Ungulates and ecosystem services in Mediterranean woody systems: A semi-quantitative review
Introduction
The five Mediterranean regions are global hotspots for biodiversity (Myers, Mittermeier, Mittermeier, Fonseca, & Kent, 2000; Underwood, Viers, Klausmeyer, Cox, & Shaw, 2009), tightly linked to human activity. Human use of Mediterranean ecosystems shaped the present landscapes through vegetation clearing, use of fire and grazing (Blondel, 2006; Camarero, Sangüesa-Barreda, Montiel-Molina, Seijo, & López-Sáez, 2018). In particular, grazing regimes have changed in several regions over the last decades, from livestock grazing, to both domestic and wild ungulate grazing or even wild ungulate grazing solely (Olea & San Miguel-Ayanz, 2006; San Miguel-Ayanz, García-Calvo, & García-Olalla, 2010). Currently, in different regions of the Mediterranean Basin, grazing with domestic animals coexists with grazing and browsing by wild ungulates.
Mediterranean ecosystems dominated by trees or shrubs (woody ecosystems) consist of forests, shrublands and woodlands (Mediterranean savannas with scattered trees and a continuous herbaceous layer, Marañón, Pugnaire, & Callaway, 2009). These woody ecosystems are widespread in the Mediterranean landscapes, as they increasingly cover larger areas following agricultural abandonment and rural exodus (Debussche & Lepart, 1992; Rolo & Moreno, 2019). They are also typically grazed and browsed by large ungulate herbivores, either domestic or wild, which behave mostly as opportunistic mixed-feeders (Papanastasis, Yiakoulaki, Decandia, & Dini-Papanastasi, 2008; Rogosic, Pfister, Provenza, & Grbesa, 2006; San Miguel, Roig, & Perea, 2016) that affect ecosystem processes and their associated services (Beschta et al., 2013). However, the effects of herbivores on ecosystem services are far from clear in the highly diverse Mediterranean regions.
Ungulates modify plant species composition and habitat structure (Gill & Fuller, 2007; Ramirez, Jansen, & Poorter, 2018; Rooney, 2009), affect ecosystem functioning (Beguin, Tremblay, Thiffault, Pothier, & Côté, 2016; Gordon, Hester, & Festa-Bianchet, 2004; Putman, Edwards, Mann, How, & Hill, 1989; Royo, Collins, Adams, Kirschbaum, & Carson, 2010) and therefore ecosystem services (Lecomte et al., 2019). “Regulating services” (sensu Millennium Ecosystem Assessment, 2005) such as carbon storage and sequestration (Bugalho, Caldeira, Pereira, Aronson, & Pausas, 2011; Bugalho, Lecomte, Caldeira, & Branco, 2011; Daryanto, Bojie, Wenwu, & Lixin, 2019), “supporting services” such as biodiversity conservation (Pereira et al., 2007), or “cultural services” such as recreation (Bugalho, Pinto-Correia, & Pulido, 2018), are valuable services for human well-being that may be affected by ungulates. Considering the ecosystem service concept may provide useful insights for better decision-making in natural resource management of systems that include ungulates (Fisher, Turner, & Morling, 2009; Nelson et al., 2009).
Plant-ungulate interactions may strongly affect multiple ecosystems services. Through browsing and rubbing, ungulates alter plant recruitment (Beguin et al., 2016; Stokely & Betts, 2019) and through grazing, trampling, grubbing, debarking or rubbing ungulates modify supporting services, such as seed dispersal (Gill & Beardall, 2001; Manzano & Malo, 2006) or nutrient cycling (Mohr, Cohnstaedt, & Topp, 2005). Furthermore, browsing and grazing affect regulatory services, for instance, by reducing above-ground and below-ground carbon stocks in the short term (Lecomte et al., 2019; Tanentzap & Coomes, 2012) or by altering plant-pollinator interactions (Gómez, 2003; Vázquez & Simberloff, 2003). In this sense, ungulates also affect provisioning services, as moderate grazing has proved to increase forage production in arid rangelands (Oñatibia, Aguiar, & Semmartin, 2015). Additionally, cultural services may increase by the mere presence of ungulate populations, for instance, by attracting wildlife tourism (Arbieu, Grünewald, Martín-López, Schleuning, & Böhning-Gaese, 2017; Murdoch, Reading, Amgalanbaatar, Wingard, & Lkhagvasuren, 2017).
The effects of ungulates on woody ecosystems services depend on animal and plant factors. Herbivore foraging traits or plant species composition and structure (Augustine & McNaughton, 1998; Gómez, Hódar, Zamora, Castro, & García, 2001) influence the way ungulates affect services provided by a certain ecosystem. Effects on ecosystem services may strongly depend on ungulate density (Kéfi et al., 2007; Massei et al., 2015; Perea, Girardello, & San Miguel, 2014). Management of ungulate populations (Gordon et al., 2004) and their habitats (Löf et al., 2016) may imply different ecosystem synergies or trade-offs. For instance, livestock management promoting habitat heterogeneity may increase habitat suitability for bird species (Derner, Lauenroth, Stapp, & Augustine, 2009) and reduction of phytovolume by ungulates may reduce wildfire risk (Velamazán, San Miguel, Escribano, & Perea, 2018) therefore contributing both to biodiversity and wildfire prevention. However, trade-offs may occur between aboveground carbon storage and wildfire hazard (Lecomte et al., 2019) or between plant diversity and wildfire hazard (Silva et al., 2019).
Our main objective is to synthesize the type of ecosystem services affected positively or negatively by domestic and wild ungulates in Mediterranean shrublands, woodlands and forests, here named as woody ecosystems. To achieve this objective, we performed a systematic semi-quantitative review across regions with Mediterranean climate. We performed the literature research for the period between 1991 and 2018. Our general aim was to gain insight on how Mediterranean woody ecosystems and their services may respond to ungulate populations and their management. We specifically aimed to: 1) Quantify the number of studies with domestic vs. wild ungulates (livestock vs. wildlife) per region and ungulate species along the study period; 2) Identify the main ecosystem services (supporting, provisioning, regulatory or cultural) of woody systems (woodlands, shrublands and forests) mediated by ungulate herbivores, and 3) Establish a relationship between ungulate density and ecosystem services in each type of woody ecosystem.
Section snippets
Material and methods
We performed a systematic literature review following previous methodological proposals (Bernes et al., 2016; Moher et al., 2015) and former reviews on ungulate species and their habitats (Herrero-Jáuregui & Oesterheld, 2018; Tanentzap & Coomes, 2012). We searched the Web of Science (no restriction) and Google Scholar (first 200 based on relevance) without language or document type restriction, but rejected book chapters and non-English papers to avoid repetitions. We followed a three-step
Results
The final database (Table S1) after selecting by title, abstract and full text is comprised of 262 studies. Supporting services were the main type of study services: 229 studies (80.5 %), followed by provisioning services (21 studies; 7.37 %), cultural services (20 studies; 7.02 %) and regulatory services (15 studies; 5.26 %).
The most studied supporting services were biodiversity and plant recruitment, followed by soil properties and wildfire prevention (Fig. 1). The majority of published
Discussion
Our results synthesized research on ecosystem services affected positively or negatively by ungulates in Mediterranean woody ecosystems across the globe. Ungulate populations and their management are key aspects in Mediterranean regions, namely when maintaining disturbance-dependent habitats (Navarro & Pereira, 2015). This is even more relevant under the current context of land abandonment and shrub encroachment in Mediterranean areas (Plieninger, Hui, Gaertner, & Huntsinger, 2014), which
Declaration of Competing Interest
All authors have participated in (a) conception and design, or analysis and interpretation of the data; (b) drafting the article or revising it critically for important intellectual content; and (c) approval of the final version.
This manuscript has not been submitted to, nor is under review at, another journal or other publishing venue.
The authors have no affiliation with any organization with a direct or indirect financial interest in the subject matter discussed in the manuscript
There are no
Acknowledgments
This work was funded by European Union FEDER funds through the Operational Programme for Competitiveness Factors—COMPETE (POCI- 01-0145-FEDER-006821) and by Portugal National Funds through FCT (UID/BIA/50027/2019) and FCT Principal Investigator (MNB) research contract (IF01171/2014) . Universidad Politécnica de Madrid (Spain) provided financial support (Programa Propio de Investigación for young researchers; PINV-18-VDKFL-85-8WYEDL).
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2021, Science of the Total EnvironmentCitation Excerpt :The Artiodactyla order is represented by 10 families and 380 species (Fennessy et al., 2016; Wilson and Mittermeier, 2011). Humans around the world have historically interacted with wild ungulates since they were scavenged, hunted and later domesticated (see Moleón et al., 2014), and societies have benefited from them by the many NCP they provide (see e.g. Pascual-Rico et al., 2020; Velamazán et al., 2020). Besides being a source of food and materials, such as bushmeat, leather and bones, some human groups are linked with wild ungulates through cultural aspects; for instance, some Sahelo-Saharan clans have totemic species like dama gazelle (Nanger dama), and Barbary sheep (Ammotragus lervia) (Tubiana, 2005).
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2021, Global Ecology and ConservationCitation Excerpt :However, both abundance and size seemed not so relevant in our case, as cattle dispersed only one plant species (wild pear) and despite the higher number of seeds per feces, a consequence of their larger size and capacity of ingesting more fruits, the seed rain density did not differ from red fox, pine martens and wildboars (Table 2, Fig. 4b). Cattle has been reported to act as seed disperser (Malo et al., 2000; Miguel et al., 2018), but regardless of their almost ubiquitous presence in many anthropogenic mosaics around the world, the seed dispersal role of domestic animals in general still poorly investigated, and those few studies available show contrasting results (Velamazán et al., 2020). For example, the only study we found that compared seed dispersal services by birds, domestic (sheep) and wild animals indicated a very low contribution of sheep to seed dispersal, although this study analyzed just one fleshy-fruited species (Escribano-Avila et al., 2012).