Discussion

Applied conservation research is most effective when research findings and conservation outputs are aligned (Balmford et al., Reference Balmford, Gaston, Blyth, James and Kapos2003; Stroud et al., Reference Stroud, Rehm, Ladd, Olivas and Feeley2014; Eklund et al., Reference Eklund, López-Bao, Tourani, Chapron and Frank2017). A discrepancy between these two factors may limit the applicability of research findings for policy and management practices (Balmford et al., Reference Balmford, Gaston, Blyth, James and Kapos2003; Linklater, Reference Linklater2003; Eklund et al., Reference Eklund, López-Bao, Tourani, Chapron and Frank2017; Gray et al., Reference Gray, Booher, Elliott, Kramer, Waller and Millspaugh2019). We detected a misalignment of this type within research on livestock depredation by carnivores in sub-Saharan Africa. Specifically, we found that spotted hyaenas were the central species in only a small proportion of studies despite being the most common primary livestock depredator. Similarly, in over one-third of the studies that reported spotted hyaenas as the primary livestock depredator, they were not a central species in that same study. In contrast, none of the other most common single central species reported to depredate livestock in the reviewed studies (African lion, African wild dog, leopard) showed similar rates of mismatch (Table 1). All three were more commonly central species than the primary livestock depredator. African lions, in particular, were disproportionately listed as the central species relative to their contributions as livestock depredators. They were central species in 45% of the studies but recorded as the primary livestock depredator in only 24% of the studies. These misalignments emerged in both the lexical and document analyses. These patterns are probably attributable, at least in part, to differing levels of charisma among large carnivores.

Species charisma is a relational trait, derived not from the inherent attributes of a species, but from the ways in which people respond to those attributes (Lorimer, Reference Lorimer2007; Albert et al., Reference Albert, Luque and Courchamp2018). Consequently, charisma is subjective and must be interpreted within the context of culture, experiences and values (Smith et al., Reference Smith, Veríssimo, Isaac and Jones2012; Ducarme et al., Reference Ducarme, Luque and Courchamp2013; Albert et al., Reference Albert, Luque and Courchamp2018). Charisma is often used to refer to a species' ability to rally financial support for conservation (Courchamp et al., Reference Courchamp, Angulo, Rivalan, Hall, Signoret, Bull and Meinard2006; Lorimer, Reference Lorimer2007; Macdonald et al., Reference Macdonald, Burnham, Hinks, Dickman, Malhi and Macdonald2015; Albert et al., Reference Albert, Luque and Courchamp2018). As the majority of conservation funding comes from Western societies (Albert et al., Reference Albert, Luque and Courchamp2018), charisma is most often framed in a Western context (Ducarme et al., Reference Ducarme, Luque and Courchamp2013; Courchamp et al., Reference Courchamp, Jaric, Albert, Meinard, Ripple and Chapron2018). Within this Western perspective, African lions and leopards are consistently highly ranked in lists of the most charismatic species (Smith et al., Reference Smith, Veríssimo, Isaac and Jones2012; Macdonald et al., Reference Macdonald, Burnham, Hinks, Dickman, Malhi and Macdonald2015; Albert et al., Reference Albert, Luque and Courchamp2018; Davies et al., Reference Davies, Cowley, Bennie, Leyshon, Inger and Carter2018). African wild dogs are also considered to be charismatic, but their overall cultural appeal is probably reduced because they are comparatively less recognizable outside their range countries (Di Minin et al., Reference Di Minin, Fraser, Slotow and MacMillan2013; Monsarrat & Kerley, Reference Monsarrat and Kerley2018). Spotted hyaenas, in contrast, tend to be perceived negatively nearly everywhere (Dickman, Reference Dickman2010; Macdonald et al., Reference Macdonald, Burnham, Hinks, Dickman, Malhi and Macdonald2015). There are notable examples of local reverence, respect and tolerance for the species (Baynes-Rock, Reference Baynes-Rock2013). However, spotted hyaenas are commonly perceived in Western cultures as ugly, greedy, unintelligent scavengers and are almost exclusively absent from the scientific literature on charisma (Goldman et al., Reference Goldman, De Pinho and Perry2010; De Pinho et al., Reference De Pinho, Grilo, Boone, Galvin and Snodgrass2014; Mitchell et al., Reference Mitchell, Bruyere, Otieno, Bhalla and Teel2019). We infer that these narratives, and comparative lack of charisma, limit the ability of spotted hyaenas to draw financial support from Western institutions for sustained research-informed conservation.

Species such as the African lion, considered to be charismatic in the West (Albert et al., Reference Albert, Luque and Courchamp2018), also tend to be associated with complex social dynamics in their range countries (Inskip & Zimmermann, Reference Inskip and Zimmermann2009; Dickman, Reference Dickman2010; Goldman et al., Reference Goldman, De Pinho and Perry2013). These dynamics may be driven by factors such as the role of the species in traditional ceremonies, the relative socio-economic position of the local communities, or the political history of the region (Inskip & Zimmermann, Reference Inskip and Zimmermann2009; Dickman, Reference Dickman2010; Pooley et al., Reference Pooley, Barua, Beinart, Dickman, Holmes and Lorimer2017). The cultural implications of these factors influence the willingness of local people to participate in conservation actions (Pooley et al., Reference Pooley, Barua, Beinart, Dickman, Holmes and Lorimer2017; van Eeden et al., Reference van Eeden, Crowther, Dickman, Macdonald, Ripple, Ritchie and Newsome2018a,Reference van Eeden, Eklund, Miller, López-Bao, Chapron and Cejtinb). The social context surrounding depredating carnivores is also linked to the species' life history. The African lion, for instance, tends to select cattle over concurrently available smaller livestock such as sheep and goats (Holmern et al., Reference Holmern, Nyahongo and Røskaft2007; Kissui, Reference Kissui2008; Hemson et al., Reference Hemson, Maclennan, Mills, Johnson and Macdonald2009). As in many communities cattle carry higher economic and cultural value than other livestock types, preventing depredation by African lions is of particular importance in many parts of sub-Saharan Africa (Holmern et al., Reference Holmern, Nyahongo and Røskaft2007; Hemson et al., Reference Hemson, Maclennan, Mills, Johnson and Macdonald2009). Combined with high levels of charisma, this cultural context has probably resulted in species such as the African lion being prioritized as central species in human–carnivore conflict research, with less charismatic species, such as the spotted hyaena, under-emphasized. Not all reported measures of livestock depredation in the studies we reviewed were indicative of the financial or emotional impact of livestock loss, and therefore we do not contend that the African lion's prevalence in the literature is without merit. Nevertheless, we did find that taxonomic bias exists within the human–carnivore conflict literature.

This taxonomic bias has two primary consequences for the mitigation of livestock depredation, and therefore for the conservation of large carnivores in sub-Saharan Africa. Firstly, coexistence between people and large carnivores largely depends upon increasing the tolerance of local people for carnivores (Bruskotter & Wilson, Reference Bruskotter and Wilson2014; Treves & Bruskotter, Reference Treves and Bruskotter2014; Pooley et al., Reference Pooley, Barua, Beinart, Dickman, Holmes and Lorimer2017). Tolerance is informed by a complex combination of attitudes, behaviours and perceptions, all of which are informed by socio-cultural norms as well as political and economic trends (Goldman et al., Reference Goldman, De Pinho and Perry2013; Bruskotter & Wilson, Reference Bruskotter and Wilson2014; Treves & Bruskotter, Reference Treves and Bruskotter2014; Margulies & Karanth, Reference Margulies and Karanth2018; van Eeden et al., Reference van Eeden, Crowther, Dickman, Macdonald, Ripple, Ritchie and Newsome2018a,Reference van Eeden, Eklund, Miller, López-Bao, Chapron and Cejtinb). Importantly, tolerance of large carnivores is also strongly influenced by overall rates of livestock depredation (Kolowski & Holekamp, Reference Kolowski and Holekamp2006; Bruskotter & Wilson, Reference Bruskotter and Wilson2014; Treves & Bruskotter, Reference Treves and Bruskotter2014). Increased rates of livestock depredation can degrade human attitudes towards carnivores and increase the probability of retaliatory killing, even for unoffending species or individuals (Romañach et al., Reference Romañach, Lindsey and Woodroffe2007; Miller et al., Reference Miller, Jhala and Jena2016a,Reference Miller, Jhala and Schmitzb; Farhadinia et al., Reference Farhadinia, Johnson, Hunter and Macdonald2017). Spotted hyaenas, as the primary depredators of livestock across much of sub-Saharan Africa, may be eroding human tolerance of sympatric carnivore species. Yet, few studies emphasize livestock depredation by this species.

The second consequence of this bias is the restriction of the knowledge base upon which conservation efforts are built. Taxonomic biases result in a large amount of knowledge on a small number of species, limiting the development of broad theoretical insights (Clark & May, Reference Clark and May2002; Hortal et al., Reference Hortal, De Bello, Diniz-Filho, Lewinsohn, Lobo and Ladle2015; Rosenthal et al., Reference Rosenthal, Gertler, Hamilton, Prasad and Andrade2017). This is not to suggest that research centred on one carnivore species necessarily omits others during fundraising, data collection and analysis. It is possible that the studies we reviewed had comprehensive research-informed conservation programmes that equitably assessed depredation patterns of multiple carnivore species. However, our findings suggest that the resultant publications framed the issue of human–carnivore conflict around a small group of highly charismatic species. As one-third of the studies that identified spotted hyaenas as the primary depredator of livestock did not include them as a central species, it follows that conflict management recommendations derived from these studies are not emphasizing the impact of this species. Additionally, we suspect that conflict management recommendations as a whole are being framed around an understanding of livestock depredation by charismatic species, with recommendations for interventions derived from knowledge of the behavioural patterns of these species. The limited research on livestock depredation by spotted hyaenas indicates they exhibit patterns of depredation different from those of African lions and leopards (Ogada et al., Reference Ogada, Woodroffe, Oguge and Frank2003; Woodroffe et al., Reference Woodroffe, Frank, Lindsey, ole Ranah and Romañach2007; Kissui, Reference Kissui2008). Therefore, interventions built upon understandings of charismatic species may omit behaviours of more common depredators and consequently be limited in their ability to prevent livestock depredation.

The taxonomic bias that we detected in research on livestock depredation by carnivores in sub-Saharan Africa is consistent with other patterns observed in the conservation literature (Clark & May, Reference Clark and May2002; Lawler et al., Reference Lawler, Aukema, Grant, Halpern, Kareiva and Nelson2006; Troudet et al., Reference Troudet, Grandcolas, Blin, Vignes-Lebbe and Legendre2017; Tensen, Reference Tensen2018; Lozano et al., Reference Lozano, Olszańska, Morales-Reyes, Castro, Malo and Moleón2019). Conservation research tends to be biased towards vertebrates, with mammals and birds receiving a level of research effort disproportionate to their prevalence in nature and, in many cases, to their level of extinction risk (Clark & May, Reference Clark and May2002; Donaldson et al., Reference Donaldson, Burnett, Braun, Suski, Hinch, Cooke and Kerr2017; Davies et al., Reference Davies, Cowley, Bennie, Leyshon, Inger and Carter2018). These types of biases correlate with species charisma, resulting in the majority of research focusing on taxa that contain colourful, large, distinctive species (Bonnet et al., Reference Bonnet, Shine and Lourdais2002; Clark & May, Reference Clark and May2002; Lawler et al., Reference Lawler, Aukema, Grant, Halpern, Kareiva and Nelson2006; Donaldson et al., Reference Donaldson, Burnett, Braun, Suski, Hinch, Cooke and Kerr2017). For example, Brambilla et al. (Reference Brambilla, Gustin and Celada2013) found that more appealing bird species in Italy received significantly more research attention, and Fleming & Bateman (Reference Fleming and Bateman2016) reported that unattractive Australian mammals were underrepresented in the literature. The consequences of such biases have been examined in the fields of climate change mitigation (Feeley et al., Reference Feeley, Stroud and Perez2017), animal behaviour (Rosenthal et al., Reference Rosenthal, Gertler, Hamilton, Prasad and Andrade2017), species reintroductions (Seddon et al., Reference Seddon, Soorae and Launay2005) and conservation more broadly (Clark & May, Reference Clark and May2002; Lawler et al., Reference Lawler, Aukema, Grant, Halpern, Kareiva and Nelson2006; Stroud et al., Reference Stroud, Rehm, Ladd, Olivas and Feeley2014; Di Marco et al., Reference Di Marco, Chapman, Althor, Kearney and Watson2017). There is clear evidence that these biases limit the development of ecological theory and conservation management practices (Lawler et al., Reference Lawler, Aukema, Grant, Halpern, Kareiva and Nelson2006; Fleming & Bateman, Reference Fleming and Bateman2016). Thus, taxonomic bias is a potential driver of the research–implementation gap in conservation (Seddon et al., Reference Seddon, Soorae and Launay2005; Amori et al., Reference Amori, Gippoliti and Helgen2008; Martín-López et al., Reference Martín-López, Montes, Ramírez and Benayas2009; Troudet et al., Reference Troudet, Grandcolas, Blin, Vignes-Lebbe and Legendre2017).

Another important component of taxonomic bias relates to conservation funding, which tends to disproportionately support charismatic species (Stroud et al., Reference Stroud, Rehm, Ladd, Olivas and Feeley2014; Fleming & Bateman, Reference Fleming and Bateman2016; Di Marco et al., Reference Di Marco, Chapman, Althor, Kearney and Watson2017; Davies et al., Reference Davies, Cowley, Bennie, Leyshon, Inger and Carter2018; Curtin & Papworth, Reference Curtin and Papworth2020). Many of the largest conservation NGOs explicitly focus their funding efforts on charismatic species (Brockington & Scholfield, Reference Brockington and Scholfield2010a,Reference Brockington and Scholfieldb; Holmes et al., Reference Holmes, Scholfield and Brockington2012). Prioritization of funding in conservation is determined by both political agendas and social contexts (Martín-López et al., Reference Martín-López, Montes, Ramírez and Benayas2009; Stroud et al., Reference Stroud, Rehm, Ladd, Olivas and Feeley2014). Public interest in charismatic species motivates donations, which support further opportunities to study those same species (Davies et al., Reference Davies, Cowley, Bennie, Leyshon, Inger and Carter2018). Furthermore, as reviewers and researchers are implicitly biased towards articles that emphasize their own study organisms, the literature continues to highlight the same subset of charismatic species (Bonnet et al., Reference Bonnet, Shine and Lourdais2002; Wilson et al., Reference Wilson, Proches, Braschler, Dixon and Richardson2007; Martín-López et al., Reference Martín-López, Montes, Ramírez and Benayas2009; Rosenthal et al., Reference Rosenthal, Gertler, Hamilton, Prasad and Andrade2017). This bias is evident in carnivore conservation, with large felids consistently receiving more funding and research effort than other species (Davies et al., Reference Davies, Cowley, Bennie, Leyshon, Inger and Carter2018; Curtin & Papworth, Reference Curtin and Papworth2020), which is particularly notable in Africa (Di Marco et al., Reference Di Marco, Chapman, Althor, Kearney and Watson2017). For example, in 2017 the Leonardo DiCaprio Foundation announced a USD 1 million seed donation to establish the Lion Recovery Fund in collaboration with the Wildlife Conservation Network. This effort was subsequently supported by a variety of additional sponsors, including the Disney Conservation Fund. Within its first year, the fund distributed c. USD 2.4 million across 28 research and conservation projects centred on the African lion (Lion Recovery Fund Progress Report, Reference Lion Recovery Fund2018). Similarly, National Geographic's Big Cat Initiative had an open request for proposals, up to mid 2021, for research programmes examining lion conservation in 20 lion-specific priority areas. Through this initiative, up to USD 100,000 of support was awarded per project. These conservation funds are allocated across a geographical range where less charismatic spotted hyaenas co-occur and tend to be more problematic for livestock owners than African lions.

It is possible that the negative effects of taxonomic bias could be ameliorated by the flagship species concept, with conservation of co-occurring species aided by the focus of conservation attention on large, charismatic species (Andelman & Fagan, Reference Andelman and Fagan2000; Roberge & Angelstam, Reference Roberge and Angelstam2004; Smith et al., Reference Smith, Veríssimo, Isaac and Jones2012; Albert et al., Reference Albert, Luque and Courchamp2018). Flagship species tend to be large-bodied mammals that are often described as beautiful or impressive (Albert et al., Reference Albert, Luque and Courchamp2018). Conservation status can also contribute to species charisma (Martín-López et al., Reference Martín-López, Montes, Ramírez and Benayas2009; Albert et al., Reference Albert, Luque and Courchamp2018). Species at greater risk of extinction, particularly those that are charismatic, tend to motivate conservation engagement and fundraising (Courchamp et al., Reference Courchamp, Angulo, Rivalan, Hall, Signoret, Bull and Meinard2006; Smith et al., Reference Smith, Veríssimo, Isaac and Jones2012; Brambilla et al., Reference Brambilla, Gustin and Celada2013; Albert et al., Reference Albert, Luque and Courchamp2018). The spotted hyaena is categorized as Least Concern on the IUCN Red List and thus carries little power for motivating conservation engagement from the perspective of species rarity. However, the African lion and leopard are categorized as Vulnerable and the African wild dog as Endangered. As the populations of these three species continue to decline, their value as conservation flagships grows (Martín-López et al., Reference Martín-López, Montes, Ramírez and Benayas2009; Ripple et al., Reference Ripple, Estes, Beschta, Wilmers, Ritchie and Hebblewhite2014; Wolf & Ripple, Reference Wolf and Ripple2017). However, the extent to which the flagship species concept demonstrably supports the conservation of species other than the flagship is a source of debate (Andelman & Fagan, Reference Andelman and Fagan2000; Caro et al., Reference Caro, Engilis, Fitzherbert and Gardner2004).

Recent studies have indicated the benefits of strategic prioritization of charismatic species to further broad-scale biodiversity conservation (Smith et al., Reference Smith, Veríssimo, Isaac and Jones2012; Bennett et al., Reference Bennett, Maloney and Possingham2015; McGowan et al., Reference McGowan, Beaumont, Smith, Chauvenet, Harcourt and Atkinson2020). However, such an approach may have adverse effects on the development of practices intended to address human–carnivore conflict. We recognize that as our study focuses on large carnivores in sub-Saharan Africa, it could be considered to have its own bias. Nevertheless, we believe our critical assessment contributes to the literature on human–carnivore interactions by helping to improve the conservation impact of future research in this field. Our findings indicate that current patterns of research prioritization are resulting in a misalignment between the drivers of human–carnivore conflict and research on that topic. Consequently, conflict intervention practices founded upon that research may be limited in their ability to mitigate declines in large carnivore populations. Solutions for this global conservation challenge may be better served by alternate prioritization schemes that promote species-specific knowledge and more comprehensive understanding of the patterns of livestock depredation. We advocate increased incentivization of the study of livestock depredation by less charismatic carnivore species, including the spotted hyaena. This will facilitate the explicit examination of the effectiveness of conflict mitigation efforts.

The call for research on less charismatic species is often based upon the conservation status of those species, where their relative omission from the literature may be increasing their risk of extinction (Seddon et al., Reference Seddon, Soorae and Launay2005; Brambilla et al., Reference Brambilla, Gustin and Celada2013). Here, we provide evidence for an additional motive for addressing this bias, as the underrepresentation of spotted hyaenas is unlikely to put the species itself at risk of extinction. Instead, we show that in the case of livestock depredation, and subsequent human–carnivore conflict, this bias may be negatively impacting the conservation of other depredating species as well. As taxonomic bias is widespread in conservation, further examination is likely to reveal similar trends in other regions and fields of study. Our study suggests that increased examination of current patterns of funding and research effort is needed to bridge the existing gap between conservation priorities and conservation research.