Firstly, given the increasing European focus on the use of raptors as biomonitors, we hypothesized that African vultures could also be useful as biomonitors. We, therefore, aimed to identify whether the respective African vulture species would be well-suited for use as avian biomonitor species, by comparing each African vulture species to all bird species, within the limits of available knowledge for each bird species. Secondly, in recognizing the dire conservation status of African vultures and that time and funds for their conservation are limited, we hypothesized that one vulture species could be used as an umbrella for all (or most) of the other African vulture species. Therefore, we aimed to evaluate each African vulture species in terms of its potential to act as an umbrella species for all African vulture species.

To assess whether the respective African vulture species would be appropriate for use as biomonitors, we considered all 10 species that occur regularly in Africa (Table 2; Mundy, 2016).

We excluded the Cinereous Vulture (Aegypius monachus) from our analyses because its core range is in Asia, Europe, and the Arabian Peninsula, and its occurrence in Africa is irregular (Copete, 2018a,b; Daboné et al., 2021). We included the Palm-nut Vulture (Gypohierax angolensis) because, although its diet includes a large proportion of plant matter (Mundy et al., 1992; Carneiro et al., 2017), it is widespread throughout Africa (IUCN, 2021; Table 2), and there is no genetic (Lerner and Mindell, 2005) or anatomical (Chapin, 1932) evidence to support its exclusion.

In the following assessments of the 10 African vulture species as avian biomonitors, and as umbrella species for all African vultures, our methods were based on data from the peer-reviewed scientific literature to ensure objectivity and repeatability of our results. Where published data were lacking, we relied on expert opinions which were pooled and the consensus was used, and we highlighted this approach in the Supplementary Materials (Supplementary Tables 1, 2).

To achieve our first aim of identifying whether African vultures (either as a group of species or as individual species) could be used as biomonitors, we compiled a list of criteria considered to be important when selecting an avian species as a potential biomonitor, following Landres et al. (1988) and Fleishman et al. (2000). We based our criteria for selecting an avian biomonitor on the list proposed by Hollamby et al. (2006), who provided their criteria based on a literature review and their own observations. They proposed 20 criteria for evaluating a candidate bird species' suitability as a biomonitor of environmental change based on the knowledge of its biological traits.

To make our scoring of the respective African vulture species as clear, repeatable, and objective as possible, we provide a quantitative classification scale for each criterion (Supplementary Table 1) with detailed information regarding (i) the variable used to measure each criterion; (ii) a description of the values for each score; (iii) the range of scores given for each criterion; (iv) the range of possible scores; and (v) the relevant table number where additional information is provided.

Seven of the 20 criteria suggested by Hollamby et al. (2006) related to the collection, transportation, or storage of the biological samples. We could not assess those seven criteria in this study without knowing which samples a researcher may collect as there is a great variety of samples that could be collected from vultures (e.g., Espín et al., 2021), and ideally, each one should be individually assessed in a separate study. We excluded those seven criteria from our analysis, retaining the other 13 criteria proposed by Hollamby et al. (2006); (Table 3).

We evaluated the 10 African vulture species (listed in Table 2) individually, for each of the criteria in Table 3, ranking the species from best- to worst-fit in terms of their suitability as biomonitors.

Our second aim was to evaluate the potential of each of the respective African vulture species as an umbrella species for all the African vulture species. Following the recommendations of Landres et al. (1988), we compiled a list of criteria for selecting an umbrella species (Seddon and Leech, 2008; Table 4). This method relies on information related to species' traits that are broadly similar to the traits proposed by Branton and Richardson (2011), and Maslo et al. (2016), for selecting an umbrella species.

We evaluated the 10 African vulture species (Table 2) individually for each of the criteria in Table 4 ranking the species from best fit (usually represented with a score of “1”) to worst fit (usually represented with a score of “10”). To make our scoring of the respective African vulture species as clear, repeatable, and objective as possible, we provide a quantitative classification scale for each criterion (Supplementary Table 6), with detailed information regarding (i) the variable used to measure each of the seven criteria, (ii) a description of the values for each score, (iii) the range of scores given for each criterion, (iv) the range of possible scores, and (v) the relevant table number where further detail is provided. The methods used to score the respective African vulture species against each criterion are presented in the Supplementary Materials. We then ranked the species, according to their scores, in terms of their suitability as an umbrella species for all the African vulture species.

Of the 10 African vulture species, the White-backed Vulture (Gyps africanus) was the best suited as a potential avian biomonitor species, and the Cape, Rüppell's and Lappet-faced Vultures tied as the second-best (Table 5). The Palm-nut Vulture was the worst suited as a biomonitor species.

As a group, African vultures scored well for some criteria. Relative to all birds, African vultures have large body sizes (criterion 2) and long lifespans (criterion 3); the various sizes, ages, and sexes can be distinguished (criterion 4); they can be monitored over numerous seasons (making them suitable for long-term monitoring, criterion 6); they are non-migratory and non-nomadic during the breeding season (criterion 7); and they also have well-known reproductive cycles (criterion 10).

Some African vulture species do not have large population sizes, and these species (the Griffon, Egyptian, and Bearded Vultures) scored poorly for criterion 1. While the biology and foraging ranges of most African vulture species are well-known, knowledge on these two aspects for the Palm-nut Vulture is relatively lacking, and so this species scored lower than the others for criteria 5 and 9.

Some African vulture species (e.g., the Palm-nut, Hooded, and Egyptian Vultures) scored poorly for criterion 8, because of the variation in their diets, while the Gyps vultures scored well, because of their fairly restricted diets (Supplementary Materials; Supplementary Table 2). Related to this, most African vulture species occupy a high-trophic level (Table 5), allowing the study of chemicals that bioaccumulate, and so most species scored well for criterion 11 (Supplementary Materials; Supplementary Table 3). There was variation in the scores for criterion 12, as we regarded some vulture species (particularly the more commensal species) easier and cheaper to trap for sampling (in ideal trapping scenarios) than the others. For criterion 13, we found no information on how the public views the use of vultures as bioindicators, and so all species scored poorly for this criterion (Supplementary Materials; Supplementary Table 4).

The White-backed Vulture was the best suited of all 10 African vulture species as a potential umbrella species for all African vultures (Table 6). The Rüppell's Vulture was the second-best, and the Cape Vulture was the third-best. The Bearded and Palm-nut Vultures were tied as the worst suited as umbrella species (Tables 6, 7).

In terms of knowledge on the natural history and ecology for each species (criterion 1), the White-backed Vulture scored the best with the most knowledge, and the Palm-nut and Griffon Vultures tied as the worst since the least is known about these two species (Supplementary Materials; Supplementary Table 5). According to the information from published studies, the White-backed, Rüppell's, Cape, and Lappet-faced Vultures have the largest home-range sizes, and so these four species scored the best for criterion 2, while there were no data available for the Palm-nut Vulture that we presumed had the smallest home-range size, and was scored the worst for this criterion, along with the Egyptian, White-headed, and Bearded Vultures, which all have relatively small home-range sizes (compared with the other vulture species, Supplementary Materials; Supplementary Table 7). For the probability of population persistence (criterion 3), all the vultures scored poorly, however, the Palm-nut Vulture scored the best for this criterion (there is no evidence of declines for this species), while most of the remaining species scored a “10” (76–100% declines in the three generations, Supplementary Materials; Supplementary Table 8). For criterion 4, the Hooded, Lappet-faced, and White-backed Vultures scored the best, as their ranges most overlapped (and their threats were common to) those of the other vulture species, while the Cape and Bearded Vultures scored the worst since their ranges overlapped little of the other vulture species' ranges (Supplementary Materials; Supplementary Table 9). For criterion 5 (has management needs that overlap those of other species), there was little variation in the scores for each species; the Palm-nut Vulture scored the worst (a “7”), while most other African vulture species scored better, with a “5” (Supplementary Materials; Supplementary Table 10). For criterion 6 (should be sensitive to human disturbance), the Palm-nut, Egyptian and Hooded Vultures scored the poorest (with scores of “5,” “7”, and “10,” respectively, since they breed and/or forage in areas disturbed by people), while all the other species received a score of “1” since we regarded them as sensitive to human disturbance (Supplementary Materials; Supplementary Table 11). Finally, in terms of the ease with which a species may be monitored (criterion 7), the Bearded Vulture scored the worst because of its inaccessible habitat, the tree-nesting species scored better, and the remaining cliff-nesting species scored the best (Supplementary Materials; Supplementary Table 12).

Our assessment showed that of the 10 African vulture species, the White-backed Vulture was the species that was best suited as a biomonitor. It scored well for every criterion apart from “public acceptance of the species as a biomonitor” (criterion 13). As a group, the African vultures are suited for use as biomonitors in some respects: they have large body sizes and long lifespans; the various sizes, ages, and sexes can be distinguished; they can be monitored over numerous seasons, making them suitable for long-term monitoring; and they have well-known reproductive cycles.

Most African vulture species scored well for criterion 11 (they occupy a high trophic level, and so can be used to study chemicals that bioaccumulate), however, there may be intraspecific variation in their diets and feeding habits; some Hooded Vultures in West Africa forage along coastlines (Barlow, 2020), increasing their potential exposure to mercury (Diop and Amara, 2016) and persistent organic pollutants (Camacho et al., 2013), while Hooded Vultures in southern Africa do not display this beachcombing behavior. These differences in feeding habits and diet between regions must be considered if using vultures as biomonitors to study chemicals that bioaccumulate.

We found no differences between the respective vulture species in terms of how the public views them, despite there being numerous studies worldwide that have investigated people's perceptions of vultures (e.g., Phuyal et al., 2016; Cailly Arnulphi et al., 2017; Cortés-Avizanda et al., 2018; Morales-Reyes et al., 2018; Duriez et al., 2019; García-Alfonso et al., 2019), including several in Africa (Santangeli et al., 2016; Craig et al., 2018; Deikumah, 2020; Mashele et al., 2021a,b). These studies tend to focus on the perceptions of people who live in communities bordering protected areas (e.g., Reson, 2012; Mdhlano et al., 2018), who bear the opportunity costs of conservation areas, i.e., disproportionate lost benefits from other land use (Adams et al., 2010). Fewer studies explore the perceptions of vultures among people in the Global North (George et al., 2016; Kluever et al., 2020) and/or urban areas (e.g., Campbell, 2009), who are wealthier and more likely to fund research or conservation work for vultures. We believe that there is a need for vulture attitude and perception studies in urban communities.

We scored all the African vulture species well for criterion 7 (they are all non-migratory and non-nomadic during the breeding season), but their home ranges, even during the breeding season when movements of adults are more constrained, are vast compared with those of many other bird species. Therefore, toxins in the tissues of African vultures could only be used to show trends in environmental pollution (e.g., in lead toxicity, Garbett et al., 2018; van den Heever et al., 2019) at massive (regional) scales, after which, other species (with smaller home ranges) would have to be used as biomonitors to pinpoint where environmental pollution is occurring on a finer scale, so that clean-up measures may be initiated. For this reason, and because all African vultures scored poorly on the criterion “Public acceptance of the species as an indicator” due to the lack of knowledge on this subject (Hollamby et al., 2006, p. 15), we believe that African vultures are, at present and relative to other species of birds, not ideally suited as avian biomonitors.

Our assessments showed that the White-backed Vulture is the African vulture species that is best suited for use as an umbrella species for all 10 African vulture species. The White-backed Vulture is the most suited as a potential umbrella species for all African vultures because: (i) its natural history and ecology are the best known of all 10 vulture species; (ii) it has one of the largest home-ranges of all the vulture species; (iii) it is the most widely distributed across Africa (i.e., it co-occurs with and represents the other vulture species); (iv) its management needs will benefit co-occurring species; (v) it is sensitive to human disturbance; and (vi) it is among the easiest to monitor (mainly due to its nests being the easiest of all the tree-nesting vulture species' nests to monitor; Thompson et al., 2018). Using the White-backed Vulture as an umbrella species for all African vultures may assist conservation practitioners in Africa to save time, money, and effort while still working toward their mandates of protecting all vulture species and the ecosystem services they provide (Safford et al., 2019). Where nesting areas of various vulture species overlap, nest monitoring efforts and studies of breeding success and productivity could focus on the White-backed Vulture. Similarly, focusing on addressing the threats to White-backed Vultures will address many of the management needs of co-occurring vulture species (Ogada et al., 2016; Botha et al., 2017; Murn and Botha, 2018; Thompson et al., 2020). The use of the White-backed Vulture as an umbrella species may augment other vulture conservation tools, such as identifying priority areas for conservation (Santangeli et al., 2019), retrofitting unsafe energy infrastructure (Perold et al., 2020), reducing wildlife poisoning, and its effects (Gore et al., 2020), reducing the trade in vultures for bushmeat and traditional medicine (Buij et al., 2016; Boakye et al., 2019), phasing out lead ammunition (Margalida et al., 2013), and encouraging hunting (which both preserves habitat and provides food for vultures) where appropriate (Mateo-Tomás and Olea, 2010). However, we should not overlook the conservation needs of any vulture species whose distributions, diets, and other natural history traits (Table 6) are not well-represented by the White-backed Vulture.

Dulsat-Masvidal et al. (2021) highlighted the legislative constraints when using raptors as biomonitors in Europe. In Africa too, vultures are protected by various international, regional, and sub-regional legal instruments (Thompson and Blackmore, 2020), which may make their use as biomonitors more challenging. Future assessments of species as potential avian biomonitors should include the requirement for non-threatened status. Any assessments of vultures as biomonitors or as umbrellas should also be periodically revised, to incorporate increases in knowledge, and changing public and expert opinion.

In our evaluation of the African vultures as biomonitors, we excluded specific criteria proposed by Hollamby et al. (2006) that relate to chemicals because this evaluation cannot be done until the chemicals to be studied have been chosen, and that does not fall within the remit of this study. Three of the criteria (numbers 6, 15, and 17) proposed by Hollamby et al. (2006) relate to the sensitivity of a candidate species to a particular chemical. While it is implicit that biomonitors must be sensitive to the chemicals under study, this has not been evaluated here, and the inclusion of these three (and the remaining excluded) criteria of Hollamby et al. (2006) could produce different results in terms of which vulture species is best suited as a biomonitor.

The disadvantage of selecting the White-backed Vulture as an umbrella for all the African vultures is that, like many other vulture species, it has a low probability of population persistence. If the White-backed Vulture is used as an umbrella species, then the Palm-nut Vulture may need additional, complementary monitoring, and conservation actions, since the Palm-nut Vulture's diet, habitat and threats are not well-covered by the White-backed Vulture.

The criteria against which we scored the respective African vulture species were partly based on qualitative data, provided by pooling of expert opinion. We acknowledge that there may be uncertainty in the predictions made using expert-based models (Johnson and Gillingham, 2004); however, we believe that our elicitation of expert knowledge was done rigorously, allowing us to rank the species in a cost-effective manner when quantitative data for certain criteria were lacking (Kuhnert et al., 2010). While this means that our datasets are not ideally suited for conducting sensitivity analyses (Thabane et al., 2013), we can still comment on the ways in which differences in scoring could affect the ranking of species. With regards to how knowledge gaps may have affected our scoring and ranking of species as biomonitors, an increase in knowledge regarding the biology (criterion 5) and the foraging range (criterion 9) of the Palm-nut Vulture could improve its score as a biomonitor from 47 to 34, which would change its ranking from 10th to 7th. Similarly, if awareness campaigns caused the public acceptance of a particular vulture species as a biomonitor (criterion 13) to change from “unknown” to a 91–100% acceptance rate, then the species' score for this criterion would change from 10 to 1, changing its ranking which could elevate the Cape, Rüppell's, Lappet-faced, Hooded or White-headed Vultures into 1st place.

In terms of how knowledge gaps may have affected our scoring and ranking of species as umbrellas, the down-listing of the global status of the Cape Vulture in December 2021 from endangered to vulnerable could change its scoring for criterion 3 from “10” to “8,” although this change alone will not alter its ranking as tied third-best umbrella. However, the rank of a species could be affected by an increase in knowledge about its natural history and ecology (criterion 1), for example, an increase in the number of publications on the Palm-nut Vulture could elevate its rank as an umbrella species above its current 9th place. An increase or decrease in a species' range could change the scoring of the species for criterion 4 (co-occurs with and represents species of interest, with threats common to both). Finally, criterion 7 (ease of monitoring) was scored by expert opinion, and, if other experts had scored this criterion, could be slightly different, based on their experience. We highlight that this study is an initial step in testing African vultures as umbrellas and biomonitors with data that are currently published and the combined experiences of experts who work with African vultures.