Fire modulates the effects of introduced ungulates on plant–insect interactions in a Patagonian temperate forest Yamila Sasal, Alejandro Farji-Brener & Estela Raffaele Biological Invasions ISSN 1387-3547 Biol Invasions DOI 10.1007/s10530-017-1455-8 1 23 Your article is protected by copyright and all rights are held exclusively by Springer International Publishing Switzerland. This e- offprint is for personal use only and shall not be self-archived in electronic repositories. If you wish to self-archive your article, please use the accepted manuscript version for posting on your own website. You may further deposit the accepted manuscript version in any repository, provided it is only made publicly available 12 months after official publication or later and provided acknowledgement is given to the original source of publication and a link is inserted to the published article on Springer's website. The link must be accompanied by the following text: "The final publication is available at link.springer.com”. 1 23 Author's personal copy Biol Invasions DOI 10.1007/s10530-017-1455-8 ORIGINAL PAPER Fire modulates the effects of introduced ungulates on plant– insect interactions in a Patagonian temperate forest Yamila Sasal . Alejandro Farji-Brener . Estela Raffaele Received: 12 September 2016 / Accepted: 12 May 2017 Ó Springer International Publishing Switzerland 2017 Abstract Disturbances like biological invasions and seed predation) were unaffected by cattle in both fire may affect in unexpected ways plant-animal forests types. Either, low browsing pressure or induc- interactions. In northwestern Patagonia, introduced tion of plant defences may explain our results. This ungulates (cattle, horses and deers) are widespread and study illustrates how modifications on biotic and very common occupying more than 50% of forests and abiotic conditions produced by fire may affect in shrublands, widely affecting these habitats. In addi- complex ways the effect of introduced ungulates on tion, fire play a major role in creating landscape plant-animal interactions. patterns in this region. We evaluated whether fire modify the impacts of introduced ungulates on plant- Keywords Berberis darwinii Á Cattle Á Patagonian animal interactions. In a mature forest (unburnt) and in forest Á Plant-animal interactions Á Post-fire an early post-fire area (burnt) we used structural equation modeling (SEM) to analyzed the impacts of introduced ungulates on insect herbivory, pollination Introduction and pre-dispersal seed predation on Berberis darwinii, one of the most common understory shrub of temper- Grazing, browsing and trampling by introduced ate forests. We found that the effects of cattle on ungulates are a common component of ecosystems pollination and fruit set depended on the habitat throughout the world (Belsky 1986; Nun˜ez et al. 2010; condition (i.e. unburnt or burnt). Introduced ungulates Va´zquez 2002). These animals modify primary pro- in unburnt forest decreased fruit set through a reduc- ductivity, nutrient cycles, soil properties and fire tion on pollinator visits. Conversely, introduced regimes, which all have an impact on the ecology of ungulates in burnt forest increased pollinator visits other organisms (Hobbs 1996; Stritar et al. 2010; and flower production without affecting fruit set. On Va´zquez and Simberloff 2003). Introduced ungulates the other hand, damage patterns (herbivory and fruit/ might disrupt plant-animal interactions affecting both animals and plants through direct and indirect ways (Rodriguez-Cabal et al. 2013; Rooney and Waller Y. Sasal (&) Á A. Farji-Brener Á E. Raffaele 2003;Va´zquez and Simberloff 2004). On plants, Laboratorio Ecotono, Instituto de Investigaciones en introduced ungulates can directly affect plant growth, Biodiversidad y Medioambiente (INIBIOMA), architecture, chemistry and phenology (Smith et al. Universidad Nacional del Comahue-CONICET, Pasaje 2015) and/or indirectly by modify plant–plant inter- Gutie´rrez 1125, 8400 S. C. de Bariloche, Rı´o Negro, Argentina actions through selective foraging and/or modification e-mail: [email protected] of floral traits (Mothershead and Marquis 2000; Smith 123 Author's personal copy Y. Sasal et al. et al. 2015). On animals, introduced ungulates affect by the late eighteenth century (Jaksic et al. 2002; insects directly by accidental predation (Go´mez and Veblen et al. 1992) and now show high density and Gonza´lez-Megı´as 2002) or nests damage (Go´mez and impact. Currently, introduced ungulates are wide- Gonza´lez-Megı´as 2007; Kearns et al. 1998), and/or spread occupying more than 50% of Patagonian indirectly through removal of food resources (i.e. forests and shrublands (Jaksic 1998; Jaksic et al. leaves, flowers, fruits, seeds) (Bolker et al. 2003;de 2002; Merino et al. 2009; Navas 1987). Introduced Paz and Raffaele 2013; Kearns and Inouye 1997). ungulates have greatly affected the vegetation of the Plant–insect interactions are crucial for maintaining region, preventing regeneration of some tree species, the structure and biodiversity of ecosystems (Fisher shifting dominance towards spiny shrubs, favoring 1998; Traveset and Richardson 2006; Valiente-Banuet exotic plants, and in some circumstances shifting the et al. 2015), but the effects of introduced ungulates on structure of forests from tall trees to shrublands biotic interactions are less documented than those (Martı´n et al. 1985; Piazza et al. 2016; Relva et al. focused on community structure. Despite this, some 2010; Relva and Veblen 1998;Va´zquez 2002; Veblen studies showed relevant impacts, both on plant-animal et al. 1989, 1992). In addition, disturbances like fire, mutualisms (Rodriguez-Cabal et al. 2013;Va´zquez both natural and human-set, had played historically a and Simberloff 2003, 2004), and on antagonistic major role in creating landscape patterns in this region interactions like herbivory (Go´mez and Gonza´lez- along the precipitation gradient from dry steppe to wet Megı´as 2007). Moreover, the sign and magnitude of Andean rain forests (Kitzberger and Veblen 1999; the effect of introduced ungulates on plant-animal Veblen et al. 2003, 2011). Hight severity fire events interactions may depend on the biotic or abiotic created a mosaic of patches of different structure, age context (Chamberlain et al. 2014). and species composition (Mermoz et al. 2005). Some Local biotic and abiotic conditions affect the studies shown that introduced ungulates, particularly abundance, behavior and foraging selectivity of non- cattle, affected post-fire plant regeneration in temper- native species, so the magnitud and even the direction ate forest modifying vegetation structure and compo- of impacts of the same species may differ across sition, retarding plant succession and growth heterogeneous sites (D’Antonio et al. 2000; Kestrup (Blackhall et al. 2008; Raffaele and Veblen 2001; and Ricciardi 2009; Randall and Walters 2011). Raffaele et al. 2011; Tercero-Bucardo et al. 2007) and Episodic disturbance agents, such as fire, interact with facilitating the introduction of non-native species introduce ungulates across time and space (Wisdom (Nun˜ez et al. 2008). Although in this region introduced et al. 2006). In particular, if the disturbance includes ungulates and fire have been present togheter since late directional change such as a shift in abiotic conditions, eighteenth century, their effects on plant-animal the environment may become less hospitable for interaction have been studied separately. natives but not necessary for non-natives, and could The goal of this study was to evaluate whether fire modify the tempo and magnitude of invasive species modify the impacts of introduced ungulates on plant- impacts (Byers 2002; Didham et al. 2007). However, animal interactions, using structural equation model- when and how disturbance acts as modulator of non- ing (SEM). Particularly, we studied cattle browsing native species impacts has been poorly explored effects in a burnt and unburnt areas on insect (Ricciardi et al. 2013). herbivory, pollination and pre-dispersal seed preda- In northwestern Patagonia Argentina, herbivory by tion on Berberis darwinii Hook. (Berberidaceae), an natives animals are less relevant than those produced abundant native understory shrub of Patagonian by non-natives (Iranzo et al. 2013; Merino et al. 2009). temperate forests. Natives ungulates such as huemul (Hippocamelus bisulcus) and pudu pudu (Pudu pudu) are present in low population densities and their impact has always Materials and methods been limited to ecotones zones (Va´zquez 2002). On the other hand, introduced ungulates like cattle (Bos Study area taurus), horses (Equus caballus), red deer (Cervus elaphus), fallow deer (Dama dama), sheep (Ovis We conducted the study in the Andean forest located aries) and goats (Capra hircus) arrived by Europeans on the eastern side of ‘‘Lago Espejo’’, in Nahuel Huapi 123 Author's personal copy Fire modulates the effects of introduced ungulates on plant–insect interactions in a… National Park, Patagonia Argentina (40°380S– areas. The distance between burnt and unburnt study 71°420W; 850 m above sea level). In this region, the areas was of 500 m, and they slightly differed in mean annual temperature is 8 °C and it ranges from a altitude; burnt area was at 890 m a. s. l. and unburnt at minimum of 2 °C (July) to a maximum of 23 °C 840 m a. s. l. Cattle move freely among burnt and (January). Precipitation is concentrated mainly in unburnt sites. autumn and winter as snow with an annual rainfall of 2000