Arthropod Structure & Development 52 (2019) 100877 Contents lists available at ScienceDirect Arthropod Structure & Development journal homepage: www.elsevier.com/locate/asd Using controlled vocabularies in anatomical terminology: A case study with Strumigenys (Hymenoptera: Formicidae) Thiago S.R. Silva*, Rodrigo M. Feitosa
, Francisco Hera
clito dos Santos Ave., Curitiba, PR, Brazil Department of Zoology, Universidade Federal do Parana a r t i c l e i n f o a b s t r a c t Article history: Received 11 March 2019 Received in revised form 23 July 2019 Accepted 24 July 2019 Available online xxx Morphological studies of insects can help us to understand the concomitant or sequential functionality of complex structures and may be used to hypothetize distinct levels of phylogenetic relationship among groups. Traditional morphological works, generally, have encompassed a set of elements, including descriptions of structures and their respective conditions, literature references and images, all combined in a single document. Fast forward to the digital era, it is now possible to release this information simultaneously but also independently as data sets linked to the original publication in an external environment. In order to link data from various fields of knowledge, disseminating morphological information in an open environment, it is important to use tools that enhance interoperability. For example, semantic annotations facilitate the dissemination and retrieval of phenotypic data in digital environments. The integration of semantic (i.e. web-based) components with anatomic treatments can be used to generate a traditional description in natural language along with a set of semantic annotations. The ant genus Strumigenys currently comprises about 840 described species distributed worldwide. In the Neotropical region, almost 200 species are currently known, but it is possible that much of the species' diversity there remains unexplored and undescribed. The morphological diversity in the genus is high, reflecting an extreme generic reclassification that occurred in the late 20th and early 21st centuries. Here we define the anatomical concepts in this highly diverse group of ants using semantic annotations to enrich the anatomical ontologies available online, focussing on the definition of terms through subjacent conceptualization. © 2019 Elsevier Ltd. All rights reserved. Keywords: Morphology Ants Ontology Semantic annotation Terminology 1. Introduction In biology, morphology is used to describe or redescribe taxa
a and Branda ~o, (Fernandes et al., 2014; Pinheiro et al., 2016; Ulysse 2012); to determine phenotypic traits linked to certain pathologies (Ortiz et al., 2017; Fiaz et al., 2018); to infer kinship among lineages in phylogenetic analyses (Fusari et al., 2014; Ramos and Melo, 2010; Zacca et al., 2016); to trace phenotypic variation during ontogenetic development (Thompson, 1999; Toyama et al., 2018); to investigate functional community organization (Gibb and Parr, 2013; Gibb ~o, 2014); to explore evolutionary hyet al., 2015; Silva and Branda potheses within anatomical groups (Kawada et al., 2015; Boudinot, 2013, 2018). The morphological terminology used by different * Corresponding author. E-mail addresses: tsranzanidasilva@gmail.com (T.S.R. Silva), rsmfeitosa@gmail. com (R.M. Feitosa). https://doi.org/10.1016/j.asd.2019.100877 1467-8039/© 2019 Elsevier Ltd. All rights reserved. research groups for related organisms, however, may differ (Silva, 2017), making analyses of broader groups based on comparative morphology very difficult (Deans et al., 2012). Morphology is the product of multiple factors. Some are intrinsic to individuals, such as the expression of differential traits through gene modularity and hormone variation throughout the ontogenetic development (Corona et al., 2016; Molet et al., 2012), while others are extrinsic, for instance climatic oscillations and environmental heterogeneity (Oms et al., 2017; Purcell et al., 2016). For this reason, morphological studies result in complex data sets that have been historically challenging in terms of referencing (Vogt et al., 2010). Morphological works generally include descriptions of traits and their conditions, literature references, images and hypotheses about trait evolution. Morphologists establish connections between specimens and their anatomic features, using images and text to document what they see. They also make interpretations and advance hypotheses. In traditional morphological publications, all 2 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 those elements are combined in a single document. In modern times, however, there is the possibility of releasing data sets in an external environment that is linked to the original publication and making them available to a broader scientific community (Deans et al., 2012; Godfray, 2002; Miller et al., 2012; Padial et al., 2010). In order to link data from various fields of knowledge in an open environment, tools such as semantic annotations can be used to enhance interoperability and to facilitate the dissemination and retrieval of phenotypic data in digital environments (Silva, 2017). Semantic annotation is the process of attaching additional information to various concepts (e.g., terms, organisms etc) in a given text or any other content. These annotations link multiple concepts across different domains inside a digital environment and can be easily retrieved and used by machines. For example, they can be used in ontology-based information retrieval queries for efficient data mining, thus facilitating the spread of the current understanding of a specific concept to multiple domains (Silva, 2017). These annotations are possible because there are multi-species anatomic ontologies (i.e. data models which represent a set of concepts belonging to a specific domain, along with their relations), which contain definitions of anatomic concepts that are logically related (Dahdul et al., 2010). Annotations are logically composed using references to these anatomic concepts along with descriptive concepts from other ontologies. They make it possible, for example, to understand which processes are involved in the evolution of anatomic traits (Mabee et al., 2007). The taxonomic and morphological diversity in Hymenoptera (ants, bees, and wasps), combined with various researchers focussing on projects in multiple domains, has led to the creation of several anatomical glossaries within the order (Yoder et al., 2010). The morphological terminology used for the group is, for the most part, family-specific (Seltmann et al., 2012), and it is not at all uncommon for a structure to be named differently across publications (e.g., “paramere” Yoder et al., 2010; see Boudinot, 2018 for a throughout discussion of genital terminology in Hexapoda) depending on the hymenopterists' community the publication originated from (Yoder et al., 2010). Despite the fact that anatomic studies in myrmecology have become less common with the advent of molecular endeavours and the development of robust analytic tools to understand variation at the molecular level (Keller, 2011), new-generation tools have become more popular in anatomical studies and have enabled the generation of fine-grained morphological data on the external and internal morphology of ants (Agavekar et al., 2017; Sarnat et al., 2016; Staab et al., 2018) in ways that are useful to other disciplines, such as biomechanics, ecology, behavioural and developmental biology (e.g., Gibb and Parr, 2013; Keller et al., 2014; Larabee and Suarez, 2014; Larabee et al., 2017; Molet et al., 2012; Silva and ~o, 2014). Branda The ant genus Strumigenys, with 840 described species distributed worldwide, is most diverse in the tropics (Bolton, 2000, 2019). Their great morphological diversity (Baroni Urbani and de Andrade, 1994, 2007) reflects the fact that a number of genera that were historically kept separate have been synonymized with it in the late 20th and early 21st centuries (cf. Bolton, 2000 for a historical overview of the taxonomic history for the genus). New publications in the last fifteen years (Baroni Urbani and De Andrade, 2007; Bharti and Akbar, 2013; Lattke and Aguirre, 2015; Longino, 2006; Rigato and Scupola, 2008; Sosa-Calvo et al., 2010; Xu and Zhou, 2004; Zhou and Xu, 2003) have added approximately 30 valid names to the genus, indicating a crescent e although, seemingly slow e rate of new species discovery for this group, and the possibility that more species will be described in the future. The present work defines anatomical concepts in Strumigenys using semantic annotations to enrich the anatomical ontologies available online, focussing on the definition of terms through subjacent conceptualization. For this, we perform a morphological investigation to substantiate previous definitions, and to establish structural correspondence between the studied group and other groups of ants and hymenopteran insects. 2. Material and methods 2.1. Sample information The specimens used in this study were obtained from the following institutions: CASC California Academy of Sciences, San Francisco, CA, USA. ~o Entomolo
gica Padre Jesus Santiago Moure, UniDZUP Coleça
, Curitiba, PR, Brazil. versidade Federal do Parana ~o Paulo, Sa ~o MZSP Museu de Zoologia da Universidade de Sa Paulo, SP, Brazil.
ria, ES, Brazil. UFES Universidade Federal do Espírito Santo, Vito For the study of comparative morphology, 11 Formicidae subfamilies were studied, namely Agroecomyrmecinae, Amblyoponinae, Dolichoderinae, Dorylinae, Ectatomminae, Formicinae, Myrmicinae, Paraponerinae, Ponerinae, Proceratiinae, and Pseudomyrmecinae. At least one specimen of each subfamily, apart from Myrmicinae, was thoroughly studied in search of morphological characteristics (Table 1). In Myrmicinae, at least one specimen for three tribes (Crematogastrini, Pogonomyrmecini and Solenopsidini), apart from Attini, were studied in search of morphological characteristics (Table 1). In Attini, at least one specimen of the following genera, apart from Strumigenys, were studied: Acromyrmex Mayr, 1865, Acanthognathus Mayr 1887, Basiceros Schulz, 1906, Octostruma Forel, 1912, Phalacromyrmex Kempf, 1960, Pheidole Westwood 1839, and Procryptocerus Emery, 1887. In Strumigenys, at least one specimen of each of the 74 species was observed (Table 1). Species belonging to this genus were arbitrarily chosen as to tentatively explore most of the morphological diversity present in the genus. Bolton (2000) recognizes several groups of species, using morphological traits to diagnose them. Since some representatives of those groups are not usually present in samples, and we opted to dissect and disarticulate most of the examined specimens, we used those species which were considered abundant in samples and were readily available for study. Other non-formicide Hymenoptera were also examined, reflecting the most recent hypothesis of relationship among hymenopteran families, to encompass a wide range of morphological diversity within the order (Branstetter et al., 2017a; Peters et al., 2017) (Table 1). 2.2. Equipment Morphological observations were made with a Leica S8APO stereomicroscope at 80 magnification. Scanning electron microscope images were obtained using an electronic microscope Tescan Vega3 LMU, under both low and high pressure. The method provided by Boudinot (2015) was used for mouthpart dissection and body disarticulation. The methods of Gibson (1985) and Vilhelmsen et al. (2010) were used in the study of the skeleton and musculature. The specimens were immersed in 100% alcohol one day prior to dissection for complete dehydration. After the dehydration process, the specimens were transferred to ethanol-immersed BluTack, which allowed better handling. All the dissections were performed using a razor blade and size zero entomological pins. 3 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 Table 1 List containing all species studied (Family, Subfamily, Tribe, Species), sex of specimens studied, morphological form (apterous, brachypterous or macropterous), their collection of origin, their conservation medium (dry-mounted or ethanol) and their locality information (COUNTRY: Department/Province, Municipality). Species Apidae Apinae Meliponini Melipona sp. Bethylidae Epyrinae Epyrinae sp. Pristocerinae Pristocerinae sp. Ceraphronidae Ceraphronidae sp.1 Ceraphronidae sp.2 Diapriidae Diapriinae Diapriinae sp. Diapriini Acanthopria sp. Eucharitidae Eucharitinae Eucharitini Kapala sp. Evaniidae Semaeomyia sp. Ichneumonidae Ophioninae Ophioninae sp. Mutillidae Sphaerophtalminae Sphaerophtalminae sp. Pompilidae Pepsinae Pepsinae sp. Pteromalidae Cleonyminae Cleonyminae sp. Vespidae Polistinae Epiponini Polybia sp. Formicidae Agroecomyrmecinae Agroecomyrmecini Tatuidris tatusia Amblyoponinae Amblyoponini Fulakora armigera Dolichoderinae Tapinomini Tapinoma melanocephalum Dorylinae Labidus coecus Ectatomminae Ectatommini Gnamptogenys sp. Formicinae Camponotini Camponotus atriceps Paraponerinae Paraponerini Paraponera clavata Ponerinae Ponerini Pachycondyla striata Proceratiinae Proceratiini Discothyrea sexarticulata Pseudomyrmecinae Pseudomyrmecini Pseudomyrmex sp. Myrmicinae Crematogastrini Crematogaster sp. Sex Form Collection of origin Conservation medium Locality information Female Macropterous DZUP Ethanol
, Curitiba BRAZIL: Parana Male Macropterous DZUP Ethanol FRENCH GUIANA: Saint-Laurent-du-Maroni, Saül Female Apterous DZUP Ethanol
, Antonina BRAZIL: Parana Female Female Macropterous Brachypterous DZUP DZUP Ethanol Ethanol
, Piraquara BRAZIL: Parana
, Piraquara BRAZIL: Parana Female Macropterous DZUP Ethanol
, Piraquara BRAZIL: Parana Female Apterous DZUP Ethanol
, Piraquara BRAZIL: Parana Male Macropterous DZUP Ethanol
, Antonina BRAZIL: Parana ? Macropterous DZUP Ethanol BRAZIL: Santa Catarina, Blumenau Male Macropterous DZUP Ethanol BRAZIL: Santa Catarina, Blumenau Female Apterous DZUP Ethanol
, Curitiba BRAZIL: Parana Female Macropterous DZUP Ethanol BRAZIL: Rio Grande do Sul, Gramado Male Macropterous DZUP Ethanol BRAZIL: Santa Catarina, Blumenau Female Macropterous DZUP Ethanol
, Curitiba BRAZIL: Parana Female Apterous DZUP Dry-mounted PERU: Madre de Dios, Puerto Maldonado Female Apterous DZUP Dry-mounted BRAZIL: Rio de Janeiro, Itatiaia Female Apterous DZUP Ethanol
, Curitiba BRAZIL: Parana Female Apterous DZUP Ethanol
, Antonina BRAZIL: Parana Female Apterous DZUP Ethanol BRAZIL: Rio Grande do Sul, Gramado Female Apterous DZUP Ethanol BRAZIL: Santa Catarina, Blumenau Female Apterous DZUP Dry-mounted ~es BRAZIL: Mato Grosso, Chapada dos Guimara Female Apterous DZUP Ethanol
, Curitiba BRAZIL: Parana Female Apterous DZUP Dry-mounted
, Tibagi BRAZIL: Parana Female Apterous DZUP Ethanol BRAZIL: Rio Grande do Sul, Gramado Female Apterous DZUP Ethanol BRAZIL: Santa Catarina, Blumenau (continued on next page) 4 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 Table 1 (continued ) Species Sex Form Collection of origin Conservation medium Locality information Female Apterous DZUP Ethanol
, Antonina BRAZIL: Parana Female Apterous DZUP Ethanol
, Curitiba BRAZIL: Parana Female Female Female Female Female Female Female Female Apterous Apterous Apterous Apterous Apterous Apterous Apterous Apterous DZUP DZUP DZUP DZUP DZUP DZUP DZUP DZUP and MZSP Ethanol Dry-mounted and ethanol Dry-mounted Ethanol Dry-mounted Ethanol Ethanol Dry-mounted Strumigenys alberti Strumigenys appretiata Female Female DZUP DZUP Dry-mounted Dry-mounted and ethanol Strumigenys beebei Female DZUP Dry-mounted and ethanol
, Curitiba Parana ^ nia, Porto Velho Rondo Santa Catarina, Indaial
, Tunas Parana Santa Catarina, Painel
, Curitiba Parana Rio Grande do Sul, Gramado Santa Catarina, Indaial
, Bocaiúva do Sul Parana ~o, Açaila ^ndia Maranha ~o Grande S~ ao Paulo, Ribeira Rio de Janeiro, Itatiaia ^ nia, Porto Velho Rondo Strumigenys borgmeieri Female DZUP and MZSP Dry-mounted Strumigenys carinithorax Strumigenys cincinatta Strumigenys comis Female Female Female MZSP DZUP DZUP and MZSP Dry-mounted Dry-mounted Dry-mounted Strumigenys conspersa Strumigenys cordovensis Female Female Apterous Apterous and macropterous Apterous and macropterous Apterous and macropterous Apterous Apterous Apterous and macropterous Apterous Apterous BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: DZUP DZUP and MZSP Dry-mounted Dry-mounted Strumigenys cosmostela Strumigenys crassicornis Female Female MZSP DZUP Dry-mounted Dry-mounted and ethanol ^ nia, Porto Velho Rondo Sergipe, Areia Branca ~o Pessoa Paraíba, Joa ^ nia, Porto Velho Rondo Rio de Janeiro, Itatiaia Santa Catarina, Canoinhas ^ nia, Porto Velho Rondo ^ nia, Porto Velho Rondo Pernambuco, Recife
polis S~ ao Paulo, Saleso Rio de Janeiro, Itatiaia Strumigenys cultrigera Strumigenys dapsilis Strumigenys denticulata Female Female Female MZSP MZSP DZUP Dry-mounted Dry-mounted Dry-mounted and ethanol BRAZIL: Rio Grande do Sul, Bom Jesus ~o Bento do Sul BRAZIL: Santa Catarina, Sa
, Piraquara BRAZIL: Parana Strumigenys dentinasis Female Apterous Apterous and macropterous Apterous Apterous Apterous and macropterous Apterous BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: DZUP and MZSP Dry-mounted Strumigenys depressiceps Strumigenys eggersi Female Female Macropterous Apterous DZUP DZUP and MZSP Dry-mounted Dry-mounted and ethanol Strumigenys elongata Female Apterous DZUP Dry-mounted and ethanol Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys emiliae emmae epelys epinotalis fridericimuelleri glenognatha godmani grytava gytha Female Female Female Female Female Female Female Female Female Apterous Macropterous Apterous Apterous Apterous Apterous Macropterous Apterous Apterous DZUP UFES MZSP MZSP MZSP DZUP DZUP DZUP DZUP and MZSP Dry-mounted Ethanol Dry-mounted Dry-mounted Dry-mounted Dry-mounted Dry-mounted Dry-mounted Dry-mounted Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys hindenburgi hyphata infidelis inusitata kompsomala lanuginosa Female Female Female Female Female Female Apterous Apterous Apterous Apterous Apterous Apterous and macropterous Apterous Apterous Apterous Apterous Apterous and macropterous MZSP DZUP DZUP DZUP DZUP DZUP Dry-mounted Dry-mounted Dry-mounted Dry-mounted and ethanol Dry-mounted Dry-mounted MZSP DZUP DZUP DZUP DZUP Dry-mounted and ethanol Dry-mounted Dry-mounted and ethanol Dry-mounted Dry-mounted ~o Grande ao Paulo, Ribeira BRAZIL: S~
, Bocaiúva do Sul BRAZIL: Parana FRENCH GUIANA: Saint-Laurent-du-Maroni, Saül BRAZIL: Minas Gerais, Boa Esperança
us BRAZIL: Bahia, Ilhe BRAZIL: Acre, Senador Guiomard ~o, Estreito BRAZIL: Maranha BRAZIL: Santa Catarina, Indaial
ria BRAZIL: Espírito Santo, Vito ~o ao Joa BRAZIL: Bahia, Mata S~ BRAZIL: Minas Gerais, Pedra Azul
ia BRAZIL: S~ ao Paulo, Canane ^ nia, Porto Velho BRAZIL: Rondo FRENCH GUIANA: Saint-Laurent-du-Maroni, Saül
va ~o BRAZIL: Sergipe, S~ ao Cristo BRAZIL: Sergipe, Malhador ~o Pessoa BRAZIL: Paraíba, Joa BRAZIL: Rio Grande do Sul, Morro Reuter PERU: Madre de Dios, Puerto Maldonado
s, Caldas Novas BRAZIL: Goia ^ nia, Porto Velho BRAZIL: Rondo ^ nia, Porto Velho BRAZIL: Rondo
, Piraquara BRAZIL: Parana BRAZIL: Rio de Janeiro, Itatiaia BRAZIL: Bahia, Milagres PERU: Madre de Dios, Puerto Maldonado
, Curitiba BRAZIL: Parana BRAZIL: Rio de Janeiro, Ilha Grande BRAZIL: Santa Catarina, Indaial MZSP DZUP DZUP MZSP MZSP DZUP DZUP MZSP DZUP Dry-mounted Dry-mounted Dry-mounted Dry-mounted Dry-mounted Dry-mounted Dry-mounted Dry-mounted Dry-mounted BRAZIL: Santa Catarina, Blumenau ~o, Açaila ^ndia BRAZIL: Maranha ^ nia, Porto Velho BRAZIL: Rondo
BRAZIL: Santa Catarina, Chapeco BRAZIL: S~ ao Paulo, Mirassol ^ nia, Porto Velho BRAZIL: Rondo PERU: Madre de Dios, Puerto Maldonado BRAZIL: S~ ao Paulo, Tapiraí FRENCH GUIANA: Saint-Laurent-du-Maroni, Saül Pogonomyrmecini Hylomyrma sp. Solenopsidini Solenopsis sp. Attini Acromyrmex crassipisnus Acanthognathus sp. Basiceros disciger Octostruma rugifera Phalacromyrmex fugax Pheidole sp. Procryptocerus sp. Strumigenys abditivata Strumigenys lilloana Strumigenys longimala Strumigenys louisianae Strumigenys pr. louisianae Strumigenys pr. louisianae “bruchi complex” Strumigenys lygatrix Strumigenys metopia Strumigenys monstra Strumigenys minuscula Strumigenys ogloblini Strumigenys perparva Strumigenys planeti Strumigenys precava Strumigenys prospiciens Female Female Female Female Female Female Female Female Female Female Female Female Female Female Apterous Apterous Apterous Apterous Apterous Apterous Apterous Apterous Macropterous 5 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 Table 1 (continued ) Species Sex Form Collection of origin Conservation medium Locality information Strumigenys reticeps Female Apterous DZUP and MZSP Dry-mounted Strumigenys rotogenys Strumigenys rugithorax Strumigenys saliens Female Female Female Apterous Apterous Apterous DZUP MZSP DZUP and MZSP Dry-mounted Dry-mounted Dry-mounted and ethanol Strumigenys sanctipauli Strumigenys schmalzi Female Female Apterous Apterous MZSP DZUP and MZSP Dry-mounted Dry-mounted and ethanol Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys schulzi signeae smilax smithii subedentata pr. sublonga teratrix trinidadensis trudifera urrhobia wheeleriana villiersi xenochelyna zeteki sp.n.1 (fe) Female Female Female Female Female Female Female Female Female Female Female Female Female Female Female DZUP DZUP MZSP DZUP DZUP DZUP DZUP DZUP DZUP DZUP DZUP DZUP DZUP DZUP MZSP Dry-mounted Dry-mounted Dry-mounted Dry-mounted and ethanol Dry-mounted and ethanol Dry-mounted Dry-mounted Dry-mounted Dry-mounted and ethanol Dry-mounted Dry-mounted Dry-mounted Dry-mounted Dry-mounted Dry-mounted Strumigenys Strumigenys Strumigenys Strumigenys Strumigenys sp.n.2 sp.n.3 sp.n.4 sp.n.5 sp.n.6 Female Female Female Female Female Apterous Apterous Apterous Apterous Apterous Apterous Apterous Apterous Apterous Apterous Apterous Apterous Apterous Apterous Apterous and m acropterous Apterous Apterous Apterous Apterous Apterous ~o Paulo, Ribeira ~o Grande BRAZIL: Sa ~o Paulo, Mogi das Cruzes BRAZIL: Sa MALAYSIA: Sabah, Maliau Basin BRAZIL: Santa Catarina, Blumenau BRAZIL: Santa Catarina, Blumenau
, S~
dos Pinhais BRAZIL: Parana ao Jose ~o Paulo, Saleso
polis BRAZIL: Sa
, Jari BRAZIL: Para ~o Pessoa BRAZIL: Paraíba, Joa ~o Paulo, Sete Barras BRAZIL: Sa MALAYSIA: Sabah, Maliau Basin ^ nia, Porto Velho BRAZIL: Rondo ^ nia, Porto Velho BRAZIL: Rondo BRAZIL: Rio de Janeiro, Itatiaia PERU: Madre de Dios, Puerto Maldonado BRAZIL: Sergipe, Nossa Senhora das Dores ^ nia, Porto Velho BRAZIL: Rondo ^ nia, Porto Velho BRAZIL: Rondo BRAZIL: Santa Catarina, Painel
n, Cerro Los Caracoles VENEZUELA: Falco ^ nia, Porto Velho BRAZIL: Rondo BRAZIL, Tocantins, Porto Nacional ^ nia, Porto Velho BRAZIL: Rondo
, Tunas BRAZIL: Parana MZSP MZSP MZSP and CASC MZSP MZSP Dry-mounted Dry-mounted Dry-mounted Dry-mounted Dry-mounted BRAZIL: BRAZIL: BRAZIL: BRAZIL: BRAZIL: (ele) (fast) (gib) (ro) (se) 2.3. Morphological data All morphological information presented in this work refer to morphemes (Richter and Wirkner, 2014) and are without functional or evolutionary implications. Morphemes are characterized as representations of the smallest morphological unit at a particular level of description and are useful to reference morphological characteristics as secondary data. Each anatomical entity is represented by a class (i.e. concept), a definition, and class relationships (i.e. the record that links two concepts via a class relationship). Anatomical classes for Hymenoptera were recovered from the Hymenoptera Anatomy Ontology (Yoder et al., 2010; HAO version 26.iv.2018), while phenotypic quality classes are based on the Phenotypic Quality Ontology (PATO version 07.ii.2018). Class relationship types are based on the OBO Relations Ontology (OBOREL 2018; version 11.vii.2018) (Table 2). All ontologies are made available through the Open Biomedical Ontologies Foundry. The list of terms used in the current work and their definitions can be found in the Table 3. Morphological definitions are constructed as genus-differentia, which are definitions structured to first describe a more inclusive class of concepts (genus) and then the characteristics differentiating (differentia) it from another subordinate of that same concept (Seltmann et al., 2012). Definitions in this format usually follow the pattern “The x that is y” (cf. Boudinot, 2018, Appendix A). To refer to the distinct morphological forms commonly found in female ants we opted to use the terms apterous and macropterous rather than workers and queens/gynes, respectively. Since the last Minas Gerais, Viçosa Santa Catarina, Palhoça ~o Paulo, Piedade Sa
, Tunas Parana ~o Bahia, Mata S~ ao Joa two concepts are intrinsically related to colonial and reproductive € lldobler and Wilson, 1990), we refrain from using them, function (Ho based on the premise that the external morphology alone is not sufficient to infer reproductive aptitude (Silva and Feitosa, 2018). The recognition criterion applied in this study to determine the biological sex of the specimens is purely anatomical, through the observation of external elements of the genitalia; in our case, we observed the distal section of the modified ovipositor (i.e. tip of the sting apparatus). 2.4. Recovering classes from natural language statements Each examined structure was described through natural language statements and variations found were discussed when pertinent. The description process was performed simultaneously by both authors in order to increase agreement during coding procedures. The descriptions were automatically parsed and concepts were recovered from each ontology using two tools: the Analyze tool from the Hymenoptera Anatomy Ontology portal (http://portal.hymao.org/projects/32/public/ontology/analyze) (Seltmann et al., 2013) for recognition of anatomical classes; and Bioportal's Annotator (https://bioportal.bioontology.org/annotator) (Shah et al., 2009) for recognition of phenotypic quality classes. Both tools recognize input natural language statements, parsing down textual data and recovering specific classes based on a defined set of dictionaries (in our case, ontologies). The output data are normally exported as CSV, JSON, or XML formats, and contains the classes recognized from the input text, along with their definitions and/or unique resource identifiers (URIs). Classes not Table 2 Object (class relationship types) and annotation properties used in the annotation of anatomical classes. Property Definition is_a part_of has_related_synonym A subsumption object property. Represents a transitive, reflexive and anti-symmetric relation between two or more classes. A composition object property. Represents a transitive, reflexive and anti-symmetric relation between two or more classes. An aggregation annotation property. Represents a predicate between a class and a literal. 6 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 Table 3 List of terms, their definitions, and their respective ontology identifiers. To recover definitions of classes and annotations through the OBO Foundry, include http://purl. obolibrary.org/obo/before the identifier (e.g., http://purl.obolibrary.org/obo/PATO_0000402). Term Definition Ontology identifier acetabulum anatomical cluster anatomical entity The area that is concave and accommodates the base of a segment. The anatomical group that has its parts adjacent to one another. Biological entity that is either an individual member of a biological species or constitutes the structural organization of an individual member of a biological species. Anatomical structure consisting of at least two non-overlapping organs, multi-tissue aggregates or portion of tissues or cells of different types that does not constitute an organism, organ, multitissue aggregate, or portion of tissue. Material anatomical entity which has inherent 3D shape and is generated by coordinated expression of the organism's own genome. A shape quality inhering in a bearer by virtue of the bearer's having at least one salient angle on the margin. The fossa that is located on the anterior coxal articular process of the mesotrochanter and accommodates the anterior trochanteral condyle of the mesocoxa. The fossa that is located anteriorly on the metatrochanter and accommodates the anterior trochanteral condyle of the metacoxa. The fossa that is located anteriorly on the proximal margin of the protrochanter accommodating the anterior trochanteral condyle of the procoxa. The foramen that is located on the head in which the radicle is positioned. The scrobe that is located dorsally of the antennal foramen and is for the reception of the antenna. The anatomical structure of the cuticle that is delimited by material or immaterial anatomical entities. A surface feature shape inhering in a surface by virtue of the bearer's being divided by ridge-like structures into a number of small, irregular spaces. The projection that bears the articular surface. The lobe that is connected proximodorsally with the manubrium and proximoventrally with the planta. The sulcus that corresponds to the basicosta. The area that is located on the coxa proximal to the basicostal suture. The tarsomere that is the proximal most annulus of the tarsus, connected proximally with the tibia and distally with the second tarsomere via membranous conjunctivae. The condyle that is located on the pectus and inserts into the pectal fossa of the coxa. A size quality inhering in a bearer by virtue of the bearer's being made wider or larger in all dimensions. The dicondylic joint that is composed of the femur and the tibia. The anatomical space that is surrounded by sclerites and allows for the passage of haemolymph, nerves and tracheae. The carina that extends along the lateral margin of the intertorular area towards the vertex. The anatomical cluster that is composed of two sclerites connected by at least one articulation and the articular membrane located connecting the two sclerite. The fossa that is located laterally on the proximal margin of the coxa and accommodates the lateral coxal condyle of the pectus. The area that extends between the anterior eye margin and the anterolateral margin of the cranium, and its width is delimited by the width of the mandible. The fossa that is located anteriorly on the proximolateral edge of the mandible and accommodates the pleurostomal coondyle. The sclerite that is located proximodorsally on the pretarsus and connects the distodorsal margin of the telotarsus with the dorsal part of the arolium. The articular process that is located on the ventral margin of the mesopectus medially of the mesocoxal foramen and bears the medial coxal condyle of the mesopectus. The articular process that is located on the ventral margin of the metapectus medially of the metacoxal foramen and bears the medial coxal condyle of the metapectus. The coxal condyle of the pectus that inserts into the medial pectal fossa of the coxa. The pectal fossa of the coxa that accommodates the median coxal condyle of the pectus. The discrimen that is located in the mesothorax and corresponds with the mesodiscrimenal lamella. The sclerite that is U-shaped in cross section, connected anteriorly with the pronotum and the propectus, dorsally with the basalare, the mesonotum, the second axillary sclerite and the subalare, posteriorly with the metapectus and bears the mesodiscrimenal lamella and the mesofurca. The area that is located anteriorly of the metapleural sulcus and ridge. A shape quality inhering in a bearer by virtue of the bearer's being perfectly circular. The sclerite that is located proximoventrally on the pretarsus and is connected proximally with the unguitractor plate and distally with the arolium. The condyle that is located on the anterior (dorsal) margin of the pleurostoma and inserts into the mandibular acetabulum. The mandibular muscle that arises posterodorsally from the cranium and inserts on the tendon attached anteroproximally on the mandible. The anatomical cluster that is apical to the telotarsus and composed of the empodium, auxilia, planta, pulvillum, unguis, unguitractor plate, auxiliar sclerite and manubrium. The basisternum that is located in the propectus. The carina that delimits posteriorly the pronotal neck. HAO_0000082 HAO_0000041 HAO_0000000 anatomical group anatomical structure angular anterior coxal fossa of the mesotrochanter anterior coxal fossa of the metatrochanter anterior coxal fossa of the protrochanter antennal insertion antennal scrobe area areolate articular process arolium basicostal suture basicoxite basitarsus coxal condyle of the pectus dilated femoro-tibial joint foramen frontal carina joint lateral pectal fossa of the coxa malar area mandibular acetabulum manubrium medial coxal articular process of the mesopectus medial coxal articular process of the metapectus medial coxal condyle of the pectus medial pectal fossa of the coxa mesodiscrimen mesopectus metapectus orbicular planta pleurostomal condyle posterior cranio-mandibular muscle pretarsus probasisternum pronotal carina HAO_0000054 HAO_0000003 PATO_0001977 HAO_0001433 HAO_0001501 HAO_0001500 HAO_0001022 HAO_0001432 HAO_0000146 PATO_0002295 HAO_0000150 HAO_0000148 HAO_0000174 HAO_0000175 HAO_0000178 HAO_0001917 PATO_0001571 HAO_0001517 HAO_0000345 HAO_0001533 HAO_0001146 HAO_0001913 HAO_0001393 /HAO_0001391 HAO_0000671 HAO_0001389 HAO_0001388 HAO_0001918 HAO_0001916 HAO_0000545 HAO_0000557 HAO_0000605 PATO_0001934 HAO_0000719 HAO_0000731 HAO_0000745 HAO_0000820 HAO_0001317 HAO_0001031 7 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 Table 3 (continued ) Term Definition Ontology identifier pronotal neck The area of the pronotum that is delimited posterodorsally by an edge and that accommodates the posterior surface of the head. The tibial spur that is located on the fore leg, is curved and together with the probasitarsus forms the strigil. The fossa that is located posteriorly on the proximal margin of the mesotrochanter accommodating the posterior trochanteral condyle of the mesocoxa. The fossa that is located posteriorly on the proximal margin of the metatrochanter and accommodates the posterior trochanteral condyle of the metacoxa. The fossa that is located posteriorly on the proximal margin of the protrochanter accommodating the posterior trochanteral condyle of the procoxa. The area that is located on the sclerite and that is composed of repetitive anatomical structures. The patch that differs from the surrounding region by having denser setae. A shape quality inhering in a bearer by virtue of the bearer's being oblong, with the lower end very much attenuated. The anatomical cluster that is composed of the probasitarsus and calcar. A shape quality inhering in a bearer by virtue of the bearer's being linear, very narrow, tapering to a very fine point from a narrow base. The spur that is curved and projects from the apex of the last tarsal segment on either side of the arolium of the pretarsus. The area that is located proximally on the femur and is delimited by a groove. The leg segment that is located proximal to the femur and distal to the coxa. The sclerite that corresponds to the site of insertion of the flexor of the pretarsus. HAO_0000837 protibial spur posterior coxal fossa of the mesotrochanter posterior coxal fossa of the metatrochanter posterior coxal fossa of the protrochanter sculpture setiferous patch spatulate strigil subulate tarsal claw trochantellus trochanter unguitractor plate recognized by those tools were manually annotated to the Hymenoptera Anatomy Ontology (Table 4). 2.5. Annotation development Annotations were made following a four-step process: 1) Phenotypic and relational classes available in OWL (Web Ontology Language, http://www.w3.org/TR/owl2-overview/) were loaded
ge
4.1 (http://protege.stanford.edu/), an open-source into Prote ontology editor and a knowledge management system; 2) Anno
ge
as tations were manually added to anatomic entities within Prote OWL class expressions using the built-in Manchester syntax (www. w3.org/TR/owl2-manchester-syntax/) editor; 3) After annotation, we used the FaCTþþ reasoner to determine if new annotations did not violate descriptions and axioms across the ontology; 4) Annotated entities were exported as OWL class expressions and individually added to mx (Mx., 2019), a collaborative open-source application that facilitates the construction of ontologies through a multi-feature environment. All phenotype statements in Manchester syntax are available in Table 4. 2.6. Images Illustrations were made using Adobe Illustrator (version CS6), based on images available at AntWeb (2019) and personal observations of the studied material. Antweb images used to prepare the plates have their respective identifier explicitly indicated at the legend of the figure (in the form of CASENT0000000). 2.7. Data repository All data obtained are available through an online open-access repository (https://doi.org/10.6084/m9.figshare.7645400) as .csv and .owl files. Annotations in Manchester syntax can be easily obtained through the ‘annotations.csv’ file. Novel anatomical classes were added to the most recent version of the ‘hao.owl’ file and are deposited as a ‘hao-merged-strumigenys.owl’ file. 3. Results and discussion Terms and definitions for structures, along with their identifiers (i.e. persistent uniform resource locators; purl), which were used HAO_0000875 HAO_0001348 HAO_0001295 HAO_0001297 HAO_0000913 HAO_0000936 PATO_0001937 HAO_0000102 PATO_0001954 HAO_0000989 HAO_0001033 HAO_0001034 HAO_0001043 throughout the text and figures, can be found in Table 3. Annotations for morphological terms discussed in the following sections, along with their definitions, can be found in Table 4. We annotated 35 new anatomical classes based on the study of Strumigenys. From those, 12 were from structures found on the head and its appendages (i.e. mouthparts and antennae), nine were from the mesosoma and its appendages (i.e. legs), 13 were from the metasoma, and one refers to a structure that can occur in more than one body region (i.e. mesosoma and metasoma). Overall, six classes presented one synonym, with one class having two synonyms, totalling seven synonyms. 3.1. Head Ants have the head oriented horizontally towards the longitudinal axis and mouthparts anteriorly-oriented. Hence, the spatial orientation terminology follows those of prognathous insects. The insect head has been divided into different areas (Snodgrass, 1993; Chapman, 1998): frons, vertex, temple, gena, postgena, malar space and occiput. However, these areas are difficult to establish, since their presence and dimensions depend on the presence and position of other structures, such as the compound eyes and ocelli. Most of those areas were named by Kirby and Spencer (1828), but their delimitations, for the most part, are elusive. 3.1.1. Fronto-vertexal area and complex In Hymenoptera, the frons is the area between the epistomal line and the anterior ocellus and limited laterally by the inner margin of
, 2009/2019). Macropterous female and male compound eye (Miko ants generally retain all three ocelli, with the posterior limits of the frons and the anterior limits of the vertex being promptly determined. In apterous ant females, however, the posterior limits of the frons and anterior limits of the vertex cannot be externally defined in most groups, due to the loss of ocelli in this form. Another complex situation found in apterous females is the reduction or loss of the eyes in some groups, making the lateral delimitation of the frons and the dorsal delimitation of the gena somewhat ambiguous (discussed thoroughly in the section “Gena”). In Hymenoptera, the vertex is the area delimited by the intersection of the margin of the compound eyes, the interorbital plane, and the anatomical line tangential to the point on the margin of the 8 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 Table 4 List of terms, their definitions, and annotations expressed in Manchester syntax. Term Definition Annotation Antero-proximal process of the scape Antero-sternite The process that is located near the base on the anterior margin of the scape and is wider or larger in all dimensions The area that is located on an abdominal sclerite and is limited anteriorly by the antecostal sulcus and posteriorly by the transverse impression of the abdominal sclerite. The antero-sclerite that is located ventrally. Antero-tergite The antero-sclerite that is located dorsally. Antero-ventral notch of the mesopectus The notch that is located anteriorly on the ventral margin of the mesopectus. Apical fork The anatomical cluster that is consisted by the apicoventral tooth and the apicodorsal tooth. Apico-dorsal tooth The projection that is located distally on the mandible and limited ventrally by the intercalar tooth or by the apicoventral tooth, forming the apical fork. The projection that is located distally on the mandible and limited dorsally by the intercalar tooth or by the apicodorsal tooth, forming the apical fork. The area of the sclerite that is raised and is divided by ridgelike structures into a number of small, irregular spaces. is_a some process and part_of some sclerite and ‘bearer of’ some dilated is_a some area and part_of some metasoma and part_of some cuticle and has_related_synonym presclerite is_a some antero-sclerite and part_of some metasoma and part_of some cuticle and part_of some sternum is_a some antero-sclerite and part_of some metasoma and part_of some cuticle and part_of some tergum is_a some notch and part_of some mesopectus and part_of some mesosoma and part_of some margin and part_of some sclerite is_a some anatomical cluster and part_of some mandible and part_of some sclerite and part_of some cuticle is_a some tooth and part_of some mandible and part_of some sclerite and part_of some ‘apical fork’ is_a some tooth and part_of some mandible and part_of some sclerite and part_of some ‘apical fork’ is_a some process and part_of some cuticle and part_of some sclerite and ‘bearer of’ some areolate and has_related_synonym spongiform tissue is_a some foramen and part_of some basicoxite is_a some foramen and part_of some disticoxite is_a some area and part_of some coxa Antero-sclerite Apico-ventral tooth Areolate process Basicoxal foramen Disticoxal foramen Disticoxite Fronto-vertexal area Fronto-vertexal complex Intercalar tooth Lateral areolate process of the petiole The foramen that is located proximally on the basicoxite. The foramen that is located distally on the disticoxite. The area that is located on the coxa distal to the basicostal suture. The area of the sclerite that is located between the epistomal line and the occipital carina and limited laterally by the inner margin of the compound eye. The sclerite that is between the epistomal line and the occipital carina and limited laterally by the inner margin of the compound eye. The tooth that is located on the apical fork, limited ventrally by the apico-ventral tooth and dorsally by the apico-dorsal tooth. The areolate process that is located at the lateral margin of the petiole. Lateral areolate process of the abdominal tergum 3 The areolate process that is located at the lateral margin of the abdominal tergum 3. Lateral coxal condyle of the pectus The coxal condyle of the pectus that inserts into the lateral pectal fossa of the coxa. Lateral mandibular articular process The articular process that is located laterally on the proximal margin of the mandible. The scrobe that is located proximally on the mandible and accommodates the anterolateral process of the head. The gland that is located on the metapleuron and opens posteriorly near the propodeal foramen, on the orifice of the metapleural gland. The anatomical space that is situated posteriorly on the metapecto-propodeal complex, lateral to the propodeal foramen. The impression that is located posteriorly to the oral foramen. Lateral mandibular scrobe Metapleural gland Orifice of the metapleural gland Postbucal impression Postero-sclerite Postero-sternite The area of an abdominal sclerite limited anteriorly by the transverse impression of the abdominal sclerite and posteriorly by the posterior margin of the abdominal sclerite. The postero-sclerite that is located ventrally. Postero-tergite The postero-sclerite that is located dorsally. is_a some area and part_of some fronto-vertexal complex has_related_synonym fronto-vertex is_a some sclerite and part_of some frons and part_of some vertex and part_of some cuticle is_a some tooth and part_of some mandible and part_of some sclerite and part_of some cuticle and part_of some ‘apical fork’ is_a some ‘areolate process’ and part_of some metasoma and part_of some ‘abdominal segment 2’ and part_of some cuticle and part_of some sclerite is_a some ‘areolate process’ and part_of some metasoma and part_of some ‘abdominal segment 3’ and part_of some cuticle and part_of some sclerite is_a some ‘coxal condyle of the pectus’ and part_of some pectus and part_of some sclerite and part_of some articulation is_a some ‘articular process’ and part_of some mandible and part_of some sclerite is_a some scrobe and part_of some mandible and part_of some sclerite is_a some gland and part_of and part_of some metapleuron and part_of some body is_a some ‘anatomical space’ and part_of some ‘metapectal-propodeal complex’ and part_of some metapleuron is_a some impression and part_of some sclerite and part_of some integument and part_of some ‘postgenal bridge’ is_a some area and part_of some metasoma and part_of some cuticle and has_related_synonym postsclerite is_a some postero-sclerite and part_of some metasoma and part_of some cuticle and part_of some sternum is_a some postero-sclerite and part_of some metasoma and part_of some cuticle and part_of some tergum T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 9 Table 4 (continued ) Term Definition Annotation Pronoto-mesonotal complex Translucent patch of the frontal carina The sclerite that is located dorsally to the propectus and mesopectus and is composed of the pronotum and mesonotum. The scrobe that is located ventrally on the femur and accommodates the tibia. The translucent patch that is located at the frontal carina. Translucent patch of the metapleuron The translucent patch that is located at the metapleuron. Translucent patch of the ventral antennal scape The translucent patch that is located at the ventral margin of the antennal scape. Transverse carina of the fourth postero-tergite The carina that is located posteriorly to the impression of the fourth abdominal tergite, belonging to the fourth postero-tergite The impression that is located on the external surface of an abdominal sclerite and does not correspond to a ridge. is_a some sclerite and part_of some cuticle and part_of some pronotum and part_of some mesonotum is_a some scrobe and part_of some sclerite and part_of some femur is_a some ‘translucent patch’ and part_of some ‘frontal carina’ and part_of some integument and part_of some cuticle is_a some ‘translucent patch’ and part_of some metapleuron and part_of some integument is_a some ‘translucent patch’ and part_of some scape and part_of some integument and part_of some cuticle is_a some carina and part_of some sclerite and part_of some postero-tergite and has_related_synonym limbus is_a some impression and part_of some metasoma and part_of some sclerite and part_of some integument and has_related_synonym cinctus and has_related_synonym ‘girdling constriction’ is_a some patch and part_of some ‘abdominal sternum 4’ and part_of some metasoma and part_of some integument and part_of some cuticle is_a some ‘areolate process’ and part_of some ‘abdominal segment 2’ and part_of some metasoma and part_of some cuticle and part_of some sclerite is_a some ‘areolate process’ and part_of some ‘abdominal sternum 3’ and part_of some metasoma and part_of some cuticle and part_of some sclerite is_a some notch and part_of some ‘propodeal foramen’ and part_of some ‘metapectalpropodeal complex’ and part_of some margin and part_of some sclerite Tibial scrobe Transverse impression of the abdominal sclerite Transverse patch of the abdominal sternum 4 The patch that is elongated and extends transversely along the anterior portion of the abdominal sternum 4. Ventral areolate process of the petiole The areolate process that is located at the ventral margin of the petiole. Ventral areolate process of the abdominal sternum 3 The areolate process that is located at the ventral margin of the abdominal sternum 3. Ventral notch of the propodeal foramen The notch that is located medially on the ventral margin of the propodeal foraminal margin. anterior ocellus which defines the minimum distance between the anterior ocellus and the oral foramen (Yoder, 2009). Similarly to the frons, the anterior margin of the vertex cannot be externally delimited in apterous females of ants, due to the lack of ocelli in most groups. Muscular organization has been useful to establish structural equivalence in other groups of Hymenoptera (Kawada et al., 2015; Popovici et al., 2014; Zimmermann and Vilhelmsen, 2016) and in male ants (Boudinot, 2013). There have been several studies exploring the internal anatomy of the head of ants, especially in groups with drastic modifications in the cephalic appendages (Gronenberg, 1995, 1996; Gronenberg and Ehmer, 1996; Gronenberg et al., 1997, 1998a,b; Larabee et al., 2017, 2018; Paul and Gronenberg, 1999), high intraspecific morphological variation (Lilico-Ouachour et al., 2018) or novel appendage functionality (Khalife et al., 2018). Since these investigations are mainly focused on the mechanics and physiology of the muscular groups related to the mandibular motion, the cephalic muscular organization in different lineages of ants has remained relatively unexplored, hampering our understanding of the regionalization and sclerite fusion in this tagma. Since we are not confident about the current understanding of the muscular arrangement in ants in a comparative context, and due to our inability to properly define the frons and vertex of apterous females both internally and externally, we opted to refer to them collectively as the fronto-vertexal complex when referring to the structure as an anatomical cluster, and fronto-vertexal area (or fronto-vertex) when referring to the externally observable area of the structure (Table 4). The main distinction between both classes is how they are recognized. An anatomical complex is understood as being an anatomical cluster, which is defined as an anatomical group that has its parts adjacent to one another (Haendel et al., 2008). An anatomical group is understood as an anatomical structure consisting of at least two non-overlapping organs, multi-tissue aggregates or portion of tissues or cells of different types that does not constitute an organism, organ, multi-tissue aggregate, or portion of tissue (Haendel et al., 2008). On the other hand, an anatomical area can be understood as the anatomical structure of the cuticle that is delimited by
, 2009/2019). material or immaterial anatomical entities (Miko Therefore, an anatomical complex can be understood as an assembly of anatomical entities (including cuticle, muscles and apodemes), while an anatomical area can be understood as a twodimensional anatomical entity (e.g., the cuticle) delimited by other anatomical entities (such as anatomical lines, anatomical spaces, or anatomical structures). In Strumigenys the fronto-vertexal area can be easily delimited laterally even in species with reduced eyes (Fig. 1). Although variable in size and antero-posteriorly positioned, the compound eyes are rarely displaced in a dorso-ventral axis. 3.1.2. Gena The gena in hymenopterans is the area delimited by the intersection of the interorbital plane, the margin of the compound eye, the margin of the oral foramen, the occipital carina and the malar sulcus (Yoder, 2009). It is divided into three other areas, namely the malar area, the gena s.s. and the temple (Fig. 1; ma, gn and tm, respectively) (Boudinot et al., 2013). Internally, it appears to not 10 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 oc oc frvx frvx tm ce fc fc ma fl clp tpfc clp posterior emd apdt fl md md imd emd anterior intt apf apvt ocf pgs pbi tm asc ai dorsal asc tm gn ai ma pbi ventral gn poc ma pbi Fig. 1. Schematic illustration of the head and mandibles of apterous females of Strumigenys. Dotted lines indicate the limits of structures. Dashed lines indicate the limits of areas. Abbreviations: ai: antennal insertion; apdt: apicodorsal tooth; apf: apical fork; apvt: apicoventral tooth; asc: antennal scrobe; ce: compound eye; clp: clypeus; emd: external margin of the mandible; fc: frontal carina; frvx: fronto-vertexal area; gn: gena; imd: internal margin of the mandible; intt: intercalar teeth; ma: malar area; md: mandible; oc: occipital carina; ocf: occipital foramen; pbi: postbucal impression; pgs: postgenal suture; poc: preocular carina; tm: temple; tpfc: translucent patch of frontal carina. T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 correspond precisely to any muscular group, although most of the cranio-mandibular muscle group has its origins in this region. In
et al., 2007) and in Bethylidae (Lanes, 2013), this Scelionidae (Miko area corresponds to the origin sites of the median band of the anterior cranio-mandibular muscle and of the posterior craniomandibular muscle. This condition is similarly found in Formicidae, although there is major variation in muscle size, area of origin, apodeme length, and area of insertion in those muscles depending on the group (personal observation), age of individuals and task repertoire (Muscedere et al., 2011). Mandibular shape appears to be intrinsically related to the characteristics of those muscles, possibly affecting the characteristics of the gena, such as size and shape. In Formicidae, there is a developed median longitudinal ridge that extends from the hypostomal margin to the occipital foramen, referred to by Khalife et al. (2018) as the ventromedial phragma, and appears to be the site of origin of a ventral band of the posterior cranio-mandibular muscle (as in Melissotarsus Emery, 1877 and Myrmoteras Forel, 1893; Khalife et al., 2018 and Larabee et al., 2017, respectively). It varies greatly in height and degree of sclerotization and could probably represent an internal folding of the lateral margins of the postgenal bridge (cf. “Postgenal bridge and postgenal suture section”). In some observed specimens belonging to long mandibulate species of Strumigenys (e.g., Strumigenys saliens Mayr, 1887, Strumigenys elongata Roger, 1863, Strumigenys pr. louisianae), this ridge is reduced but stills represents the site of origin of part of the posterior cranio-mandibular muscle. However, this structure may vary in other species that possess distinct mandibular morphologies. 3.1.3. Postgenal bridge and postgenal suture According to Burks and Heraty (2015), a lot of variation can be found on the subforaminal bridges in Aculeata, and the modifications in cephalic ventral elements in this group have not been properly studied. Internally, the putative lateral margins of the postgenal bridge are greatly expanded in some ants, acting as an attachment site for mandibular muscles (cf. discussion at the Mandible section). The modifications of the postgenal bridge and the reduction of the postgenal suture in various groups of ants are still poorly understood. In view of the high sexual polymorphism found in the family, comparative studies are needed to investigate the modifications in this region. We observed, in Strumigenys, that the postgenal bridge is fused anteriorly. In some species, the postgenal suture (Fig. 1; pgs) is visible only from the occipital carina to the medial region of the ventral surface of the head. Internally, there is a reduced longitudinal ridge spanning from near the occipital foramen to the postgenal inflection anteriorly (in which the labiomaxillary complex rests). In some dissected specimens, part of the medial band of the posterior cranio-mandibular muscle has its origins in this ridge. Compared with other groups that rely on mandibular strength to process resources (such as major females of Pheidole), the longitudinal ridge of Strumigenys is greatly reduced. 3.2. Antenna 3.2.1. Scape Among the female ants observed, the basal antennal segment is usually extremely long when compared with other groups of Hymenoptera (Fig. 2). In most genera of ants, the scape may be as long as the flagellum (Fig. 2; scp and F1-4, respectively). Much of the variation in the scape of different ant groups has remained undocumented. For example, the muscular and glandular aspects of this particular structure in Strumigenys have been broadly overlooked by researchers. 11 One example of variation in the scape that might be informative in Strumigenys can be found on its ventral surface. While some species have an unsculptured patch there (e.g., Strumigenys reticeps (Kempf, 1969) and Strumigenys thaxteri (Wheeler, 1916); Lattke et al., 2018)), others (e.g., Strumigenys alberti Forel, 1893, Strumigenys appretiata (Borgmeier, 1954), Strumigenys borgmeieri Brown, 1954) have this area mostly occupied by a translucent patch. The scape also varies in overall shape (from cylindrical to dorsoventrally flattened) and presence of a dilated process near its base on the anterior margin (Fig. 2; scp) (such as in Strumigenys crassicornis Mayr, 1887). When the dilated process is present, it can be defined as “The process that is located near the base on the anterior margin of the scape and is wider or larger in all dimensions” and named as antero-proximal process of the scape. Rows of erect and decumbent setae on the anterior margin of the scape occur in several species and they can vary from subulate to orbicular. 3.2.2. Flagellum In Hymenoptera, variation in the number of segments of the flagellum is significant, with various conditions of fusion or reduction of segments (Polaszek et al., 1992; Heraty, 2002). In Formicidae, the antennal segments of many groups seem to be fused. Some individuals of some species seem to have asymmetrical numbers of segments (Fischer et al., 2015). There is a slight variation in the number of segments of the flagellum in Strumigenys (Fig. 3AeE), ranging from two to four, possibly representing the more reduced number of flagellar segments in the entire family. In other genera of the tribe, the number varies from five (e.g., Eurhopalothrix) to ten segments (e.g., Basiceros) (Fig. 9). Since we cannot easily trace fusion or reduction of segments in the flagellum based on structural equivalence, previous definitions based on this method are questionable. 3.3. Mouthparts 3.3.1. Labrum In Hymenoptera, the labrum is defined as the sclerite that is situated along the distal margin of the clypeus and is connected along its proximal margin with the distal margin of the epipharyngeal wall (Vilhelmsen and Miko, 2010). In non-formicid hymenopterans it is connected posterodorsally to the clypeus by the clypeolabral articulation, contrasting with the anterior connection found in many other insects. In Formicidae, the position of the clypeolabral articulation varies among groups, but most often it is articulated lateroventrally with the clypeus. In Strumigenys, the labrum is located posteroventrally in relation to the clypeus, as in most groups of ants. Most commonly, the apodeme of the posterior fronto-labral muscle is well-developed and sclerotized, bearing the site of attachment of the posterior fronto-labral muscle, which acts as the retractor of the labrum (Gronenberg, 1996). Since the shape of the labrum is extremely variable within the genus, the apodeme of the posterior frontolabral muscle also appears extremely variable, especially in position, which, although appearing laterally in the sclerite, differs in distance from the clypeolabral articulation (Fig. 2; cllba). The setae located in the labral lobes (Fig. 2; lbl) vary among species, ranging from orbiculate to subulate. Most long-mandibulate species possess long subulate setae that are as long as the mandibles. According to Bolton (1999) the labrum can be modified in two distinct conditions: (i) the labrum lacks lateral processes and the anterior labral lobes are large; and (ii) the labrum is T-shaped (sic), with lateral processes, and the anterior labral lobes are reduced or vestigial. However, J.C.M. Chaul and coworkers (pers. comm.) observed that there is immense variation in shape of the labrum within the genus, even within distinct types of Bolton's 12 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 Fig. 2. Illustration of the labrum in dorsal (top left) and ventral (top right) views and of the antenna in ventral view (bottom) of apterous females of Strumigenys. Abbreviations: afrlb: apodeme of the posterior fronto-labral muscle; amscp: anterior margin of the scape; cllba: clypeo-labral articulation; F1: first segment of the flagellum; F2: second segment of the flagellum; F3: third segment of the flagellum; F4: fourth segment of the flagellum; lbl: labral lobe; lbst: labral seta; lplb: lateral process of the labrum; pdc: pedicel; scp: antennal scape; tpscp: translucent patch of the antennal scape. T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 13 Fig. 3. Variation in the number of antennal segments in specimens of Strumigenys (AeE), Eurhopalothrix (F), Pilotrochus (G) and Basiceros (H). A: Strumigenys anchis CASENT0900916; B: Strumigenys minuscula CASENT0281948; C: Strumigenys clypeata CASENT0103000; D: Strumigenys chroa CASENT0436719; E: Strumigenys ornata CASENT0104478; F: Eurhopalothrix floridana CASENT0003195; G: Pilotrochus besmerus CASENT0047617; H: Basiceros disciger CASENT0914887. 14 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 Fig. 4. Illustration of the mandible in dorsal (top left, top right, and bottom left) and ventral (bottom right) views of apterous females of Strumigenys. Abbreviations: bpm: basal process of the mandible; cmd: carina of the mandible; dia: diastema; dmap: dorsal articular process of the mandible; tpmd: translucent patch of the mandible; vmap: ventral articular process of the mandible. T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 15 Fig. 5. Basal section of the external margin of the mandible of two apterous females of Strumigenys. A: Disarticulated mandible of Strumigenys saliens; B: Mandible inserted in the head of Strumigenys planeti, showing the points were the lateral scrobe of the mandible (marked by asterisks) would approximately contact the head capsule (marked by circles) when the mandible is open. The star indicates the surface of the lateral articular process of the mandible, which is concealed within the oral foramen when the mandible is open. Abbreviations: bpm: basal process of the mandible; dmap: dorsal articular process of the mandible; lmap: lateral articular process of the mandible; lms: lateral scrobe of the mandible; vmap: ventral articular process of the mandible. 16 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 dorsal posterior anterior bcf pc bcs ventral pn bc mti pmsa dc pr fmtp pdsp pmss pd anep pdsr tc fm pdc pdl mtp avnmsp ktep tbs tb tbtp msepc btrtp mspmtps mtppds ptr btr trcl pr pn anterior ppl pmsa pbst avnmsp posterior msp msdm mti mcapms mtp mtdm pd mcapmt pdsp vnpdfr Fig. 6. Illustration of the mesosoma and fore leg of apterous females of Strumigenys. From top to bottom: lateral view, dorsal view and ventral view. Abbreviations: anep: anepisternum; avnmsp: antero-ventral notch of the mesopectus; bc: basicoxite; bcf: basicoxal foramen; bcs: basicostal suture; btr: basitarsus; btrtp: translucent patch of the basitarsus; dc: disticoxite; fm: femur; fmtp: translucent patch of the femur; ktep: katepisternum; mcapms: medial coxal articular process of the mesopectus; mcapmt: medial coxal articular process of the metapectus; msdm: mesodiscrimen; msepc: mesepisternal carina; msp: mesopectus; mspmtps: mesopecto-metapectal suture; mtdm: metadiscrimen; mti: metanotal impression; mtp: metapectus; mtppds: metapecto-propodeal suture; pbst: probasisternum; pc: pronotal carina; pd: propodeum; pdc: propodeal carina; pdl: propodeal lobe; pdsp: propodeal spine; pdsr: propodeal spiracle; pms: pronoto-mesonotal complex; pmsa: pronoto-mesonotal area; pmss: pronoto-mesonotal suture; pn: pronotal neck; ppl: propleura; pr: pronotal rim; ptr: pretarsus; tb: tibia; tbs: tibial spur; tbtp: translucent patch of the tibia; tc: trochanter; trcl: tarsal claw; vnpdfr: ventral notch of the propodeal foramen. T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 17 Fig. 7. Variation in the size of the anteroventral notch of the mesopectus in specimens of Strumigenys (AeC, G and H), Phalacromyrmex (D), Rhopalothrix (E) and Octostruma (H). A: Strumigenys alperti CASENT0003239; B: Strumigenys actis CASENT0005467; C: Strumigenys denticulata CASENT0178117; D: Phalacromyrmex fugax CASENT0103116; E: Rhopalothrix ishtmica CASENT0235905; F: Octostruma stenognatha CASENT0280761; G: Strumigenys inusitata; H: Strumigenys saliens. From A to F the white arrow indicates the position of the anteroventral notch of the mesopectus. In H, the white arrow indicates the position of a small circular impression adjacent to the anteroventral notch of the mesopectus. 18 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 Fig. 8. Image representing the transverse impression of the third abdominal segment in a specimen of Gnamptogenys striatula. Blue: transverse impression of the third abdominal tergite; Green: anterior area of the third abdominal tergite; Red: antecosta of the third abdominal tergite. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.) “mandibular mode of action” in Strumigenys (cf. “Mandible” section). A more in-depth exploration of labral variation has to be addressed as to properly establish structural correspondence of its instances in a broader scenario within the family, so as to enable accurate annotation within multi-species ontologies. The labrum of Strumigenys commonly has setae on the anterior section of the sclerite (Fig. 2; lbst), which in some species appears to play a major role in prey recognition (Gronenberg, 1996). The setae can be orbicular, spatulate or linear, each type occurring alone or in combination with other types. In species in which the labral setae are not linear, several setae are disposed over the anterior half of the labrum, most of them concentrated over the labral lobes. In these cases, we do not know which role they perform and if it is related to prey recognition. The lateral processes (Fig. 2; lplb) can be present or absent; when present, the lateral labral margin appears angular. The lateral processes in Strumigenys have been extensively studied and appear to function as part of the locking mechanism that holds the mandibles wideopen during hunting, interlocking with the proximal processes of the mandible (Brown and Wilson, 1959; Gronenberg, 1996). Similar to other groups of ants (Gotwald, 1969), the anterior fronto-labral muscle is absent, while the paired posterior fronto- 19 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 at3 ptn pt pt3 ptp ps3 dorsal tppt anterior posterior ventral cpt4 pt4 tpps4 ps4 Fig. 9. Illustration of the metasoma in lateral view of apterous females of Strumigenys. Abbreviations: at3: third antero-tergite; cpt4: carina of the fourth postero-tergite; ps3: third postero-sternite; ps4: fourth postero-sternite; pt3: third postero-tergite; pt4: fourth postero-tergite; pt: petiole; ptn: petiolar node; ptp: petiolar peduncle; tpps4: transverse patch of the fourth postero-sternite; tppt: translucent patch of the petiole. 20 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 labral muscles are present and are solely responsible for the retraction of the sclerite. 3.3.2. Mandible Overall, the mandible in Formicidae has three well-defined margins (Bolton, 1994): the masticatory margin, the basal margin and the external margin. The masticatory margin corresponds to the longitudinal margin of each mandibular blade near the anterior extension of the median line of the head. This margin, generally bearing one or more teeth, can be also called apical margin. The teeth can be well-developed or extremely reduced and both types can be found in the same specimen. Normally, the dentition occurs along all the masticatory margin (Bolton, 1994). When there is a space in the teeth row, it is called diastema (Bolton, 1994) (Fig. 4; dia). The base of the masticatory margin finds a basal angle and turns into a transverse or oblique basal margin (Bolton, 1994). The external margin of each mandible can be straight, concave or convex (Bolton, 1994). In most species of ants, the external margins converge anteriorly and become triangular in dorsal view. In some cases, they project anteriorly, in an elongate-triangular shape (Bolton, 1994). When the mandibles are slender and linear, the distinction between the masticatory and basal margins is absent, due to the loss of the basal angle (Bolton, 1999). In some lineages of Formicidae, the mandible is linear, with a long and slender blade and the masticatory and external margins approximately parallel or gradually converging anteriorly (Bolton, 1999). In groups with linear and elongate mandibles, the section with teeth is positioned at the apex of the mandible and is called apical fork (Fig. 1; apf) (Brown, 1948). In their 1994 contribution, Baroni Urbani and de Andrade (1994) asserted that previous authors had never properly defined the apical fork. According to Bolton (2000), in most species with elongate and slender mandibles, the teeth at the apical section commonly form a fork of two or three vertically disposed teeth. Still according to the author, an apical fork is normally composed of two teeth, one dorsal and one ventral, called apicodorsal and apicoventral tooth, respectively (Fig. 1; apdt and apvt, respectively). The tooth that is located between those teeth is called intercalar tooth (Fig. 1; intt). According to Baroni Urbani and de Andrade (1994), one of the important characteristics of Strumigenys is that a pair of acute mandibular blades, dented or pointy, are opposed, but do not overlap. Still according to Baroni Urbani and de Andrade (op. cit.), a putative reduction occurred in the number and/or size of the median and basal teeth until their total loss, normally accompanied by the atrophy of one, or the formation of an apical fork with two or more distal teeth. According to Bolton (op. cit.) the section that receives all teeth positioned apically would correspond to the masticatory margin (e.g. Strumigenys fridericimuelleri Forel, 1886) in species previously classified in Pyramica (a current synonym of Strumigenys), Schmidt and Shattuck (2014) mentioned that in the Ponerinae genera Anochetus Mayr, 1861 and Odontomachus Latreille, 1804, the masticatory margin corresponds to the internal margin of the mandible, in dorsal view. However, in Strumigenys the accurate delimitation of the distinct regions of the mandible can be difficult. The delimitation between the basal and masticatory margins is clear in some species (e.g., Strumigenys alberti, Strumigenys schulzi Emery, 1894, Strumigenys urrhobia (Bolton, 2000)) but not in others (e.g., Strumigenys crassicornis, Strumigenys denticulata Mayr, 1887, Strumigenys elongata Roger, 1863), especially in the case of the masticatory margin and the apical fork. Although this last can be easily observed, according to Bolton (2000), the variation in shape and presence sometimes leads to confusing interpretations. Hence, the term masticatory margin should be avoided, since the structural equivalence in distinct groups of ants cannot be correctly established. On the basal section of the internal margin of the mandible a cuticular process with variable shape and size is normally present, the basal process of the mandible (basimandibular process according to Bolton (2000)) (Fig. 4; bpmd). In some species this structure connects with the dorsolateral margin of the labrum when the mandibles are open, thus locking them and preventing the torsion or displacement of the mandibles while they are open. In some species, there is a translucent patch near the base of the mandible where a putative gland reservoir can be seen through transparency (Fig. 4; tpmd). Internally, the basal section of the mandible has two angled processes, one near the dorsoproximal margin and the other near the ventroproximal margin of each mandible, corresponding, respectively, to the dorsal articular process of the mandible and the ventral articular process of the mandible (Fig. 4; dmap and vmap, respectively). Both processes are responsible for maintaining the mandible in place during mandibular movement. In all observed formicide specimens, there is a lateral dilated process at the external margin of the basal section of the mandible; in Wasmannia affinis, it is understood as the process that bears the posterior cranio-mandibular muscle apodeme (Richter et al., 2019; see discussion below). In Strumigenys, this lateral articular process (abductor swelling in Richter et al., 2019; Fig. 5A, lms) can greatly vary in size (as in some long-mandibulate species, such as Strumigenys godmani, Strumigenys saliens and Strumigenys planeti Brown, 1953), and is limited anteriorly by a lateral mandibular scrobe (Fig. 5A; lms). It is uncertain if this scrobe is structurally equivalent to the mandibular acetabulum found in other hymenopteran groups (e.g., in Opius dissitus and in Biosteres carbonarius; Karlsson and Ronquist, 2012). In species, in which the lateral process is hypertrophied, its dorsal surface (Fig. 5B; star) possibly connects with an internal fossa at the head near the mandibular insertion during mandibular opening. The anterior margin of the mandibular scrobe (Fig. 5B; asterisks) would connect to an anterolateral process at the head of the specimen (Fig. 5B; circles), near the mandibular insertion, holding the mandible into place, preventing its displacement from excessive opening. This lateral process of the head could be structurally equivalent to the pleurostomal condyle in other hymenopteran groups, although overall modification of Strumigenys' head hampers more acurate interpretations of structural equivalence. A similar mechanism has been observed in Acanthognathus rudis (Gronenberg et al., 1998b), although its morphology differs drastically. Mandibular movement occurs by two muscles attached to the external articular margins of the mandibles via two apodemes: the anterior cranio-mandibular muscle apodeme and the posterior craniomandibular muscle apodeme. The anterior cranio-mandibular muscle apodeme receives the anterior cranio-mandibular muscle, which originates at the internal surface of the temple, in the posterodorsal section of the head and inserts on its respective short apodeme. The posterior cranio-mandibular muscle apodeme receives the posterior cranio-mandibular muscle, which originates at the ventromedian region of the head and on the postgenal ridge and inserts on its respective long apodeme. This apodeme is inserted in the lateral mandibular articular process through a membrane, similar to other genera (W. affinis; Richter et al., 2019). According to Gronenberg (1996), the first muscle is responsible for the adduction movement of the mandible, whilst the latter is responsible for the abduction movement of the same structure. 3.3.3. Labiomaxillary complex In Hymenoptera, the labium and maxilla are united posteriorly by a membranous cuticle, forming the labiomaxillary complex T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 (Deans, 2009). In Formicidae, the maxillary palp is composed of 1e6 sclerites, being rarely absent, while the labial palp is composed of 1e4 sclerites (Fisher and Bolton, 2016). According to Gotwald (1969), the galea and the lacinia are broadly joined in members of the family, and although the former is larger than the latter, the lacinia is still conspicuous in ants, compared to the reduced condition found in other families of Hymenoptera. According to Popovici et al. (2014), the anatomical complex comprised by the fusion of the galea and lacinia is termed as galeo-lacinial complex and can be defined as the area of the stipes that is delimited proximomedially by the stipito-premental conjunctiva, proximolaterally by the stipitomandibular conjunctiva and posteroproximally by the margin of the
2014). posterior stipital sclerite (Miko Compared to other Hymenoptera and particularly to Formicidae, the labiomaxillary complex of Strumigenys presents reduction of several sclerites, especially the lacinia, which is poorly sclerotized and broadly joined to the proximolateral galeal sclerite. The lacinial lever, lacinial bar, lacinial lobe and lacinial setiferous patch could not be observed. Regarding the galeal sclerite, this structure is easily distinguished in Strumigenys, with both distolateral and proximolateral galeal setiferous patches well-developed. Although most sclerites of the labium appear fused, they are more sclerotized if compared to the maxilla, especially the prementum. Both the glossa and the prementum are well-developed. The number of palpi, both the maxillary and labial, are reduced, with most species having one segment each. 3.4. Mesosoma 3.4.1. Pronoto-mesonotal complex In Hymenoptera and in most groups of Formicidae the pronotum is articulated posteriorly with the mesonotum. In Myrmicinae ants, however, the pronotum and mesonotum are externally fused
ndez, 2003) and represent an anatomical in apterous females (Ferna cluster. In some groups within the subfamily, an arched, transverse impression marks the section in which the putative areas representing the pronotum and the mesonotum might be located. Internally, the pronotal surface in apterous females of ants correspond to the site of origin of multiple muscles, such as the pronotolaterocervical, pronoto-postoccipital, pronoto-profurcal, pronotopropleural, and pronoto-procoxal muscles. Other muscles normally observed in macropterous specimens have not been observed in apterous females belonging to the subfamily, possibly as a result of loss or fusion of several axillary sclerites. The same pattern of pronotal muscle organization was observed for apterous females of Strumigenys. As in all specimens of Myrmicinae observed, the prophragma of apterous females of Strumigenys could not be observed. In fact, in other non-myrmicine ants (such as the formicine Camponotus Mayr, 1861 and the ponerine Pachycondyla Smith, 1858), a small anterior ridge can be observed on the mesonotum. However, there seems to be no muscles arising from it, suggesting the absence or reduction of the prophragma in apterous female ants. Although the reduction or absence of this structure can be intuitive when considering the loss of flight sclerites in apterous insects (since it is one of the main points of insertion of the indirect flight muscles; Snodgrass, 1993), a reduced prophragma can be observed in other species of apterous insects (Leubner et al., 2016) and may be related to the process of head movement. However, since the present study did not extensively focus on the muscular characteristics of the pronoto-mesonotal complex in Myrmicinae (and hence, in Strumigenys) and other subfamilies of ants, the skeletomuscular features of this anatomical cluster remains poorly understood. Externally, the shape and surface features of the dorsal area of the pronoto-mesonotal complex of Strumigenys (Fig. 6; pms) 21 greatly varies among species. However, all species of the genus have a distinct pronotal neck, delimited anteriorly by the pronotal rim and posteriorly by the transverse pronotal carina (Fig. 6; pn, pr and pc respectively). In some species (e.g., Strumigenys nitens Sanstchi, 1932 and Strumigenys villiersi (Perrault, 1986)), the transverse pronotal carina is absent. 3.4.2. Mesopectus In Hymenoptera, the mesopectus can be defined as the sclerite that is U-shaped in cross section, connected anteriorly to the pronotum and the propectus, dorsally with the basalare, the mesonotum and the second axillary sclerite and the subalare, posteriorly with the metapectus and bears the mesodiscrimenal lamella and the mesofurca
2014). Since this definition considers the presence of fully(Miko developed flight sclerites, much of the structures in the definition cannot be observed in apterous specimens. Hence, in apterous females, the mesopectus can be roughly defined as the anatomical cluster composed of the mesopleura and mesosternum, connected anteriorly to the pronotum and the propectus, dorsally with the mesonotum, posteriorly with the metapecto-propodeal complex and bears the mesodiscrimenal lamella and the mesofurca. However, since there is a wide range of variation in this complex in ants, especially in Myrmicinae, throughout studies of skeletomusculature of this specific complex have to be conducted, encompassing females and males, apterous and macropterous specimens, to properly define the limits of the mesopectus. The anteroventral region of the mesopectus in females of Strumigenys has a transverse notch (Fig. 6; avnmsp) that is variously developed (Fig. 7AeC). In some species, there is a setiferous patch occurring throughout the ventral margin of the structure, with the shape of the setae varying among species. Bolton (1999) considered that the lateral margin of this structure would bear a glandular apparatus, although this could not be observed in the current work. Externally, a circular minute impression was observed in several specimens, positioned laterally to the notch (Fig. 7H). However, it was not possible to determine if the circular structure was an external indicative of the pleural apophyses, or the opening connected to a glandular duct. Although most common in Strumigenys, the anteroventral notch occurs in other groups of myrmicine ants, such as Phalacromyrmex, Octostruma and Eurhopalothrix (Fig. 7DeF). 3.4.3. Metapecto-propodeal complex In Hymenoptera, the fusion of the first abdominal tergite with the third thoracic tergite is considered a diagnostic trait for the order. This anatomical complex has been studied in several hymenopteran lineages (Vilhelmsen et al., 2010; Kawada et al., 2015). It can be defined as the sclerite that is connected anteriorly with the mesopectus, dorsally with the metanotum, the metabasalare, the second axillary sclerite of the hind wing and the metasubalare and
2014). In articulates with the metacoxae and the metasoma (Miko apterous female ants, it can be roughly defined as the sclerite that is connected anteriorly with the mesopectus and dorsally with the metanotal-propodeal sulcus and articulates with the metacoxae and the metasoma. This anatomical complex varies greatly among different groups of ants, reflecting their variety of habits. This region accommodates the metapleural gland, metacoxae, and petiolar articulation. In Strumigenys, the propodeal foramen invaginates ventrally between the metacoxae, forming a medial notch (Fig. 6; vnpdfr). Some distinct pilosity can be found near the metacoxal foramina, and its shape varies from filiform to spatulate. Distinct types of processes can be found in the propodeal lobe, and some species lack any processes (e.g. Strumigenys denticulata, Strumigenys elongata, Strumigenys eggersi Emery, 1890). The same can be said regarding the 22 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 propodeal spine. Although this structure is present in most species, showing various degrees of development, it can be translucent in some species. One of the main characteristics of ants is the presence of a gland located dorso-laterally to the coxal foramen and named as metapleural gland. It is composed of a reservoir (commonly known in myrmecology as bulla) and a duct that connects the reservoir to an orifice near the propodeal foramen. In most species of ants, the orifice is easily observed and varies greatly in shape and size. In some species, the reservoir can be observed externally through a translucent patch of the metapleuron, while in others the putative location of the reservoir can be inferred based on the presence of a dilated area of the cuticle, anterior to the orifice of the metapleural gland. 3.5. Legs 3.5.1. Coxa Similar to the general coxal conformation of Formicidae, the coxa of Strumigenys is divided in a small basicoxite, separated from the larger disticoxite by a basicostal suture (Boudinot, 2015) (Fig. 6, bc, dc and bcs, respectively). In most female ants (both apterous and macropterous), the disticoxa of the fore leg is evidently enlarged if compared to the disticoxite of the other pairs of legs (such as in Myrmecia nigrocincta; Liu et al., 2019), and, according to Liu et al. (2019), it is possible that this could be considered as an apomorphic condition for the family, despite a similar condition occurring in other non-related hymenopteran families (Branstetter et al., 2017b). The disticoxite of the fore legs in Strumigenys follows the general elongated pattern occurring in ants. According to Boudinot (2015), the basicoxite is limited proximally by the coxal articulation with the mesosoma consisting of a basicoxal foramen (Fig. 6; bcf), and lateral and medial pectal fossae of the coxa, which, in turn, articulate with the lateral and medial coxal condyle of the pectus, respectively. In Strumigenys, several muscles arise from distinct regions of the pronoto-mesonotal complex, propleuron and profurca and connect directly to the procoxal rim (anteriorly, mesally and laterally), similar to the condition observed in other species (M. nigrocincta; Liu et al., 2019). The disticoxa articulates distally with the anterior and posterior trochanteral condyles through the anterior and posterior coxal fossae of the trochanter, respectively (Boudinot, 2015). The disticoxal foramen of the fore leg is directed laterally, similar to other groups of ants (Boudinot, 2015; Liu et al., 2019). Externally, the coxae of Strumigenys can be variously sculptured, ranging from areolate to totally smooth. studied (e.g., Octostruma and Pheidole). The protrochanteral base is completely enclosed by the disticoxal foramen, providing additional support to the hypothesis of the apomorphic condition of this character for Formicidae (Boudinot, 2015; char. 6). 3.5.3. Femur Trochantero-femoral joint is partly enclosed by the distal trochanteral foramen. The femur (Fig. 6; fm) in Strumigenys does not vary much apart from size and sculpture. As in all members of the family (Bolton, 2003), the trochantellus is absent. Translucent patches (Fig. 6; fmtp) are present on the dorsal area of the femur, mainly on the middle and distal section of the structure. Some species have a tibial scrobe on the ventral margin of the femur, which receives the tibia when it is pressed towards the femur. 3.5.4. Tibia Femoro-tibial joint is enclosed by the distal femoral foramen. Although its sculpture pattern appears to be mainly smooth, in some species this region is completely areolate (e.g. Strumigenys lilloana), differing significantly from the remainder of the tibia (Fig. 6; tb). Protibial spur (Fig. 6; tbs) is similar to other ant groups, forming the proximal section of the strigil. Translucent patches are present on the dorsal area of the tibia, mainly on its dorsodistal margin, varying among species, being most common on the protibia. 3.5.5. Tarsus The basitarsus (Fig. 6; btr) of Strumigenys varies considerably both in size and shape. The proximoventral margin of the probasitarsus is concave and bears a row of setae, forming the distal section of the strigil. In some species, the distodorsal margin of the basitarsus bears a translucent patch. The pretarsus (Fig. 6; ptr) of Strumigenys is simplified, if compared to other hymenopteran and formicide groups. The tarsal claws (Fig. 6; trcl) are structurally simple, varying in size, distance and curvature. The arolium is extremely reduced, which is a common condition within the family; the manubrium and the unguitractor plate are extremely reduced and the planta was not observed due to reduction, fusion or possible loss. The pretarsal anatomy is poorly studied in ants as a whole, despite their putative importance during exploration of structurally complex landscapes and their variation across different lineages in the family. Lattke et al. (2018) discussed the putative importance of pretarsal morphology (mainly size and shape of tarsal claws) during foraging in two species of Strumigenys. 3.6. Metasoma 3.5.2. Trochanter Studies on external and internal trochanteral anatomy in Hymenoptera are extremely scarce. Some studies superficially address this structure, when exploring adjacent structures (Boudinot, 2015; Johnson, 1988; Vilhelmsen et al., 2010); muscular organization and overall variation of said structure, however, are still poorly understood, especially in ants. Boudinot (2015) provided some commentaries on the trochanter for the family, whilst briefly discussing coxal variation in ants and Liu et al. (2019) briefly described and discussed trochanteral variations in M. nigrocincta. The trochanter of Strumigenys is reduced in size (Fig. 6; tc), if compared to other hymenopteran specimens observed in this study (e.g. Diapriidae, Evaniidae), but has a size similar to some formicide groups (e.g. Camponotus, Pheidole, Octostruma). The size and shape of this structure is somewhat variable in the genus and its variation deserves a more throughout exploration. However, all specimens of Strumigenys observed have the meso- and metatrochanters proximally slender and distally dilated, similarly to other ant groups The metasoma of ants is unique among other extant Hymenoptera families in having a transverse impression from the first metasomal segment (¼ petiole) to the second-third metasomal segment in female ants, varying in presence and size depending on the group. Internally, this impression does not correspond to the site of attachment of any muscular group. The metasomal acrosclerites are located laterally on their respective sclerites (Fig. 8 in red), followed posteriorly by a reduced antecostal sulcus. Posteriorly, a distinct plate follows (Fig. 8 in green) and, posterior to that, an arched impression occurs in all the sclerites (Fig. 8 in blue). Bolton (1994) refers to this impression as a girdling constriction, while Serna and Mackay (2010) refer to the same condition as cinctus. Nevertheless, Bolton (1990) mentioned that the region anterior to the impression, and posterior to the antecostal sulcus, should be referred to as presclerites and the region posterior to it should be referred to as postsclerites. However, according to Snodgrass (1993), the postsclerites (i.e. posttergites and T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 poststernites) correspond to the postcostal lip of a definitive plate that includes the intersegmental sclerotization following, with the anterior counterpart being the acrosclerites, both separated from each other by the antecostal sulcus. Since the transverse impression of the metasomal segment does not appear to be structurally equivalent to an antecostal sulcus, the pre- and postsclerites sensu Bolton (1990) are not structurally equivalent to the “pre”- and postsclerites of Snodgrass (1993). Hence, the most adequate term to refer to the region of the sclerites anterior and posterior to the transverse impression of the abdominal segment would be the antero- and postero-sclerites of the said segment. For the anterosclerites, the definition would be the area of the sclerite delimited anteriorly by the antecostal sulcus and posteriorly by the transverse impression of the abdominal segment for the antero-sclerite (Fig. 9; aat3) and the area of the sclerite delimited anteriorly by the transverse impression of the abdominal segment and posteriorly by the posterior margin of said sclerite for the postero-sclerite (Fig. 9; pt3, ps3, pt4 and ps4). 3.6.1. Areolate processes (¼spongiform tissue) Several groups of ants possess a set of intricate shaped processes located in various regions of their metasoma, such as Tetheamyrma (Bolton, 1991), Dacetinops (Brown and Wilson, 1957) and, most commonly, Strumigenys (Bolton, 2000). These processes possess an overall areolate shape that superficially resembles a sponge and, historically, have been collectively referred as spongiform tissues (or spongiform processes) (Bolton, 2000). It is not clear when the term was first proposed and if an explicit definition was provided. For the best of our knowledge, a similar term (spongy substance; p. 149 under Strumigenys lewisi Cameron, 1886) was first used by Bingham (1903), while Forel (1886; p.5) described Strumigenys fridericimuelleri Forel, 1886 as having ‘a small foaming growth’ in the ventral margin of the petiole. In both cases, neither of the authors explicitly defines the concepts adopted. Since then, subsequent publications that dealt with the description of the Strumigenys fauna used some modifications of the term - membranous appendices (Emery, 1924), spongiform processes (Smith, 1931), spongiform tissue (Brown, 1953), spongiform appendages (Brown, 1954; Kempf, 1959; Bolton, 1972) - while not providing explicit definitions for the structure. Based on an etymological analysis, the possible definition of the concept could be ‘a structure that resembles a sponge’. The concept itself could also be understood as a “structural quality (..) resembling a sponge in elasticity, absorbency, or porousness” similar to the spongy class from PATO (http://purl.obolibrary. org/obo/PATO_0001480). Since we do not explicitly know which condition (i.e. shape, elasticity or permeability) a “spongiform” structure needs to possess to attain such quality, and, so far, we do not have documented observations that objectively describe other structural qualities of this structure (i.e. we do not know if it is elastic or permeable in live specimens), we opted to use a surface feature shape class to describe and define it. Hence, we also opted to use the term areolate process, in opposition to the traditional use of spongiform tissue to refer to this concept. 3.6.2. Second abdominal segment (¼petiole) The tergosternal fusion in the second abdominal segment (Fig. 9; pt) was observed in all Myrmicinae in the present work, although this is not the case in other subfamilies of ants. The tergosternal fusion of the second abdominal segment in Strumigenys is evident, and the lateral limits of the tergite and the sternite cannot be observed. In some species of Strumigenys there is a wide range of variation in the development of the areolate processes in the ventral margin of the petiole, when they are present. Apart from that, all studied specimens present a transverse carina in the 23 anteriormost region of the ventral margin of the petiole, near the articulation with the propodeal foramen. 3.6.3. Third abdominal segment (¼postpetiole) The tergosternal fusion of the third abdominal segment is universal in the Dorylinae females and almost universal among poneroid ants (Ward, 1994; Bolton, 2003; Keller, 2011). In Myrmicinae, however, it has only been documented for Cataulacus Smith, 1853, Myrmicaria Saunders, 1842, and Cephalotes Latreille, 1802 (Bolton, 2003). We did not observe the tergosternal fusion in any of the specimens of Myrmicinae available to us. On the other hand, we observed the tergosternal fusion of the third abdominal segment in all examined specimens of female Strumigenys. The segment is fused along its length and, although the putative tergosternal limits are present, the impression defining it is often hard to see as areolate processes covers it in many species. 3.6.4. Transverse carina on the fourth abdominal tergite (¼limbus) According to Bolton (2000), the limbus is an elevated cuticular rim that prolongs transversely in the entire anterior region of the fourth abdominal tergite, near its articulation with the third abdominal tergite. According to Bolton (op. cit.), this structure would be diagnostic for the genus, and, hence, exclusive to Strumigenys. However, Baroni Urbani and De Andrade (2007) mentioned that in some species belonging to other genera (e.g. Octostruma stenognatha Brown and Kempf 1980) there is a similar structure. Similar structures are also present in species of other attine genera, namely Basiceros scambognathus (Brown, 1964), Colobostruma sp. and Ishakidris ascitaspis Bolton, 1984. In the description of B. scambognathus, Brown (1949) defined this structure as an “anterior border semicircularly excised to receive the postpetiole”. Later, Feitosa et al. (2007) described the structure similarly. Besides the abovementioned works, there are no citations to similar structures in the groups mentioned. Although differing in size and shape, the position of the structure remains constant in the studied specimens. In Strumigenys, the structure has been found in the examined specimens, presenting drastic variation in shape and size. It can be described as a transverse carina that is located posteriorly to the impression of the fourth abdominal tergite, belonging to the fourth postero-tergite (Fig. 9; cpt4). 4. Conclusions Previous studies on the morphology of Strumigenys were insufficient, in part due the great specific and morphological diversity of the genus. Also, in the past, it was difficult to exploit the minute and fragile structures or complexes of structures (such as the labio-maxillary complex). These structures can now be more easily addressed with the advent of new-generation tools. Specifically, for Strumigenys, some aspects related to skeleto-musculature of the head are currently being studied (D. Booher, pers. comm.) and collaborative efforts are being made to extensively explore the variation in the morphology of both males and females of Strumigenys J.C.M. Chaul, pers. comm. The use of ontologies to reference and to organize anatomical knowledge is extremely important to align anatomical terminology (and thus, anatomical data) with other groups of ants and families of Hymenoptera, aiming for an unambiguous referencing of morphological classes. However, one of the trade-offs for annotating anatomical classes is the need of indepth exploration of anatomical parts and their instances. Therefore, the coarser the level of anatomical study, the more difficult it is to generate a fine-tuned class annotation. The ideal scenario would be to individually explore specific body regions (such as subforaminal bridges, or the legs and associated structures) and 24 T.S.R. Silva, R.M. Feitosa / Arthropod Structure & Development 52 (2019) 100877 provide the recognition criteria and conceptualization for those parts and their instances using an ontology framework. Under these circumstances, definitions construed on a genus differentia strategy promote a basis for unambiguous referencing and could possibly enhance annotation capability in ontologies, although lacking the qualities to define epistemological recognition criteria (Vogt and Bartholomeus, 2019). Author contributions TSRS and RMF designed the study and conducted the morphological documentation. TSRS recovered anatomical classes from natural language statements, developed the anatomical class annotations, performed the scanning electron microscopy, and prepared the figure plates. TSRS and RMF wrote the first version of the manuscript. All authors revised the manuscript and read and approved the final version. Acknowledgements ^nica The authors are deeply indebted to Ricardo Kawada, Mo
a, John Lattke and Cla
udio Carvalho for providing important Ulysse observations in previous versions of this work. We are equally indebted to three anonymous reviewers who pointed out several issues throughout the text, while providing insights on the discussion of data accessibility and methodological consistency. We
n Miko
for patiently would like to thank Matthew Yoder and Istva explaining important aspects of the Hymenoptera Anatomy Ontology and for providing access to HAO through mx. We are also indebted to Brian Fisher and all the Antweb team for providing open-access high-quality images of several Strumigenys species. Also, Alexandre Casadei Ferreira, Mila Martins, Weslly Franco, Natalia Ladino, Aline Oliveira, Gabriela Camacho, Júlio Chaul, Douglas Booher and Brendon Boudinot provided important knowledge on ant morphology as a whole, greatly improving the discussion of this work. The results presented were supported by ~o de Aperfeiçoamento de the grant 40001016005P5 (Coordenaça Pessoal do Nível Superior - CAPES) to TSRS and the grant 02462/ 2016-3 (Brazilian Council of Research and Scientific Development CNPq) and project 3-188 from the Partnerships for Enhanced Engagement in Research (PEER) Science Program (NAS/USAID) to RMF. This work was supported in part by Finance Code 001 (CAPES). 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