two collections, even though they are in neighbouring countries that have similar ecological habitats. At IFAN, there are 56 WAC species that are not present in IITAB. There are 35 WAC species represented in the IITAB holdings that are not found in the IFAN collection. The lack of overlap could be due to collecting biases in the projects or expeditions that occurred at each institution. A large percentage of taxa represented in these museums was collected by only a few individuals (Fig. 3) which is consistent with that scenario. In fact, the combined WAC diversity at these two collections (40 genera, 129 species), represents only 75% of genera and 50% of the species already known to occur in the region as reported in the literature (KH). This lack of overlap between collections may be due in part from being at an early stage of discovery and collection development for WAC diversity. It is clear that there is a need for much more thorough study and sampling in order to accurately assess the diversity of this important group across West Africa.
It is noteworthy that both collections include African coccinellids from outside West Africa. The IITAB also has material from Central and South America (Bolivia, Columbia, Guatemala and Mexico). These non-West African specimens were probably received as exchanges between international collaborators who were conducting general systematics research or were collaborating with the various Insect Pest Management programmes carried out by IITA. These collaborations with researchers from around the world might help to explain why the identifications of material at IITAB were taxonomically more current than at IFAN. In fact, most of the IITAB coccinellids were identified by a German researcher, Helmut Fürsch, a taxonomic authority of Afrotropical Coccinellidae.
The noteworthy periods of development for the IITAB WAC collection were 1950-1979, 1980-1989 and 1990-2009. Not surprisingly, IFAN's slower growth in the 1960s coincided with the lowest rate of growth for IITA's new collection. In the late 1970s, however, there were major pest outbreaks (e.g. Maize streak virus, cassava mealybug, cassava green mite, mango mealybug, fruit tree mealybug etc.) that led IITA scientists to establish collaborative integrated pest management programmes with Central and South American researchers at the International Center for Tropical Agriculture (CIAT) (Agounké et al. 1988, Ortiz 2017). These biological control programmes were very successful in importing, rearing and releasing natural enemies to manage these pests (Agounké et al. 1988, Ortiz 2017. During research trials for those projects, insects were sampled from agricultural lands. In fact, more than 40% of WAC specimens in the IITA museum were collected between 1979 and 1989 on cassava alone. It is likely that many coccinellids in the IITA collection were collected because the 1970s pest outbreaks pushed the institution to establish partnerships with stakeholders, international researchers and other African research institutions. From 1990 to the present, records from the IITA museum show a very significant decrease in the number of coccinellids collected. This decreased rate of growth could be explained by the spectacular success of the biological pest control programme carried out by IITA on cassava, mango trees and other crops, thereby reducing the need for field sampling. In addition to the identified material referred to in the present paper, there is still a huge backlog of unidentified coccinellid specimens at IITAB. The non-WAC specimens obtained at that same time are another benefit from those same events and resulting collaborations. Despite the success of IPM programmes and taxonomic expeditions led by IFAN and IITA in many African countries, it is clear that some groups of West African coccinellid genera with high known diversity were poorly sampled (e.g. species of Adalia, Anisolemnia, Clitostethus, Coccinella, Diomus, Megalocaria, Micraspis, Nephus, Psyllobora, Rodolia, Scymnus etc.). For example, 22 species of Nephus have been reported to occur in West Africa (KH), yet only 6 are represented in these collections.
This gap in taxonomic knowledge about lady beetles mirrors the situation seen in many other insect taxa in West Africa. The assessment of biodiversity in the region has been hampered historically by a lack of local taxonomic expertise, inaccessibility of scientific literature, rarity of reliable arthropod reference collections, limited scientific infrastructure and a lack of financial resources. Recent advances in systematics, especially in "cybertaxonomy," now provide web-based taxonomic tools, diverse publication outlets and easy access to a wealth of digitised scientific resources including technical literature, high quality photographs, specimen data etc., thereby reducing the taxonomic impediment for researchers in places like West Africa. If coupled with strategic development of international, institutional collaborations to conduct biodiversity surveys and inventory projects, great progress could be made towards filling large taxonomic and geographical gaps in our knowledge of West African insects.