Ungulates and ecosystem services in Mediterranean woody systems: A semi-quantitative review

Highlights

• Supporting (mainly biodiversity and fire prevention) was the main positive service.

• Cultural and regulatory services are typically overlooked (<10 % of all studies).

• Disservices (mainly vegetation conservation) were reported in 32.82 % of studies.

• Tolerance to ungulate pressure rises from shrublands, through forests, to woodlands.

• Managers should try to maximize services and minimize disservices.

Abstract

Ungulates are key elements that modulate the type and direction of ecosystem services in Mediterranean environments. Our main objective is to synthesize the provision of ecosystem services in forests, shrublands and woodlands dominated by ungulates (wildlife or livestock) in Mediterranean environments. To achieve this objective, we performed a systematic semi-quantitative review (n = 262 studies) across the Mediterranean climate area for the 1991−2018 period.

Most studies focused on supporting services (80.35 % of all studies), with biodiversity (49.11 %) and plant recruitment (18.15 %) as the most studied services. A great number of studies addressed plant biodiversity preservation (63.40 % of studies on biodiversity). Surprisingly, we found a low number of studies on cultural (7.02 %) and regulatory (5.26 %) services.

Regarding the direction of the relationship of ungulate effects on ecosystem services, 67 studies (25.57 %) showed positive effects and 86 studies (32.82 %) mentioned negative effects (disservices). Most studies that showed positive effects focused on biodiversity, mainly vegetation and birds, and wildfire prevention. However, most studies reporting negative effects were also based on biodiversity loss (mainly vegetation) and plant recruitment failure. Distribution of services remained similar across regions and species but positive effects of ungulates were reported mainly in shrublands and negative effects were reported primarily in forests and woodlands.

Despite the fact that ungulate density is key to explain the direction of ungulate effects on ecosystem services, only 9.51 % of all studies considered different estimates of herbivore pressure and just 7.22 % of all studies considered different contrasted densities in the analysis. Overall, our analysis of services showed a decreasing tolerance to ungulate pressure from woodlands, through forests, to shrublands. Mean ± SE ungulate densities (Livestock Units per ha) in studies that showed negative effects were 0.20 ± 0.01 in shrublands, 0.22 ± 0.01 in forests, and 1.98 ± 1.70 in woodlands (including dehesas, montados and rangelands). Management in Mediterranean woody ecosystems should focus on neglected services (e.g. regulatory services) and try to adjust ungulate population densities to maximize positive effects and minimize negative effects on ecosystem services.

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.