Taxonomic bias in animal behaviour publications

Animal Behaviour 127 (2017) 83e89

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Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav

Taxonomic bias in animal behaviour publications Malcolm F. Rosenthal a, *, Matthew Gertler b, Angela D. Hamilton b, Sonal Prasad a, Maydianne C. B. Andrade a a b

Department of Biological Sciences & Ecology and Evolutionary Biology, University of Toronto Scarborough, ON, Canada University of Toronto Scarborough Library, Scarborough, ON, Canada

a r t i c l e i n f o Article history: Received 19 October 2016 Initial acceptance 2 January 2017 Final acceptance 2 February 2017 MS. number: A16-00919R Keywords: behavioural ecology citation bias ‘model’ taxa publication skew taxonomic prejudice

Evidence suggests that certain taxonomic groups are more thoroughly studied than others across a wide range of biological disciplines. Such taxonomic biases have the potential to define our understanding of theory, and limit the generality of our insights. To assess the distribution of taxonomic representation in current and historical animal behaviour research, we constructed a data set containing article metrics and taxonomic information for all research articles published in the journal Animal Behaviour between 1953 and 2015. We found significant taxonomic bias, with chordate papers making up 70% of all publications in the past 15 years, despite accounting for less than 7% of all animal species. Within chordates, Animal Behaviour content is biased towards endotherms, with birds and mammals comprising more than 50% of all publications. In sum, six animal orders account for more than half of all publications, with the most commonly published order, Passeriformes, representing one in five articles. Our findings confirm that a relatively narrow group of ‘model’ taxa represent the vast majority of articles, and may have a disproportionate influence on our understanding of behavioural patterns and processes. Furthermore, we find evidence of a citation bias, with chordate studies receiving on average four citations more per paper than arthropod studies. While historical trends suggest that the publication gap between arthropods and chordates has been shrinking for the past 45 years, our findings show that a considerable bias still remains. These biases may originate from human preferences for certain animal types, but we argue that they are likely maintained by a mixture of taxonomic prejudices, cultural aspects of behavioural ecology as a field, and of academia in general. We suggest that the patterns are clear and their implications serious, and that it is time that both researchers and journals give serious consideration to addressing them. © 2017 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

The field of animal behaviour strives to address broad, integrative hypotheses about the evolutionary and ecological processes underlying patterns of behaviour by inferring general principles from empirical studies. The broadest goals of this research require a taxonomically diverse foundation of work, as we strive to discern the features of the particular system under study and distinguish these from patterns that are general features of how a particular process works. Understanding the dynamics of behaviour in one taxonomic group is an important goal, but the entire field moves forward only when a series of such studies across a variety of taxa allows leaps in global understanding. For example, testing established theory across new taxonomic groups can lead to the discovery that paradigms established in popular model taxa do not

* Correspondence and present address: M. F. Rosenthal, Department of Environmental Science, Policy, and Management, University of California, Berkeley, 137 Mulford Hall, Berkeley, CA 94720, U.S.A. E-mail address: [email protected] (M. F. Rosenthal).

hold generally (e.g. Zuk, Garcia-Gonzalez, Herberstein, & Simmons, 2014). If we restrict the bulk of our research effort to a subset of taxa, we risk drawing conclusions that are invalid at broader scales by assuming that the predominant behaviours in that subset of taxa are universal. Simply put, if we have a skewed representation of taxa in our research, then we have a skewed understanding of the world. Furthermore, a broad taxonomic basis can increase the value of animal behaviour research outside of our field, as demonstrated by direct applications to problems in conservation, captive breeding and reintroduction programmes, assessment of risks from zoonotic diseases or animal disease vectors (e.g. Caro, 1999; Guidobaldi, May-Conchua, & Guerenstein, 2014; Vinauger & Lazzari, 2015), and the importance of behavioural mechanisms for understanding Allee affects (Stephens & Sutherland, 1999; Stephens, Sutherland, & Freckleton, 1999). Nevertheless, it is highly likely that animal behaviour research is taxonomically skewed. There is widespread evidence that ecology and evolution research is biased towards endotherms (Bonnet,

http://dx.doi.org/10.1016/j.anbehav.2017.02.017 0003-3472/© 2017 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved.

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Shine, & Lourdais, 2002), that conservation work is biased towards vertebrates, and birds and mammals in particular (Clark & May, 2002; Seddon, Soorae, & Launay, 2005), and that animal research in general is biased towards the species we find inherently attractive or appealing (Estren, 2012; Fleming & Bateman, 2016). These biases not only threaten the utility of meta-analysis, surveys of the literature and any approach used to synthesize general insights and concepts from multiple studies, they may weaken our progress in uncovering broad theoretical insights. The potential magnitude of these biases and their root causes have mostly been ignored. Taxonomic biases in research are not frequently discussed in journals or the academic societies that support them (with few exceptions, e.g. Bonnet et al., 2002; Clark & May, 2002; Leather, 2009; Seddon et al., 2005), and the same is true for Animal Behaviour. This may be partly because no study has examined the magnitude of taxonomic skew in published animal behaviour research, thus relegating discussions to speculation based on anecdotal impressions. Most research on taxonomic skew has focused on conservation studies (e.g. Clark & May, 2002; Seddon et al., 2005), and studies that include animal behaviour generally restrict their analyses to a subset of taxa (e.g. Bonnet et al., 2002) or a subset of research questions (e.g. Stahlschmidt, 2011). Here, we provide a clear quantification of skew in the behaviour literature by directly examining, in depth, patterns of taxonomic representation in published research papers. It is our assumption that the taxonomic distribution of published papers reflects the priorities and emphases of research in the field of animal behaviour. In the absence of any bias in studied taxa, the publication record should reflect the diversity of life; we consider this an a priori expectation about taxonomic representation. However, the publication record almost certainly does not conform to these expectations, as is made clear by previous studies on taxonomic bias in ecology and evolution research. While we will almost certainly reject the null hypothesis that the representation of taxa in published studies is in direct proportion to the relative number of species in that taxon, it is the degree to which the publication record deviates from that expectation that will be of the most interest. Here, we focus on publications from a single journal, Animal Behaviour, as a representative for the field of behavioural research, although the methods we outline here can be used to generate similar data sets with other journals. Animal Behaviour is the oldest of the top three behaviour journals (Animal Behaviour, Behavioral Ecology, and Behavioral Ecology and Sociobiology), having begun publication in 1953. Its articles are broadly representative of the field. Most behavioural researchers publish at least a portion of their papers in Animal Behaviour, and while there are differences in research emphases among the top behaviour journals, the general €rner, content overlap is strong (Ord, Martins, Thakur, Mane, & Bo 2005). Since Animal Behaviour is not a taxon-specific journal, our a priori supposition that the number of papers for a given taxon should be proportional to its number of species is a useful null hypothesis. We chose Animal Behaviour because we expect its publications to reflect the broad state of research in the field. We do not expect our findings to be driven by publication biases or problems specific to Animal Behaviour, and we intend our findings to shed light on the nature and extent of the taxonomic skew in the field more broadly. Additionally, we demonstrate a procedure for generating large data sets with the potential to address multiple questions, including questions about historical trends in taxonomic focus, authorship patterns and citation rates. It is our hope that our examination of a single journal will engender frank discussion about the nature and magnitude of taxonomic bias and potential solutions.

METHODS Data Set Generation We generated a comprehensive data set containing taxonomic, authorship and citation information for papers published in the journal Animal Behaviour. We downloaded citation and use data from the abstract and citation database Scopus in 24 separate files for all articles published from 1953 to 2015. Using R (v.3.2.1, R Foundation for Statistical Computing, Vienna, Austria) and the packages ‘plyr’ (Wickham, 2011), ‘stringr’ (Wickham, 2015) and splitstackshape (Mahto, 2014), we compiled the files into a single data table, removed extraneous columns, split author names into unique columns and generated a column of species names from the available data. Each publication in the data set is represented by one row for each species studied in the publication. Publications with multiple species have multiple rows in the data set, with all information being identical between rows save for the species names. We removed all publications from the data set that did not contain new observational or experimental data on at least one animal species (i.e. review, commentary and meta-analytical papers), and all rows representing nonanimal study organisms (e.g. symbiotic bacteria, host plants, etc.). We labelled all remaining publications with a unique identification number, which is shared for all rows from the same publication. Species names for all publications (including those with species information from Scopus) were manually confirmed, and missing species names were filled in using information from the title, abstract or body text of affected publications. We checked species names for spelling errors and synonymized all names to their current accepted forms using the R package ‘taxize’ (Chamberlain & Szocs, 2013). We also used ‘taxize’ to fill in family, order, class and phylum data for all rows of the data set. To gain perspective on whether taxonomic distributions vary across research subjects, we assigned publications from the most recent 15 years of the data set (2000e2015; N ¼ 4076 papers) to any of five nonmutually exclusive research categories: predation/ foraging, mating, parental care, sociality and communication. While these categories do not exhaustively cover all possible areas of animal behaviour research, they were chosen to allow us to broadly examine the possibility of nonuniform sorting of taxa by research subjects. These categories, or variations on these, have been consistently represented in the organization of talks and poster sessions at annual meetings of the Animal Behavior Society over the past 10 years. Although more specific subjects are often named, these can generally be categorized under one or the other of these areas of study. As such, we feel these categories represent some of the broadest and most common areas of research, a contention supported by the fact that 79% of papers in our data set sort into one or more of these categories. Additionally, one explanation for observed bias in publications is that not all behaviours are universal, and some questions may only be relevant in a subset of taxa. For example, parental care is only studied in species that exhibit parental care, and will therefore be biased towards those species. To address that, we chose three categories that likely represent universal behaviours (mating, predation/foraging, communication) and two categories that likely represent behaviours that appear only in certain taxa (sociality, parental care). If relevance to a given taxon drives taxonomic skew, then it might be expected that bias will be most pronounced in the latter two categories. Papers were categorized by one of us (M.F.R.) based on titles, and when these were ambiguous, abstracts. Prior to assigning categories in our full data set, a subset of papers (N ¼ 200) were

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Data Analysis To assess the taxonomic distribution of current research, we restricted our analysis to the most recent 15 years of the data set (2000e2015; N ¼ 4076 papers). We used chi-square analyses to compare the observed numbers of publications on taxa at two levels, phylum and class, to expected frequencies generated from the recorded number of species in each taxon in the Catalogue of Life (Roskov et al., 2016), an online project that provides a comprehensive and continuously updated taxonomic database. At lower taxonomic levels, a deviation from expected frequencies is unavoidable, given the large ratio of animal taxa to animal behaviour researchers. We therefore present the most intensively studied animal orders for qualitative assessment without accompanying statistics. For all analyses and figures, publications with multiple study species within a taxonomic level were counted only once for any given taxon, but were counted once for each if they included study species from more than one taxon. Less than 2% of papers include data from more than one animal order, and the percentages are even lower at higher taxonomic levels. We therefore consider the effect to be minimal and our approach justifiable in order to simplify analysis. We assessed the possibility of a citation bias between publications on Chordata and Arthropoda (the two most-studied phyla) using a t test on log-transformed citations per paper for chordate and arthropod papers published between 2000 and 2012 (N ¼ 3264). We excluded the most recent 3 years of the data set because there was a significant lag between publication time and time of first citation, and citations for papers in the most recent years of the data set were not likely to be reflective of their true impact. Supporting this, 85% of papers with zero citations (238 of 281 total papers) occurred in the most recent 3 years of the data set. To determine whether taxonomic distributions in published papers differed across research categories, we focused on the three most common classes (Insecta, Mammalia, Aves) and asked whether the degree of skew in publication varied across subject areas. Together, these three classes accounted for 75% of all publications, and included roughly similar numbers of orders (20e30). We examined how publications in each subject category were distributed across these classes relative to a null expectation that the class-specific proportion of studies in each subject area should match the proportion of studies on that class in our entire sample. All analyses were run with publication numbers for these three classes, as well as a catch-all group that included every other class of life (‘all others’). Given that research categories differed significantly from one another in taxonomic distribution (c2 ¼ 451.86, P < 0.0001) we ran five separate chi-square tests comparing the observed taxonomic distributions in each category to an expected distribution from the numbers of taxa across our entire data set. To correct for multiple comparisons, we took the conservative approach of using a Bonferroni-corrected alpha of 0.01 for those tests. Finally, we visualized historical trends in taxonomic bias and diversity in two ways. First, we plotted the ratio of arthropod to chordate papers for all years from 1953 to 2015 (N ¼ 9953 publications). Second, we plotted the number of animal families studied per year for all years from 1953 to 2015 (N ¼ 10 563 publications). We tested for changes in these numbers with linear regressions on data from 1970 onwards, as the number of papers published per year prior to 1970 was very low (<50 papers per year average).

RESULTS Taxonomic Distribution Two phyla, Chordata and Arthropoda, accounted for 98% of all publications, with chordates representing 71% of publications, and arthropods representing 27% (Fig. 1, Supplementary Table S1). This distribution was significantly different from the expected distribution (c2 ¼ 30 209, P < 0.0001), as chordates comprise 7% of described species, and arthropods comprise 84% of described species. Species from 29 animal classes were represented in research from the past 15 years, but four classes (Aves, Mammalia, Actinopterygii, Insecta) accounted for 84.75% of all publications (Fig. 2, Supplementary Table S2). This distribution was also significantly different from expectations (c2 ¼ 87 562, P < 0.0001). Endothermic vertebrates were the most overstudied, comprising more than half of all publications (with birds and mammals representing 28% and 26% of publications, respectively) but less than 1.5% of all species. Insects were the most understudied, representing nearly 73% of animal species, but only 20% of publications. Species from 135 animal orders were represented in the data set. However, the six most studied orders accounted for more than 50% of publications (Fig. 3, Supplementary Table S3), with the most commonly studied order being Passeriformes at nearly 20% of all articles. Five of the top six orders were endothermic vertebrates. The sixth, Hymenoptera, was also the only invertebrate order in this group, representing 9% of publications. Citation Bias On average, chordate publications received four more citations per article than arthropod publications (Chordata ¼ 24.26, Arthropoda ¼ 19.86; t ¼ -6.107, P < 0.0001). Research Categories Taxonomic representation varied significantly by research category (Fig. 4, Supplementary Table S4), and four of the five categories differed significantly from the patterns of representation in the whole data set (mating: c2 ¼ 128.23, P < 0.0001; parental care: c2 ¼ 53.37, P < 0.0001; communication: c2 ¼ 62.73, P < 0.0001; social behaviour: c2 ¼ 199.81, P < 0.0001; predation and foraging: c2 ¼ 8.62, P ¼ 0.035). In particular, Aves were over-represented relative to the whole data set in studies on communication and parental care, and under-represented in studies on sociality. Mammalia were over-represented relative to the whole data set in studies on sociality, but under-represented in studies on mating. Insecta

No. of papers

independently scored by two of us (M.F.R. and M.C.B.A.), and our assessments were compared. Any discordance in categories were discussed, and rules for category assignment were then established and applied to the 15-year data set.

85

3500

Observed

3000

Expected

2500 2000 1500 1000 500 0

Chordata

Arthropoda

All others

Figure 1. The observed and expected numbers of papers that focused on the two most common animal phyla in publications from the journal Animal Behaviour from 2000 to 2015. Expected values were generated from species numbers published in the Catalogue of Life (www.catalogueoflife.org/annual-checklist/2016).

No. of papers

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3500

Observed

3000

Expected

2500 2000

DISCUSSION

1500 1000 500 0

Aves

Mammalia Insecta Actinopterygii All others

Figure 2. The observed and expected numbers of papers that focused on the four most common animal orders in publications from the journal Animal Behaviour from 2000 to 2015. Expected numbers were generated from species numbers published in the Catalogue of Life (www.catalogueoflife.org/annual-checklist/2016).

25

% Publications

20 15 10 5 0

Cetartiodactyla Carnivora Rodentia

Primates Hymenoptera Passeriformes

Figure 3. Percentage of all publications in the journal Animal Behaviour from 2000 to 2015 that focused on the six most-published animal orders.

60 50 % Publications

(F2,44 ¼ 52.27, P < 0.0001; Fig. 5). Likewise, the number of families studied per year has been steadily increasing since 1970 (F2,44 ¼ 277.3, P < 0.0001; Fig. 6).

40 30 20 10 0

* Mating

*

*

*

Parental care Communication Social behaviour Foraging and predation

Figure 4. Taxonomic representation of papers published in the journal Animal Behaviour (2000e2015) for the top three most-published classes across five research categories, represented as the percentage of papers in each class per category. The solid line represents class Aves, the dashed line represents class Mammalia, and the dotted line represents class Insecta. Horizontal lines show the percentage of papers in each class in the overall data set. Asterisks indicate categories with distributions that differed significantly from the overall data set.

were under-represented relative to the whole data set in studies on parental care and communication, but were otherwise close to expected values. Notably, while patterns of representation in most categories differed significantly from the patterns of representation in the whole data set, the skew towards endothermic vertebrates and against arthropods was still strongly evident in all categories. Historical Trends The ratio of arthropod to chordate papers has fluctuated since 1953, however it has been steadily increasing since 1970

We found significant skew in Animal Behaviour publications relative to neutral expectations based on biodiversity. Publications exhibited a strong taxonomic bias against Arthropoda, although it is by far the most speciose phylum. Chordata, on the other hand, was highly over-represented. Birds and mammals, the endothermic vertebrates, were the most over-studied, comprising more than half of all publications despite accounting for less than 1.5% of all animal species. While still over-represented relative to arthropods, ectothermic vertebrates were highly under-represented relative to endothermic vertebrates. Ray-finned fish represented only 10% of publications despite having more than twice the number of species of birds and mammals combined. Likewise, reptiles and amphibians represented a combined 7% of all publications, although both have many more species than do mammals, and reptiles have a similar number of species as do birds. At lower taxonomic levels, the intensity of the bias was even more apparent. Perching birds (Passeriformes) accounted for one in five publications (Supplementary Table S3). Hymenoptera and Primates both represented around 9% of publications, although there are more than 200 times more hymenopteran species than primate species (Supplementary Table S3). Other taxonomic groups were conspicuous by their absence. Coleoptera, by far the largest animal order, representing as many as a quarter of all species, was barely present, with only 77 publications in the past 15 years. Moreover, these publications concerned only 40 of the ~240 000 species of beetles. In comparison, in the same time frame, there were 370 publications on 76 different species of primates, a group with less than 500 species in total (Supplementary Table S3). Taxonomic representation also differed significantly across the surveyed research categories, however, the endothermic vertebrates were still strongly over-represented in all research categories. Differences between categories are likely due to the fact that certain behaviours are more prevalent in some groups than in others. However, the arrow of causation can point either way; our assumptions concerning the prevalence of various behaviours across taxa were based in part on our surveys of those taxa, which, as we show here, were themselves skewed. Critically, representation was also skewed in categories that are likely to be more universal, such as communication, mating, and predation and foraging, with birds and mammals over-represented in all three categories. Furthermore, several less well-studied taxonomic groups exhibited a strong research category skew. For example, 68% of amphibian publications (78 of 115) scored in the mating category, the communication category, or both, suggesting that research effort in some understudied systems may mainly address a narrow set of questions; in this case, frog chorus calls. Taken altogether, it is clear that, as a research community, we have failed to act in an unbiased manner when working to uncover the broad patterns and processes that underlie animal behaviour. It is also clear, from our historical examination, that these patterns of taxonomic bias are not new. Rather, they have been in place since the origin of modern animal behaviour research. Encouragingly, we find evidence of an increasing taxonomic breadth of study, as well as evidence that the strength of our prominent bias against arthropod studies has been lessening over the past 45 years. However, while such trends are promising, they are vastly outweighed by the magnitude of the bias that still exists. We now turn to a discussion of the factors that may underlie these biases and a

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1

Arthropoda/Chordata

0.8

0.6

0.4

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1953 1955 1957 1959 1961 1963 1965 1967 1969 1971 1973 1975 1977 1979 1981 1983 1985 1987 1989 1991 1993 1995 1997 1999 2001 2003 2005 2007 2009 2011 2013 2015

0.2

Figure 5. The ratio of arthropod to chordate papers published per year for all publications in the journal Animal Behaviour between 1953 and 2015. The regression line represents a fit based on data from 1970 to 2015 only.

70

No. of families

60 50 40 30 20

0

1953 1955 1957 1959 1961 1963 1965 1967 1969 1971 1973 1975 1977 1979 1981 1983 1985 1987 1989 1991 1993 1995 1997 1999 2001 2003 2005 2007 2009 2011 2013 2015

10

Figure 6. The total number of families on which papers were published per year in the journal Animal Behaviour for all years between 1953 and 2015. The regression line represents a fit based on data from 1970 to 2015 only.

consideration of the types of changes in culture could rebalance these biases in the long-term. Why Does This Bias Exist? Scientists generally choose study systems based on their relevance to a given set of questions, their tractability, and some degree of personal preference and interest. Ultimately, variation across taxa in any of these factors may be responsible for the biases we have described, and understanding the relative importance of these factors is key to determining a solution. One possibility is that bias results from the fact that some research questions are relevant only to a subset of taxa. For example, some behaviours (e.g. eusociality, brood parasitism, parental care, tool use, etc.) are exhibited only in some taxa, and are therefore only studied in those taxa. This factor likely does affect taxonomic patterns of representation. However, the fact that we find bias even in studies on universal behaviours such as predation and foraging, communication and mating suggests that this factor alone does not drive the bias. Another possibility is that some taxonomic groups are simply easier to study than others, or are more ideal for answering certain

types of research questions (i.e. Krogh's Principle; Krogh, 1929). Over time, we may have focused our efforts on the subset of species in which our questions can be most efficiently addressed. This may be particularly true for researchers seeking understanding of human behaviour using animal models. This argument is appealing, and makes intuitive sense, yet there is scant direct evidence to suggest that it is true. In fact, while arthropods are underrepresented in publications, some evidence suggests that arthropod research actually requires less effort per study than vertebrate research (Pawar, 2003). Moreover, studies aimed at understanding human behaviour are only a subset of the many fields of study published in Animal Behaviour, with ‘behavioural psychology’ only one of nine different research areas covered by the journal (https://www.journals.elsevier.com/animal-behaviour/, Animal Behaviour Aims & Scope) On the whole, there is no evidence to support or deny the claim that these biases have arisen as a result of differences in tractability or inherent relevance to broad behavioural topics. We suggest that, ultimately, taxonomic biases in research are likely to stem from the innate biases of humans. There are considerable relevant data on human preferences and aversions

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with respect to animals, and these map closely onto the biases we show here. We exhibit preferences for larger (Ward, Mosberger, Kistler, & Fischer, 1998) neotenous animals (Borgi & Cirulli, 2016; Estren, 2012), the notorious ‘charismatic megafauna’ preference. We also prefer animals that are more closely related to us (Batt, 2009) while reacting with fear towards distantly related taxa (Kubiatko, 2012), and these responses appear to exist from early childhood (Borgi & Cirulli, 2015). Long-standing cultural preferences for vertebrates and endotherms are already known to affect patterns of conservation funding and research, with public interest being focused on, again, a ‘charismatic’ subset of endangered species (Czech, Krausman, & Borkhataria, 1998; Knight, 2008). Given that many study systems are chosen based on the passions or interests of researchers, it seems likely that such biases are one reason why most of the most heavily studied taxa are birds and mammals. Yet while such preferences may explain the origin of taxonomic bias, of equal concern is the possibility that there are proximate factors working to maintain the skew in current research. Specifically, researchers who focus on less popular systems may be at a disadvantage when attempting to publish their work. Bonnet et al. (2002) argued that narrowly written papers on popular systems may appear more broadly appealing to editors or reviewers than similar (or even broader) papers written on nonmodel systems. In support of this, they found that publications on less popular study systems such as fish, reptiles and amphibians have more broadly framed introductions than papers on birds or mammals. This could be the result of innate preferences for some taxa leading to gentler critiques of the relevance of the work in some cases, or harsher in others. If present, such biases are likely unintentional, and reviewers may not be aware of any differential treatment of subject matter (e.g. Devine, 1989; Dovidio, Kawakami, Johnson, Johnson, & Howard, 1997). While we consider this an important possibility to assess, our study does not address it, and further research is required to test this hypothesis. Patterns of citation differ as well. Bird and mammal publications are significantly more likely to cite within their own taxa than are publications on invertebrates or ectothermic vertebrates (Taborsky, 2009). Given the high ratio of vertebrate to invertebrate publications, this kind of taxonomic parochialism should lead to taxonomic biases in citation rates, a possibility which we confirm in our findings here, as arthropod publications were cited significantly less frequently than chordate publications. Even in small degrees, these factors may present career handicaps to researchers who focus on less popular systems, especially in a field that so strongly emphasizes the publication count and the H-index as metrics of success (Kelly & Jennions, 2006), and where publication in a highimpact journal requires reviewers and editors accept arguments about generality of interest. Lastly, beginning to work in a new study system presents barriers that may be difficult to overcome for younger researchers. While building a research programme around an understudied taxon may pay eventual dividends, the necessary first steps involve broad, observational work, mainly on natural history and life history. This type of basic science is strongly discouraged by the publish-or-perish, citation-focused model of academic assessment, as such studies end up in mid- to low-profile, or taxon-specific journals, which are less valuable on a CV or job application due to their narrower readership, lower impact factors and reduced prestige. Likewise, our grant-giving process favours research projects that are most likely to be productive in the short term, which may further incentivize conservative studies likely to produce results, but less likely to innovate. For example, a recent study of 74 years of published literature in biomedicine and chemistry (Foster, Rzhetsky, & Evans, 2015) found that the percentage of conservative

research projects are increasing. For this and other reasons, openended exploratory research of the kind necessary to expand our taxonomic breadth is not appealing to many career-focused researchers. Yet natural history, observational studies and tests of generality represent the foundation on which we build our more theoretical and hypothesis-driven research. To ignore one is to slowly starve the other. Concerns that we are abandoning a critical area of research are not new; in fact, they date back to the earliest days of the modern field. As early as 1963, Niko Tinbergen was warning that the interest in experimental and hypothesis-driven research had begun to erode work on purely descriptive projects, reminding us that ‘we would deceive ourselves if we assumed that there is no longer a need for descriptive work’ and that ‘contempt for simple observation is a lethal trait in any science, and certainly in a science as young as ours’ (Tinbergen, 1963, p. 412). On the whole, we argue that the taxonomic biases we describe here are just one quantifiable result of a larger structural problem with the state of our field which, as with many other fields (Foster et al., 2015), rewards risk-averse, conservative decision making with respect to study focus, especially by younger scientists. How to Solve the Problem? We strongly believe that understanding how our behaviour as researchers fits into this pattern is critical to understanding both the extent of the problem and its solution. Our findings shed light only on the magnitude of the bias. More discussion and research is needed, and it is our hope that this study will generate interest in doing just that. In some cases, discussion of the subject itself has the potential to provide a benefit. As researchers, reviewers and editors, we have the capacity to critically assess our actions, and to assess our own tendency towards parochialism when citing papers and bias towards model systems when peer reviewing. We can work harder to consider how our question is addressed in other taxa, and to be aware of the ways in which the taxon of study affects our opinion of a manuscript's novelty or breadth of interest. In short, we can begin to ask ourselves how our own preferences and opinions shape, and possibly distort, our assessment of the research we are reading and writing about. Likewise, journals such as Animal Behaviour, and the societies that support them, could work to bring further visibility to highquality publications from new or emerging study systems. This would help offset the barriers faced by researchers working in nonmodel systems or on critically undervalued insights from natural history. There are many forms this support could take, such as featuring one or two ‘taxonomic breadth’ articles per issue, or strong, substantial natural history research on new systems with high potential for transformative insights. Another alternative is producing yearly special issues (or virtual issues) that highlight emerging systems or tests of generality of established paradigms in new species, as such tests are highly undervalued but are critical to producing the cross-taxon base of knowledge necessary for more synthetic work. There are many potential methods for addressing these concerns, and it is not clear yet which are the most appropriate or the most feasible. We collected data only on the form and magnitude of the skew. Further discussion, studies and innovation will be necessary to determine how to chart a track that will lead to change. Conclusion Our examination and its findings are not intended as an indictment against Animal Behaviour. The biases we describe are endemic to the field, and apparently, to many fields of research, and many journals (e.g. Bonnet et al., 2002; Clark & May, 2002; Fazey,

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Fischer, & Lindenmayer, 2005; Leather, 2009). Additionally, we are not suggesting that these biases are the result of injustices perpetrated by one set of researchers on another, or of prejudices peculiar to ornithologists or mammologists. We suggest these biases are the result of prejudices inherent to all researchers (and possibly all humans) coupled with an academic culture that at best, rarely rewards, and at worst, punishes the kind of research necessary for the long-term viability and growth of our field. We hope that the information and ideas in this article will serve as the beginning of a conversation about the effects of taxonomic bias on the ability of our field to generate strong, integrative hypotheses about the fundamental patterns of animal behaviour, and about how such effects can be addressed. Acknowledgments We gratefully acknowledge the help of Ahiraa Supeinthiran who assisted with early attempts at generating the data set. We also thank members of the Andrade lab for feedback on this project, and on early drafts of the manuscript, and Jackie Sojico for prompting the discussion that originated this project. Supplementary Material Supplementary material associated with this article is available, in the online version, at http://dx.doi.org/10.1016/j.anbehav.2017. 02.017. References Batt, S. (2009). Human attitudes towards animals in relation to species similarity to humans: A multivariate approach. Bioscience Horizons, 2, 180e190. Bonnet, X., Shine, R., & Lourdais, O. (2002). Taxonomic chauvinism. Trends in Ecology & Evolution, 17, 1e3. Borgi, M., & Cirulli, F. (2015). Attitudes toward animals among kindergarten chil€s, 28, 45e59. dren: Species preferences. Anthrozoo Borgi, M., & Cirulli, F. (2016). Pet face: Mechanisms underlying humaneanimal relationships. Frontiers in Psychology, 7, 298. Caro, T. (1999). The behavioureconservation interface. Trends in Ecology and Evolution, 14, 366e369. Chamberlain, S., & Szocs, E. (2013). Taxize: Taxonomic search and retrieval in R [version 2; referees: 3 approved]. F100Research, 2, 191. http://f1000research. com/articles/2-191/v2. Clark, J. A., & May, R. M. (2002). Taxonomic bias in conservation research. Science, 297, 191e192. Czech, B., Krausman, P. R., & Borkhataria, R. (1998). Social construction, political power, and the allocation of benefits to endangered species. Conservation Biology, 12, 1103e1112. Devine, P. G. (1989). Stereotypes and prejudice: Their automatic and controlled components. Journal of Personality and Social Psychology, 56(1), 5e18. Dovidio, J. F., Kawakami, K., Johnson, C., Johnson, B., & Howard, A. (1997). On the nature of prejudice: Automatic and controlled processes. Journal of Experimental Social Psychology, 33, 510e540.

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