An emerging global problem of mass mortalities

Mass mortality events (MMEs) involve the rare, sudden death of large numbers of animals (Fey et al. Reference Fey, Siepielski, Nussle, Cervantes-Yoshida, Hwan and Huber2015). They affect all age groups in a population and so differ from natural events such as seasonal migration (Subalusky et al. Reference Subalusky, Dutton, Rosi and Post2017) or mass emergence events (Yang Reference Yang2004), and they are increasingly attributed to extreme climate- and weather-related phenomena (Seneviratne et al. Reference Seneviratne, Zhang, Adnan, Badi, Dereczynski, Di Luca, Masson-Delmotte, Zhai, Pirani, Connors, Péan and Berger2021) such as droughts, floods or wildfires and cause mortality via heat stress, asphyxiation, disease or starvation (Fey et al. Reference Fey, Siepielski, Nussle, Cervantes-Yoshida, Hwan and Huber2015). In our view, MMEs represent an emerging but overlooked problem that extends beyond species conservation into ecosystem functioning, and our aim in this paper is to highlight the potential of scavenger guilds to be a key nature-based solution to mitigating the effects of MMEs.

In the last decade, many MMEs have occurred across a global range of biomes and animal taxa (Fig. 1), and the proximate causes of death are mostly linked to climate and weather extremes (Table 1). MMEs range in magnitude from a few hundred elephants in Botswana (Wang et al. Reference Wang, Xu, Liu, Jeppesen, Svenning and Wu2021) or reindeer in Norway (Hansen et al. Reference Hansen, Isaksen, Benestad, Kohler, Pedersen and Loe2014) through to many millions of mussels in the English Channel (Seuront et al. Reference Seuront, Nicastro, Zardi and Goberville2019) and perhaps billions of mammals and birds following Australia’s catastrophic megafires in 2019/2020 (Dickman et al. Reference Dickman, Driscoll, Garnett, Keith, Legge and Lindenmayer2020). The resulting quantities of carcass biomass through MMEs are therefore staggering (e.g., 700 million tonnes in a single event; Fey et al. Reference Fey, Siepielski, Nussle, Cervantes-Yoshida, Hwan and Huber2015). As the magnitude of climate variability worsens and extreme weather events increase in frequency and intensity (Field et al. Reference Field, Barros, Stocker, Qin, Dokken, Ebi and Mastrandrea2012, Seneviratne et al. Reference Seneviratne, Zhang, Adnan, Badi, Dereczynski, Di Luca, Masson-Delmotte, Zhai, Pirani, Connors, Péan and Berger2021), the world will probably witness more frequent and severe MMEs (Fey et al. Reference Fey, Siepielski, Nussle, Cervantes-Yoshida, Hwan and Huber2015, Lamberti et al. Reference Lamberti, Levesque, Brueseke, Chaloner and Benbow2020).

Fig. 1. Selected animal mass mortality events (MMEs) showcasing links to extremes in weather that have occurred across multiple biomes and animal taxa, involving hundreds to billions of individuals over periods of days to weeks. Examples are numbered 1–14 with details provided in Table 1.

Table 1. Details of example mass mortality events (MMEs) as illustrated in Fig. 1 and grouped by cause of death and link to climate change.

HAB = harmful algal bloom.

MMEs can affect ecosystem equilibria through rapid and large shifts in numbers of the affected species, but they also cause changes to species interactions and energy flows through food webs (Fey et al. Reference Fey, Gibert and Siepielski2019, Lamberti et al. Reference Lamberti, Levesque, Brueseke, Chaloner and Benbow2020). In nature, background inputs of carrion are continuously provided by countless species of animals across a large body-size spectrum that die from natural causes such as predation and disease (Barton et al. Reference Barton, Evans, Foster, Pechal, Bump, Quaggiotto and Benbow2019a). Regular inputs of animal carcasses are important for maintaining the ecological and evolutionary processes that enhance biodiversity (DeVault et al. Reference DeVault, Rhodes, Olin and Shivik2003, Barton et al. Reference Barton, Cunningham, Lindenmayer and Manning2013, Benbow et al. Reference Benbow, Barton, Ulyshen, Beasley, DeVault and Strickland2019), and they contribute to the dynamics of ecosystem productivity, structure and function through, for example, scavenging by well-adapted species (Wilson & Wolkovich Reference Wilson and Wolkovich2011, Subalusky et al. Reference Subalusky, Dutton, Rosi and Post2017, Barton et al. Reference Barton, Evans, Foster, Pechal, Bump, Quaggiotto and Benbow2019a). But MMEs are a risk to ecological equilibria and human well-being where such events are not the result of millennia of evolution and adaptation (Oro et al. Reference Oro, Genovart, Tavecchia, Fowler and Martínez-Abraín2013, Fey et al. Reference Fey, Siepielski, Nussle, Cervantes-Yoshida, Hwan and Huber2015, Reference Fey, Gibert and Siepielski2019, Lamberti et al. Reference Lamberti, Levesque, Brueseke, Chaloner and Benbow2020) and where scavenging food webs have become severely altered due to landscape modification or direct persecution by humans (Pain et al. Reference Pain, Cunningham, Donald, Duckworth, Houston and Katzner2003, Ogada et al. Reference Ogada, Shaw, Beyers, Buij, Murn and Thiollay2016, Sebastian-Gonzalez et al. Reference Sebastian-Gonzalez, Morales-Reyes, Botella, Naves-Alegre, Perez-Garcia and Mateo-Tomas2020). For example, increasing occurrences of MMEs could lead to nutrient pollution in soils or waterways, subsidies of pest species populations or promote disease transmission among wildlife. Among the most frequently threatened scavengers, vultures and top predators are functionally dominant species that are able to rapidly consume large amounts of carrion in some ecosystems (Supplementary Table S1, available online). Accordingly, their removal from those ecosystems could result in dysfunctional scavenger guilds and lead to longer carcass persistence in landscapes (Cunningham et al. Reference Cunningham, Johnson, Barmuta, Hollings, Woehler and Jones2018, Hill et al. Reference Hill, DeVault, Beasley, Rhodes and Belant2018). This has also been demonstrated in Asia and Africa, where vultures have undergone significant declines (Pain et al. Reference Pain, Cunningham, Donald, Duckworth, Houston and Katzner2003, Sebastian-Gonzalez et al. Reference Sebastian-Gonzalez, Morales-Reyes, Botella, Naves-Alegre, Perez-Garcia and Mateo-Tomas2020). An overlooked but ubiquitous group of scavengers is made up of blowflies (Calliphoridae), which can also contribute significantly to carrion removal (Barton & Evans Reference Barton and Evans2017, Lashley et al. Reference Lashley, Jordan, Tomberlin and Barton2018). The absence of dominant scavenger groups may lead to altered pathways of nutrient flow or elevated risks of disease transmission to wildlife, livestock or people (Ogada et al. Reference Ogada, Torchin, Kinnaird and Ezenwa2012, O’Bryan et al. Reference O’Bryan, Braczkowski, Magalhães and McDonald-Madden2020, Sanderson & Alexander Reference Sanderson and Alexander2020, Barbier Reference Barbier2021, Bloom et al. Reference Bloom, Chan, Baric, Bjorkman, Cobey and Deverman2021). Thus, conserving scavenger communities should be considered as part of the solution to mitigating the effects of MMEs on both ecosystems and human well-being.

Native scavenger guilds as a nature-based solution to mitigating MMEs

Although scavengers cannot prevent MMEs from occurring, they can help buffer ecosystems against the impacts of MMEs on species interactions and nutrient flows through their consumption and dispersal of carrion biomass. A diverse range of scavenger species contribute to carcass consumption and removal from landscapes (Mateo-Tomás et al. Reference Mateo-Tomás, Olea, Moleón, Selva and Sánchez-Zapata2017, Anderson et al. Reference Anderson, Archer, Barton, Wallace, Olea, Mateo-Tomas and Sanchez-Zapata2019, Sebastian-Gonzalez et al. Reference Sebastian-Gonzalez, Morales-Reyes, Botella, Naves-Alegre, Perez-Garcia and Mateo-Tomas2020). Vertebrate scavengers include a range of mammalian, bird and reptile taxa (DeVault et al. Reference DeVault, Rhodes, Olin and Shivik2003, Mateo-Tomás et al. Reference Mateo-Tomás, Olea, Moleón, Vicente, Botella and Selva2015, Selva et al. Reference Selva, Moleon, Sebastián-González, DeVault, Quaggiotto, Bailey, Olea, Mateo-Tomas and Sanchez-Zapata2019), as well as invertebrates such as flies, beetles and ants (Anderson et al. Reference Anderson, Archer, Barton, Wallace, Olea, Mateo-Tomas and Sanchez-Zapata2019, Barton & Bump Reference Barton, Bump, Olea, Mateo-Tomas and Sanchez-Zapata2019). These different taxa combine to form scavenging guilds that are unique to different biogeographical regions, land uses and habitat types (Anderson et al. Reference Anderson, Archer, Barton, Wallace, Olea, Mateo-Tomas and Sanchez-Zapata2019, Beasley et al. Reference Beasley, Olson, Selva, DeVault, Olea, Mateo-Tomas and Sanchez-Zapata2019, Sebastian-Gonzalez et al. Reference Sebastian-Gonzalez, Barbosa, Perez-Garcia, Morales-Reyes, Botella and Olea2019, Selva et al. Reference Selva, Moleon, Sebastián-González, DeVault, Quaggiotto, Bailey, Olea, Mateo-Tomas and Sanchez-Zapata2019). Where data are available for carrion consumption, they show that removal of carcasses can be up to 100% for some scavenger species and groups (Table S1). However, consumption rates are still poorly understood for many taxa and locations, and increasing knowledge in this regard is critical to improving our understanding of the extent to which scavengers can assist with MME mitigation. Consumption capacity (as quantities per unit time or proportions of carcasses visited or biomass consumed) is particularly well known for keystone and native scavengers such as vultures, which dominate carcass consumption in many ecosystems across Asia, Africa and Europe (e.g., Mateo-Tomás et al. Reference Mateo-Tomás, Olea, Moleón, Selva and Sánchez-Zapata2017, Gutierrez-Canovas et al. Reference Gutierrez-Canovas, Moleon, Mateo-Tomas, Olea, Sebastian-Gonzalez and Sanchez-Zapata2020, Buechley et al. Reference Buechley, Murgatroyd, Ruffo, Bishop, Christensen and Marra2022). Large native predators such as eagles, lions, wolves and bears are also able to rapidly consume large quantities of carrion in some African, European and North American ecosystems (Wilmers et al. Reference Wilmers, Stahler, Crabtree, Smith and Getz2003, Mateo-Tomás et al. Reference Mateo-Tomás, Olea, Moleón, Selva and Sánchez-Zapata2017). The contributions of many less dominant species, including ‘meso-scavengers’ such as foxes, corvids and suids, may also be important in some contexts (Beasley et al. Reference Beasley, Olson, Selva, DeVault, Olea, Mateo-Tomas and Sanchez-Zapata2019, O’Bryan et al. Reference O’Bryan, Holden and Watson2019).

Despite the impressive quantity of carrion that many scavengers can consume (Table S1) in a few hours or days (e.g., >15 kg/day for Gyps vultures in Mediterranean and African ecosystems; Mateo-Tomás et al. Reference Mateo-Tomás, Olea, Moleón, Selva and Sánchez-Zapata2017), there could be a threshold over which scavengers will be overwhelmed and cannot assist with the rapid consumption and dispersal of carrion resulting from MMEs without further affecting ecosystem integrity (Oro et al. Reference Oro, Genovart, Tavecchia, Fowler and Martínez-Abraín2013). In these instances, additional intervention (e.g., disposing of carcasses via burial, burning or composting) may be required to reduce the impacts of MMEs on altered species interactions, pest species, nutrient pollution or disease risk. It is important to recognize this limitation, but research is needed to develop our knowledge regarding the ecological functions of scavenger guilds in different ecosystems and their capacity to consume very large and irregular influxes of carrion biomass, as well as other ecological and evolutionary consequences of such consumption (e.g., population and community alterations; Oro et al. Reference Oro, Genovart, Tavecchia, Fowler and Martínez-Abraín2013).

Dominant scavenger species play an important role in the rapid consumption of large quantities of carrion across ecosystems (Mateo-Tomás et al. Reference Mateo-Tomás, Olea, Moleón, Selva and Sánchez-Zapata2017, Buechley et al. Reference Buechley, Murgatroyd, Ruffo, Bishop, Christensen and Marra2022), but it is the combined effect of the entire scavenger guild that often results in the complete recycling of carcass biomass and will be important to their response to MMEs. Research has identified behavioural plasticity among social vultures (black vultures, Coragyps atratus) that resulted in higher consumption rates when presented with larger carrion inputs (Baruzzi et al. Reference Baruzzi, Barton, Cove and Lashley2022). Furthermore, the rapid development times and voracious appetite of blowflies (Calliphoridae; Barton et al. Reference Barton, Evans, Higgins, Strong and Quaggiotto2019b) suggest that they also have the capacity to rapidly colonize and consume excess carrion biomass (Lashley et al. Reference Lashley, Jordan, Tomberlin and Barton2018). Yet scavenger guilds may also include pest or invasive species that opportunistically consume carrion, such as wasps (Vespula germanica) or pigs (Sus scrofa) in south-east Australia (Spencer et al. Reference Spencer, Dickman, Greenville, Crowther, Kutt and Newsome2021), or rats (Rattus sp.) and dogs (Canis familiaris) where vultures (Gyps sp.) have been extirpated in Southeast Asia (Pain et al. Reference Pain, Cunningham, Donald, Duckworth, Houston and Katzner2003). These pest species have been shown to alter species interactions at carcasses or change disease transmission risk, respectively. Thus, although scavenger guilds are a part of the solution to mitigating MMEs through the rapid consumption and dispersal of carrion, consideration must be given to those vertebrate and invertebrate scavengers that are able to maintain ecosystem resilience after climate-driven MMEs.

How can scavengers be incorporated into climate change mitigation strategies?

The UNEP Adaptation Gap Report 2020 (United Nations Environment Programme 2021) stresses the importance of identifying ecosystem-based solutions to mitigating the effects of climate change on people and nature. This should extend to the conservation and management of scavengers and scavenging food webs in order to boost ecosystem resilience to shocks and pressures stemming from MMEs. We suggest that this can be achieved in three ways: (1) improving knowledge of the roles of different vertebrate and invertebrate scavengers as providers of nutrient cycling services across ecosystems; (2) the protection and conservation of extant scavenger species known to be dominant carrion consumers and the reintroduction of locally extinct ones; and (3) planning mitigation actions to assist scavenger communities that are not able to deal with MMEs, particularly in vulnerable ecosystems already experiencing multiple threatening processes (Tulloch et al. Reference Tulloch, Mortelliti, Kay, Florance and Lindenmayer2016).

Globally, there is also a need for greater awareness of MMEs and their link to extreme weather and climate events, as well as raised awareness of scavengers as ecosystem service providers (Mateo-Tomás et al. Reference Mateo-Tomás, Olea, Moleón, Selva and Sánchez-Zapata2017, Olea et al. Reference Olea, Mateo-Tomas and Barton2019). Such knowledge should be integrated into international policies and agreements dealing with climate change, but also with the conservation and management of biodiversity in general and of scavengers in particular (Mateo-Tomas & Olea Reference Mateo-Tomas and Olea2018). For example, the action plan for vultures in Africa and Europe (Botha et al. Reference Botha, Andevski, Bowden, Gudka, Safford, Tavares and Williams2017) highlights the potential impacts of climate change on these species but does not mention vultures as potential key actors for resilient ecosystems through rapid carcass consumption over large areas (Ogada et al. Reference Ogada, Torchin, Kinnaird and Ezenwa2012, Mateo-Tomás et al. Reference Mateo-Tomás, Olea, Moleón, Selva and Sánchez-Zapata2017).

At regional and local scales, conservation management plans should include concrete actions for handling MMEs, acknowledging the key role that scavengers could play as providers of both supporting and regulating ecosystem services in this regard. Assessments of the status and health of ecosystems for adaptation to global change should include the assessment of scavenger biodiversity and the identification of dominant scavenger species, their conservation status and their contribution to carcass removal.

We also emphasize that species conservation is biased towards vertebrates (Clark & May Reference Clark and May2002), but equal emphasis on both vertebrate and invertebrate scavenger guilds (Olea et al. Reference Olea, Mateo-Tomas and Barton2019) should be promoted in conservation policy to encourage resilience to perturbations resulting from MMEs.

In light of the recently started United Nations Decade on Ecosystem Restoration (www.decadeonrestoration.org), conservation actions should also consider reintroductions of previously extirpated scavengers that clearly play a major role in carrion consumption and removal from landscapes. Scavengers should be part of a multi-pronged approach to MME mitigation that combines their conservation with practices such as carcass dispersal or removal when exceeding a threshold quantity. Scavengers may not be a silver bullet to solve all problems associated with MMEs, but it is important to recognize that they are one of the few nature-based solutions available to mitigate the effects of mass mortalities on ecosystems and human well-being.