Abstract Representation of women in science drops substantially at each career stage, from early student to senior investigator. Disparities in opportunities for women to contribute to research metrics, such as distinguished speaker events and authorship, have been reported in many fields in the U.S.A. and Europe. However, whether female representation in scientific contributions differs in other regions, such as Latin America, is not well understood. In this study, in order to determine whether female authorship is influenced by gender or institutional location of the last (senior) author or by subfield within ecology, we gathered author information from 6849 articles in ten ecological and zoological journals that publish research articles either in or out of Latin America. We found that female authorship has risen marginally since 2002 (27 to 31%), and varies among Latin American countries, but not between Latin America and other regions. Last author gender predicted female co-authorship across all journals and regions, as research groups led by women published with over 60% female co-authors whereas those led by men published with less than 20% female co-authors. Our findings suggest that implicit biases and stereotype threats that women face in male-led laboratories could be sources of female withdrawal and leaky pipelines in ecology and zoology. Accordingly, we encourage every PI to self-evaluate their lifetime percentage of female co-authors. Female role models and cultural shifts–especially by male senior authors–are crucial for female retention and unbiased participation in science.

Citation: Salerno PE, Páez-Vacas M, Guayasamin JM, Stynoski JL (2019) Male principal investigators (almost) don’t publish with women in ecology and zoology. PLoS ONE 14(6): e0218598. https://doi.org/10.1371/journal.pone.0218598 Editor: Pablo Dorta-González, Universidad de las Palmas de Gran Canaria, SPAIN Received: August 7, 2018; Accepted: June 5, 2019; Published: June 19, 2019 Copyright: © 2019 Salerno et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability: All relevant data are within the Supporting Information files. Funding: JLS received a postdoctoral fellowship from the American Association for University Women (aauw.org) which contributed to the completion of this work. MPV received assistance with publication costs from the Universidad Tecnológica Indoamérica. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist.

Introduction It is well documented that women are underrepresented in science fields, particularly at senior levels [1, 2], and in spite of recent reduction of pay gaps and other advances in gender equity [3–5]. Many studies have investigated how biases generate the phenomenon known as the “leaky pipeline” [3], whereby minorities including women are more likely to be diverted out through the joints between pipes, dropping in representation at every stage in the career pipeline [1, 2]. Female retention is a problem in all STEM (Science, Technology, Engineering and Mathematics) fields, including the biological sciences, where females are overrepresented at the undergraduate level, but withdraw at shockingly high rates at higher career levels [6–9]. Gender underrepresentation is an important issue not only because of social equity and justice [2] but also scientific advancement [10, 11]. However, we still have little understanding of the reasons why women so frequently withdraw from STEM fields and publish less than their male colleagues [4, 12]. In order to properly address female retention in STEM fields and enforce commitments to diversity and inclusion, a closer examination is needed [9]. Disparities in representation and leaky pipelines can be driven by both internal and external sources of bias [1, 2, 13–15]. Stereotype threats, in which individuals doubt their own ability to perform well in a field due to social information, are important internal drivers [16–19]. Unconscious biases against minorities and women are important external drivers. For example, male and female undergraduates consistently rate female peers and instructors lower in academic performance and teaching ability [20, 21]. Also, male and female professors are biased against female students; when hiring future laboratory staff, they ranked application documents with the name “John” about 25% higher than identical documents with the name “Jennifer” [15]. Moreover, female academics are more likely to have their work attributed to a male colleague [22], less likely to have their work cited when in dominant authorship positions [12], and more likely to encounter harassment and discrimination at different stages of their careers [23–25]. Underrepresentation of women is less pronounced in biology than in other STEM fields [5, 26–28], but the leaky pipeline remains an important concern in STEM fields that are female-dominated at the graduate student level [2, 7]. For example, in ecology, a female-dominated field [7], bias against females has been found at the levels of ecological textbooks [6], distinguished speaker invitations [7], and authorship contributions [27]. Authorship order is meaningful in the life sciences, particularly in collaboration-intensive and expensive fields like ecology [8, 29–31]. Despite some regional variation in norms of authorship designation [32–34], the last author usually connotes the head of the lab, the first author connotes the researcher that conducted most of the writing or experiments, and “middle” authors vary in their degree of contribution [8, 30, 33, 35]. Thus, name order influences the credit assigned to researchers, and can point out power imbalances [5, 30, 32]. Gender parity in science becomes even more complex when taking into account cultural and socio-economic differences at the global scale. Previous research has found country and regional indicators of development and gender equality to be poor predictors of female participation in science [36]. Because most studies of academic gender disparity have been conducted in North America and Europe, extrapolation to Latin American ecologists is not straightforward. One might predict gender disparity to be higher in Latin America, as women are relatively less represented in high profile positions such as public office [37, 38]. For example, in Brazil, funding awards and senior-level academic positions in the life sciences are strongly imbalanced against women [39]. Furthermore, because female authorship is higher in countries and regions with lower scientific output [12], career prestige and female representation may be negatively correlated [40]. However, one recent study found the proportion of female authors to be slightly higher among Latin American ecologists as compared to other regions [34]. In this study, we aimed to evaluate gender disparity in the fields of ecology and zoology and to understand variation in gender representation both among subfields and regionally within and outside Latin America. We gathered authorship information from ten peer-reviewed journals in 2002–2016, sampling them in a paired design such that each subfield was represented by journals that focus on publishing research either within or outside Latin America (e.g. Ecology and Biotropica). Based on recent publications, we predicted that women would be underrepresented as authors regardless of region, and that representation would increase over time. We also predicted lower female representation in Latin America. Finally, we predicted that the proportion of female authors would vary by country within Latin America and by gender of last author, but would remain similar across subfields.

Methods We obtained information about the authors of articles from ten journals (Table 1), two in general ecology: (1) Biotropica (ISSN 0006-3606) and (2) Ecology (ISSN 0012-9658); and eight in taxon-specific journals within three zoological subfields, mammalogy: (3) Acta Zoológica Mexicana (ISSN 0065-1737) and (4) Journal of Mammalogy (ISSN 0022-2372), ornithology: (5) Ornitología Neotropical (ISSN 1075–4377) and (6) The Auk (0004–8038), and herpetology: (7) Herpetologica (ISSN 0018–0831); (8) Journal of Herpetology (ISSN 0022-1511); (9) Phyllomedusa (ISSN 1519–1397); (10) South American Journal of Herpetology (ISSN 1808–9798). We selected journals such that each subfield was represented by at least one journal focused on research in Latin America and one focused on research outside of Latin America (or without a regional focus; Table 1). PPT PowerPoint slide

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larger image TIFF original image Download: Table 1. Journals sampled in this study, ordered by impact factor. Table includes information about the field of study, the country of the publisher, the society and publisher of the journal, its impact factor, genders of the chief editorial board (M = male, F = female), and the proportion of female associate editors. https://doi.org/10.1371/journal.pone.0218598.t001 We collected author data directly from the title page of 6849 articles published in 2002–2016. Journals varied in the number of volumes and articles printed annually, so we reduced uneven representation by sampling 60 articles among the volumes in a given year in a given journal. For example, in a journal with 6 volumes per year, we used data from the first 10 articles in each of the 6 volumes. In cases in which less than 60 articles were printed in a given year, we included all articles from that year. For each article, we recorded: (1) year; (2) title; (3) number of authors; (4) proportion of female authors; (5) gender of first author; (6) gender of last author; (7) proportion of authors with a Latin American institutional affiliation; and (8) location of last author’s institutional affiliation (outside Latin America or the country in Latin America). We emphasized affiliation of authors rather than ethnic origin to maximize sampling of information available within articles. We excluded articles in which an author's gender was not obvious based on the first name itself or after searching for an academic website with a photo of the author. Because generalized linear models (GLMs) with binomial error distribution (appropriate for proportion data) were overdispersed, we analyzed data with GLMs using quasibinomial error distribution. To understand author demographics, we determined whether the proportion of female authors, first author gender, last author gender, or proportion of authors based in Latin America as response variables were explained by journal or year as predictor variables. Then, we tested if the gender of the last author, who is generally the head of the research group [8, 30, 33, 35], influenced the proportion of female authors or the gender of the first author, and whether any such effect differed among biological subfields. We also tested whether institutional affiliation of the last author in or out of Latin America influenced the proportion of female authors or the gender of the first or last author. We tested whether last author gender, first author gender, institutional affiliation, or their interaction influenced the number of co-authors. And, we visualized the proportion of female authors by Latin American country. We repeated analyses of the effect of last author gender and institutional affiliation after excluding articles by a single author. We also repeated analyses allowing relationships to vary with journal as a random variable in generalized linear mixed models. Analyses were conducted in R (version 3.5.1 [41]; data and analyses available in S1 Table and S1 Script).

Acknowledgments We would like to thank Diana Dominguez, Bibiana Rojas, Karen Warkentin, Kim Hoke, Ximena Bernal, and Jenni Cross for fruitful conversations that improved the study, as well as the participants of the “Women in Latin American herpetology: challenges and achievements” at the XI Latin American Congress of Herpetology in Quito, Ecuador in 2017. The authors received no explicit funding for this project, and declare no conflict of interest.