Received: 6 June 2022 | Revised: 1 September 2022 | Accepted: 5 September 2022 DOI: 10.1002/edn3.363 C O M M E N TA R Y Environmental DNA surveys of African biodiversity: State of knowledge, challenges, and opportunities Sophie von der Heyden Evolutionary Genomics Group, University of Stellenbosch, Matieland, South Africa Correspondence Sophie von der Heyden, Evolutionary Genomics Group, University of Stellenbosch, Private Bag X1, Matieland, 7602, South Africa. Email: svdh@sun.ac.za Abstract Environmental DNA surveys have become a well-­established tool for detecting natural communities, showing excellent promise for supporting biodiversity monitoring, conservation, and management efforts. Africa is a continent of exceptional biodiversity, threatened not only by anthropogenic pressures but also by a general lack of research capacity and infrastructure, limiting evaluation and monitoring of ecosystems. This commentary explores the use of environmental DNA in surveying natural diversity, a rapidly moving field, within the context of capturing Africa's natural capital. Through an extensive literature search and filtering, 65 papers from 22 countries were identified, with research from Madagascar and Africa forming the bulk of the literature (~38%), with many countries only represented by one to three papers. There was a diverse range of studies, with more than half reporting on communities or diet analyses; freshwater and marine research are underrepresented, accounting for ~5% of studies. There were some papers on disease monitoring, particularly in freshwater. Disturbingly, representation of authors was highly skewed and highlights the ongoing inequality of scientific publishing and the extent of parachute science; one-­third of papers (n = 21) reported no African representation, in contrast with the 18 papers that had either first or senior authors affiliated with an institution in Africa. The remainder of the papers (n = 27) had at least one author affiliated with an African institution. In addition, less than half of papers reported appropriate sampling permits. Importantly and with a concerted global effort, building long-­term capacity, through meaningful and equitable relationships will help increase self-­sustaining science around technologies based on eDNA, thus ensuring not only biodiversity but also humanitarian benefits across Africa. 1 | I NTRO D U C TI O N much of which supports crucial ecosystem services and ~16% of the global population. From the Cape Floristic region at the tip of The African continent and associated islands, both in the Indian and the continent to the desert and mountainous regions of northern Atlantic oceans, is without a doubt one of the biodiversity jewels Africa, the African continent harbors eight of the world's biodiver- of the world. Its uniqueness of natural biodiversity is unparalleled, sity hotspots (Myers et al., 2000), ranging from temperate to tropical This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2022 The Author. Environmental DNA published by John Wiley & Sons Ltd. 12 | wileyonlinelibrary.com/journal/edn3 Environmental DNA. 2023;5:12–17. | HEYDEN 13 and high to low rainfall areas and diverse ecosystems such as rain- authorship contributions and also touches on permitting. As such forests to deserts with some of the lowest rainfall globally. As else- this work provides insights into the future of eDNA surveys in Africa, where, urbanization (Güneralp et al., 2017), agricultural expansion whilst highlighting the necessity for equitable access to ensure that and land cover changes (Brink & Eva, 2009; Marchant et al., 2018), not only African biodiversity is documented and accounted for, but alien and invasive species (Linders et al., 2021), overexploitation that the continent can thrive through capacity building, equal ac- (Riggio et al., 2018) and the effects of climate change (Dejene, 2018; cess, and applied solutions to safeguarding biodiversity through the Pecl et al., 2017) all threaten Africa's unique biodiversity and the exciting technologies that eDNA offers. ecosystem services they provide (Archer et al., 2021). Although patterns of biodiversity in Africa are broadly understood, there remain ongoing challenges for monitoring species and 2 | M E TH O D S communities. This is especially problematic in the context of climate change, where species are known to shift their ranges in response to A Web of Science search was carried out in February 2022 with environmental variation (Brodie et al., 2021; Carvalho et al., 2021; the following search terms (“Country” AND eDNA) OR (“Country” Dejene et al., 2021; Pecl et al., 2017) and it is likely that for the vast AND “environmental DNA”) OR (metabarcoding AND “Country”) OR majority of African biodiversity, contemporary distribution patterns (“Country” and “eDNA metabarcoding”) where “country” was sub- or even broad habitat requirements, which would allow for pre- stituted for each of the 58 countries in Africa. In addition, a search dictive modeling of future ranges, are undocumented. This lack of for “Country” AND “environmental DNA” AND “biomonitoring” was biodiversity knowledge limits opportunities for maximizing conser- carried out to ensure that the first round of searches did not exclude vation and management opportunities that can benefit biodiversity papers with a biomonitoring focus. Following Antich et al. (2021), and people and strengthen their resilience under climatic change the term “environmental DNA” was used to generally include “any (Dejene, 2018; Kapuka & Hlásny, 2021). DNA extracted from an environmental sample.” All papers were ex- Given the numerous logistical and financial challenges associated ported into an Excel database for further assessment. Papers with with monitoring biodiversity, particularly in remote or deep aquatic the sole focus on microbial diversity were not included for analyses ecosystems, environmental DNA surveys have become a well-­ and only papers with multicellular eukaryotes retained (with the ex- established as a tool for detecting natural communities from water, ception of two studies that focused on the gut microbiota of host sediment, and even air (Deiner et al., 2017; Gaither et al., 2022; animals); methods papers were also excluded. In addition, one paper Ruppert et al., 2019; Thomsen & Willerslev, 2015). Environmental from Mozambique was excluded as the work was not conducted in DNA approaches have been used to detect rare, endangered, or in- the country but rather in the Mozambique Channel; relevant papers vasive species (Franklin et al., 2019; Wilcox et al., 2013) and even from La Reunion and Mayotte (n = 7) were also not included in the contributed toward our understanding of population genetic struc- final list given their designations as overseas departments of France, turing in natural populations (Adams et al., 2019). Species monitoring rather than independent African states. based on eDNA surveys has been shown to be comprehensive and Post filtering and retention, papers were scanned and broadly likely have broad applicability in conservation and management (Bani divided into the following categories: (1) Marine, terrestrial, or et al., 2020; Barnes & Turner, 2016; Beng & Corlett, 2020). However, freshwater; (2) community or diet study or gut microbiome or par- despite the numerous benefits of carrying out biodiversity surveys asite or species detection (but excluding parasites such as free-­ using eDNA and the general ease with which to collect samples, living parasites such as schistosomiasis, which were included in generating data is complex, requiring specialized DNA extraction “parasites”). To identify the spread of eDNA studies across Africa venues, as well as access to advanced sequencing platforms (e.g., the country where each study took place was noted, as well as Illumina MiSeq or HiSeq). Such challenges have likely led to uneven the composition of the authors on the paper; specifically, (1) the applications of eDNA surveys globally, with tropical regions, South number of papers with first or senior authors affiliated with an America, and Africa reporting significantly fewer eDNA studies than institution in Africa, (2) the number of papers with an author af- the Northern Hemisphere (for example in freshwater surveys Belle filiated with an African institution elsewhere on the author line (ex- et al., 2019) and there have been calls to ensure more equal access cluding first/senior authors) and (3) the number of papers without to data generated from eDNA biodiversity surveys to ensure better any African representation. The latter was carried out to identify uptake and application (Berry et al., 2021). Paradoxically, Africa's im- African participation in developing environmental DNA barcoding portance to global biodiversity and associated ecosystem services and to gauge the extent of “parachute science,” that is instances will be severely undermined without equitable access to eDNA tech- where researchers from one country (primarily the global North) nologies and all the benefits this offers for biodiversity monitoring. conduct studies in another (mostly the global South), without This commentary explores environmental DNA surveys from a wide including or engaging with people from that nation, effectively range of environmental samples in order to provide a state of knowl- sidelining researchers or other stakeholders from a scientific inves- edge of the field in Africa. In addition to investigating the applicabil- tigation (Asase et al., 2020; de Vos & Schwartz, 2022; Stefanoudis ity of eDNA for biodiversity surveys, this commentary also explores et al., 2021). Finally, for each paper, it was noted whether a collec- the “academic” origin of eDNA research through investigating tion or research permit was provided. 26374943, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/edn3.363 by Namibia Hinari NPL, Wiley Online Library on [01/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License von der 3 | von der | R E S U LT S A N D D I S CU S S I O N 3.1 | Environmental DNA surveys have diverse applications in Africa HEYDEN 3.2 | Unequal representation of host nations on eDNA-­based research and a lack of research permits Representation of authors was surprisingly skewed and highlights the ongoing inequality of scientific publishing and in particular parachute The WoS search returned 103 papers, with 65 retained after assess- science. Only ~28% of papers had first or senior authors affiliated with ment (excluded papers were either not focused on eDNA or reported African institutions in “host nations” (i.e., where the research was car- on free-­living microbial communities; available in Table S1). The ma- ried out; Figure 1), which is fewer than the 32% of papers that had no jority of studies were carried out on terrestrial ecosystems (n = 51), African institution affiliated authors listed on the author line, although with only nine and five focusing on marine or freshwater systems, re- some of these papers list African participants in acknowledgments for spectively. There was a wide geographic spread in the 22 countries enabling research through fieldwork and support. The remainder of in which eDNA surveys were carried out, but for many of these only publications had some African representation as middle authors. Most between one and five studies were recorded (Figure 1). Research from of the latter category only had one or two African authors and only only two countries, Madagascar (n = 10) and South Africa (n = 15) one country, South Africa, had papers where all authors were associ- made up ~38% of all eDNA studies. There was a wide array of study ated with African institutions. These findings show a deep disconnect systems, but community and diet studies made up the bulk of the re- of African researchers from what is happening elsewhere globally, search (~70%; Figure 1), with ~23% of papers having a focus on either which is highly problematic given the accelerating developments in free-­living or internal parasites, the latter particularly mammals. Gut the field. This is further underscored by how many papers listed per- microbiome and species detections studies made up less than 2% of missions for accessing environmental samples, with less than half of all studies (Figure 1). There was a diverse range of focal taxa, from the papers providing details on permits or similar. Permits were most fungal communities associated with root systems of trees, to large likely to be reported when working in Madagascar, South Africa, or charismatic mammal species such as cheetahs, rhinos, and elephants. those studies focusing on large mammals. It was surprising that pa- Studies carried out in freshwater systems, targeted either invasive pers without explicit permit statements were published, given that the species (such as Silver carp) or parasite detection. Several papers fo- majority of established publishers require collection and permission cused on agricultural aspects, including detection and dynamics of information, highlighting that publishers need to do better on report- pest species and their management, as well as the detection of human ing requirements. Finally, although not explicitly analyzed, the vast diseases, not only in freshwater systems but also mammalian hosts. majority of funding stemmed from outside of Africa (with only South F I G U R E 1 Map of Africa providing an overview of the number of papers on environmental DNA surveys retrieved for each country (central panel), as well as a subset of taxonomic diversity targeted in studies (green panel). The top graph shows the different categories of eDNA research (note that “species detection” excludes parasites), whereas the bottom graph notes authorship of studies. The size of the circles on the main map indicates the number of studies. 26374943, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/edn3.363 by Namibia Hinari NPL, Wiley Online Library on [01/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 14 | HEYDEN 15 research field but extends to other biological areas such as human BOX 1 health, genomics, and biodiversity monitoring (Chu et al., 2014; Stephenson & Ruiz de Pas, 2022; Svardal et al., 2020). For example, There are many exciting opportunities for expanding eDNA Svardal et al. (2020) highlight numerous barriers when carrying out workflows and studies in Africa. Although several global genomic research in Africa, with a lack of access to resources and initiatives such as the Ocean Best Practices (OBIS) and finances probably the largest inhibitors to growing genomic capac- UNESCO have environmental DNA working groups, these ity in Africa. Parachute science is another significant challenge by themselves are not sufficient to address the inequality identified in this commentary, as it has been elsewhere (Asase of research. As such, the recommendations below echo et al., 2020; de Vos & Schwartz, 2022; Stefanoudis et al., 2021). those made elsewhere (see for example Chu et al., 2014; Unlike working directly with plants or animals, environmental DNA O'Connell et al., 2017; Schmeller et al., 2017; Stephenson samples from water and sediment are particularly easy to collect, & Ruiz de Pas, 2022; Svardal et al., 2020): transport and process, making them more susceptible to collection 1. Meaningful collaborations that include African re- and transport without permits. This makes it difficult to enforce searchers and allow for capacity building for long-­term eDNA work, particularly if there is a lack of oversight from funding self-­sufficiency, thereby minimizing dependence on ex- bodies and publishers. This challenge has to be addressed outside ternal researchers. This includes the identification of of Africa and lies predominantly with researchers themselves, who research problems and co-­creation of projects, includ- have ethical obligations toward the biodiversity capital of other ing access to funding. Although some efforts are made nations. Further, the importance of the identification of research around citizen science and citizen involvement is laud- and knowledge gaps and the co-­creation of projects by African and able and important, alone it is not substitutes for knowl- other partners, to fill those gaps is not only crucial for bridging edge sharing and meaningful collaborations at a higher the science-­p olicy interface but has the potential to revolution- level. ize how science can be applied to solve real-­world challenges. For 2. Ensuring and enabling access to eDNA biodiversity data example, in this review, one paper dealt specifically with human through standardizing repositories and eDNA reporting, health and monitoring disease vectors but did not include African which includes not only data but also methods (Berry collaborators for whom such data is relevant for managing disease et al., 2021), in order to facilitate researchers unable to or provide any insights as to how the data might be used to bet- fund international travel access to the latest in eDNA ter manage vector-­b orne disease. This shows a vast disconnect developments. between research through parachute science, which can only 3. Publishers and funders must ensure that appropriate limit the development of science and its application. Overall, for and valid permits/permissions for sample collection are African biodiversity research to fully benefit from the exciting op- obtained and reported. portunities that environmental DNA surveys have to offer, deep, 4. Continued building of DNA barcode databases to allow for more accurate linking of specimens from eDNA data, long-­term, and equitable working relationships are foundational to achieving fully integrated and self-­sustaining eDNA research. thus supporting conservation, management, and spatial planning (Bani et al., 2020; Cristescu, 2014). AC K N OW L E D G M E N T I sincerely thank Courtney Gardiner for help with the creative artwork and Wiley Publishers for granting a waiver that supported the OA fees for this paper. Africa providing significant financial support to environmental DNA research). As such funding bodies, including those supported through C O N FL I C T O F I N T E R E S T the EU and NSF need to do more to provide oversight and to positively The author declares no conflict of interest. influence their grantholders not only regarding appropriate permitting but also to ensure meaningful participation of researchers and other DATA AVA I L A B I L I T Y S TAT E M E N T stakeholders for capacity development, especially for countries out- No new data was generated for this article. side their immediate jurisdiction. ORCID 3.3 | A way forward for eDNA biomonitoring in Africa Although the diverse range of eDNA-­ based research in Africa is encouraging, numerous challenges remain (see Box 1), but a global approach will find solutions. This is not unique to the eDNA Sophie von der Heyden https://orcid.org/0000-0001-9166-976X REFERENCES Adams, C. I. M., Knapp, M., Gemmell, N. J., Jeunen, G.-­J., Bunce, M., Lamare, M. D., & Taylor, H. R. (2019). 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Environmental DNA surveys of African biodiversity: State of knowledge, challenges, and opportunities. Environmental DNA, 5, 12–17. https://doi.org/10.1002/edn3.363 17 26374943, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1002/edn3.363 by Namibia Hinari NPL, Wiley Online Library on [01/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License von der