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Comparing Classical and Geometric Morphometric Methods To Comparing classical and geometric morphometric methods to discriminate between the South African honey bee subspecies Apis mellifera scutellata and Apis mellifera capensis (Hymenoptera: Apidae) Tomas Bustamante, Benjamin Baiser, James D. Ellis To cite this version: Tomas Bustamante, Benjamin Baiser, James D. Ellis. Comparing classical and geometric morphome- tric methods to discriminate between the South African honey bee subspecies Apis mellifera scutel- lata and Apis mellifera capensis (Hymenoptera: Apidae). Apidologie, 2020, 51 (1), pp.123-136. 10.1007/s13592-019-00651-6. hal-03060423 HAL Id: hal-03060423 https://hal.archives-ouvertes.fr/hal-03060423 Submitted on 14 Dec 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Apidologie (2020) 51:123–136 Original article * INRA, DIB and Springer-Verlag France SAS, part of Springer Nature, 2019 DOI: 10.1007/s13592-019-00651-6 Comparing classical and geometric morphometric methods to discriminate between the South African honey bee subspecies Apis mellifera scutellata and Apis mellifera capensis (Hymenoptera: Apidae) 1 2 1 Tomas BUSTAMANTE , Benjamin BAISER , James D. ELLIS 1Entomology and Nematology Department, University of Florida, Gainesville, FL 32611, USA 2Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, FL 32611, USA Received 28 June 2018 – Revised 11 February 2019 – Accepted 26 April 2019 Abstract – There are two endemic subspecies of western honey bees (Apis mellifera L.) in the Republic of South Africa (RSA), A.m. capensis and A.m. scutellata . They have traditionally been identified using morphometric characteristics, but geometric morphometric data from honey bee wings are easier to collect, possibly making them a useful alternative for identifying these subspecies. We compared the accuracy of both morphometric and geometric morphometric methods using linear discriminant and classification and regression tree analyses. We found that using geometric wing shape data from both forewings and hindwings resulted in a lower classification accuracy (73.7%) than did using models derived from the full set of standard morphometric data (97% accurate) in cross-validation. Tergite color and average ovariole number were the most important features for discriminating between the two subspecies. Finally, we used Kreiger interpolation to construct maps illustrating probable distributions of A.m. capensis and A.m. scutellata in the RSA. Apis mellifera capensis / Apis mellifera scutellata / Morphometrics / Wing geometry / Discrimination 1. INTRODUCTION 1998). These two subspecies are considered pests in some regions where they are not endemic (Allsopp Apis mellifera scutellata (Lepeletier 1836), the 2003; Beekman et al. 2012; Dietemann et al. 2006; African or Savannah honey bee, and Apis mellifera Schneider et al. 2003). capensis (Eschscholtz 1822), the Cape honey bee, Apis mellifera capensis is native to the Fynbos are two western honey bee subspecies native to the ecoregion of RSA (Du Preez 2014). Its natural Republic of South Africa (RSA) (Hepburn 2002) distribution is bound by mountain ranges and the where their natural distributions overlap to create a natural distribution of A.m. scutellata to the north stable hybrid zone (Crewe et al. 1994; Hepburn et al. (Hepburn and Crewe 1991) and the Atlantic and Indian Oceans to the south. Apis mellifera capensis Electronic supplementary material The online version of possess a unique phenotype whereby workers can this article (https://doi.org/10.1007/s13592-019-00651-6) produce diploid female offspring without mating contains supplementary material, which is available to (Onions 1912; Lattorff et al. 2005). This trait, known authorized users. as thelytoky, enables A.m. capensis workers to act Corresponding author: T. Bustamante, [email protected]; as social parasites when introduced into apiaries J. Ellis, [email protected] housing colonies of other honey bee subspecies Handling editor: David [email protected] (Velthuis et al. 1990). In this scenario, A.m. capensis 124 T. Bustamante et al. workers can drift to other colonies where they re- analysis and clustering techniques to analyze the produce and drain colony resources without benefit- standard morphometrics data and establish two sep- ing the host (Hepburn and Allsopp 1994; Greeff arate populations in RSA (Ruttner 1988). Hepburn 1997). Host colonies eventually die, at which point et al. (1998) went further by using jackknifed linear the remaining A.m. capensis workers disperse to discriminant analysis to estimate probability scores other colonies (Allsopp 1998; Neumann et al. for each colony in order to classify some colonies as 2001). The ability of A.m. capensis to parasitize hybrids of the two subspecies. colonies of other subspecies of honey bees makes Developing models that can discriminate be- it a potential threat to manage honey bee populations tween these two honey bee subspecies using stan- outside of its native range. dard morphometric data is laborious and time Apis mellifera scutellata is native to south and consuming due to the challenges associated with south-central Africa, where it is the primary subspe- dissecting and measuring the various anatomical cies used for honey production because it outcom- features of the bees. The purpose of our study was petes other introduced subspecies in that region to attempt to overcome these difficulties using (Johannsmeier 2001). It was introduced into Brazil geometric morphometric data collected from wing in the late 1950s in an effort to increase honey vein intersections as landmarks (wing geometry). production there (Schneider et al. 2003). Since that Wing geometry has been used before to dis- time, the feral population (called “African,”“Afri- criminate between several other subspecies of canized,” or “killer” honey bees) has spread through- honey bees, namely A.m. intermissa , A.m. out South and Central America and into the south- sahariensis , A.m. carnica , A.m. ligustica , A.m. western United States of America (USA) and parts of mellifera , A.m. scutellata , A.m. carnica , A.m. FL, USA. It has become the subspecies of choice for caucasica , and Africanized honey bees (Barour beekeepers in South and Central America (Schneider and Baylac 2016; Francoy et al. 2008; Tofilski et al. 2003). In these areas, the bees out-compete 2008). This approach works by laying morpho- European subspecies as producers of honey and logically common characteristics, forewings in providers of pollination services (Winston 1993). this case, on a Cartesian plane. The resulting x – Apis mellifera scutellata is considered an invasive y coordinates of common landmarks, such as the pest in North America, however, because of its pro- wing vein intersections, are used in lieu of tradi- nounced defensive behavior and general lack of tional morphometric data after being rotated, productivity in temperate climates (Schneider et al. resized and aligned (Slice 2007). Both types of 2003; Guzman-Novoa and Page 1994). In North morphometric data, standard and wing geometry, America, extensive efforts have been made to iden- can be analyzed similarly and used for subspecies tify, monitor, and control the use of this subspecies in identification purposes (Meixner et al. 2013). managed colonies (Rinderer et al. 1993, 1983). Linear discriminant analysis (LDA) and classi- Monitoring for either of these two subspecies is fication and regression tree (CART) analysis are problematic in regions where they co-occur because two ways of analyzing morphometric data that they are difficult to distinguish from one another were tested in the present study. LDA produces a qualitatively (Ruttner 1988). Both bee subspecies function, or equation, that can be used to give each have been classified historically using morphometric colony a score based on the morphometric data techniques outlined by Ruttner (1988), hereafter measured. The benefit of LDA is that the score referred “standard morphometrics.” Standard mor- given by a discriminant function can be converted phometrics involves quantifying various external into a probability score showing the likelihood features of each specimen, such as wing length or that a sample belongs to a given group, allowing number of hamuli, and using those measurements in the identification of specimens that fall between multivariate analyses to identify populations of the groups. LDA was used to develop the Universal bees. Some internal features, namely ovariole num- System for Detecting Africanization Through ber and spermathecal size, also have been used in Identification Based on Morphology (USDA-ID) comparative studies of A.m. capensis and A.m. and the Fast Africanized Bee Identification Sys- scutellata . Ruttner used principal component tem (FABIS), two methods used to discriminate Comparing methods to discriminate African bees 125 Table I. Sampling information for each apiary in the Republic of South Africa from which A.m. scutellata and A.m. capensis samples were collected City number City Sample size of apiaries
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