Ben‑David et al. BMC Ecol (2019) 19:52 https://doi.org/10.1186/s12898‑019‑0270‑8 BMC Ecology RESEARCH ARTICLE Open Access Increased songbird nest depredation due to Aleppo pine (Pinus halepensis) encroachment in Mediterranean shrubland Asaf Ben‑David1,2† , Hila Shamon2,3*†, Ido Izhaki4, Ronny Efronny1, Roi Maor1,5 and Tamar Dayan1,2 Abstract Background: In recent decades, a decrease of passerine densities was documented in Mediterranean shrublands. At the same time, a widespread encroachment of Aleppo pines (Pinus halepensis) to Mediterranean shrubland occurred. Such changes in vegetation structure may afect passerine predator assemblage and densities, and in turn impact passerine densities. Depredation during the nesting season is an important factor to infuence passerine population size. Understanding the efects of changes in vegetation structure (pine encroachment) on passerine nesting success is the main objective of this study. We do so by assessing the efects of Aleppo pine encroachment on Sardinian war‑ bler (Sylvia melanocephala) nest depredation in Mediterranean shrublands. We examined direct and indirect predation pressures through a gradients of pine density, using four methods: (1) placing dummy nests; (2) acoustic monitoring of mobbing events; (3) direct observations on nest predation using cameras; and (4) observation of Eurasian jay (Gar- rulus glandarius) behaviour as indirect evidence of predation risk. Results: We found that Aleppo pine encroachment to Mediterranean shrublands increased nest predation by Eura‑ sian jays. Nest predation was highest in mixed shrubland and pines. These areas are suitable for warblers but had high occurrence rate of Eurasian jays. Conclusions: Encroaching pines directly increase activity of Eurasian jays in shrubland habitats, which reduced the nesting success of Sardinian warblers. These fndings are supported by multiple methodologies, illustrating diferent predation pressures along a gradient of pine densities in natural shrublands. Management of Aleppo pine seedlings and removal of unwanted trees in natural shrubland might mitigate arrival and expansion of predators and decrease the predation pressure on passerine nests. Keywords: Nest predation, Acoustic monitoring, Pine encroachment, Sylvia melanocephala, Garrulus glandarius Background for the majority of biological invasions worldwide and Alteration of natural habitat due to anthropogenic activi- have tremendously impacted ecosystems [3]. Plant inva- ties is the leading cause of biodiversity loss in terrestrial sion changes habitat cover and structure, creating bot- habitats [1]. Globalization has promoted alien species tom-up cascading events with adverse efects on native invasion to many parts of the world, thus threatening species [4]. Encroachment is a form of biological inva- human livelihood and biodiversity [2]. Plants constitute sion, whereby native species spread to habitats from which they were historically absent. In some cases, encroachment of native species to non- *Correspondence: [email protected] native habitats are a consequence of human actions † Asaf Ben David and Hila Shamon—frst authorship or managements. For example, native conifer species 3 Smithsonian Conservation Biology Institute, National Zoological Park, Front Royal, VA, USA encroachment to grassland, savannas and shrublands are Full list of author information is available at the end of the article a well-documented phenomenon across the globe [5]. In © The Author(s) 2019. 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The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Ben‑David et al. BMC Ecol (2019) 19:52 Page 2 of 12 north America it is mainly attributed to lack of fre events [32, 33], as well as for nest predators; edges allow nest due to human intervention, allowing conifers to expand predators to forage in habitats other than their primary and establish in low vegetation habitats [6–8]. Conifer natural habitat (i.e., forest species forage in shrubland on encroachment changes both biotic and abiotic conditions forest edge). Increased nest predation is highly associ- in soils, native vegetation composition, diversity and den- ated to edges of fragmented habitats [34], and is higher in sities of primary and secondary consumers [9–11]. clear edges like forest to agriculture. Aleppo pine (Pinus halepensis), is a widespread spe- Tere are several main predators of songbird nests in cies in Mediterranean forests [12], but in the Mediterra- forested areas and shrublands. Small mammals (e.g. mice, nean region of Israel, native populations inhabit relatively rats) were found to be signifcant nest predators in forest small and restricted areas on Mt. Carmel and the Judean habitats due to lower parental activity around the nest mountains [13]. Aleppo pines were planted in the early in such habitats [35], as predatory bird species are more twentieth century across Israel on over 100,000 ha, and associated with forest edges [36]. We hypothesized that account for half of the planted forests in the state. Since avian predators will take advantage of spreading pines to then, a widespread encroachment of Aleppo pines into natural shrublands in our study area. natural habitats has been observed across Israel [14], Lahti [37] suggested that nest predation probability can mostly into Mediterranean shrublands [15]. Whether be determined by specifc predator behavior [37]. Mem- Aleppo pine is now an invasive- or encroaching species in bers of the Corvidae family are known for their learning this region is still debated [14, 16, 17]; we take a conserv- abilities and adaptive and opportunistic skills; therefore, ative approach and consider it encroaching, following these species are known to take advantage of forest edges Osem et al. [15]. Planted Aleppo pines produce seeds for to prey in low vegetation habitats [38, 39]. Long term approximately 30 years in the Mediterranean landscapes monitoring through biennial bird surveys (by sound in Israel [15], and therefore, their impact on the foral and and vision along fxed transects) has been ongoing since faunal structure is expected to continue. Hence, under- 1985 [18]. Tese surveys of the study area have shown an standing the cascading efects of such changes is signif- increase in Eurasian jay density and have led to our cur- cant for understanding changes in the Mediterranean rent study. Pine encroachment to natural habitats may ecosystem of Israel. increase edge efects thus promoting increased presence Birds are considered sensitive to habitat change due of avian predators, such as jays in the study area. Con- to their specifc adaptations to vegetation types, heights current with an increase of jay density, long term surveys and densities [18, 19], and therefore they can be used as show a decrease in songbird nests. Here, we investigate indicators of ecosystem intactness. Changes in vegeta- nest predation pressure rates over a gradient of pine den- tion structure may afect species’ ability to seek shelter sities with diferent vegetation composition and height. or cover from threats such as predators [20]. We stud- Specifcally, we address the following questions: (1) is ied the efects of pine encroachment in natural habitats there a correlation between songbird open nest predation on the presence of the Eurasian jay (Garrulus glandarius and (a) pine density, (b) vegetation structure (c) predator atricapillus), a common songbird nest predator [21, 22], community assemblage; (2) is there a correlation between and the indirect efect of pine encroachment on Sardin- nest predation pressure and presence and activity of jays. ian warbler (Sylvia melanocephala) nest predation. We hypothesized that avian predators such as the Eurasian Results jay may use pines as observation points to detect nests Egg predation in artifcial nests and that consequently pine encroachment will increase Over half of the 123 artifcial nests (quail (Coturnix predation pressure. coturnix) and plaster eggs were pooled) were predated on Te breeding season is a critical phase in the annual life (65 nests, 52.8%). Te probability of nest predation was cycle of birds, with important consequences to popula- not equal among the four habitat types. Greatest preda- tion growth and survival [23–26]. Nest predation rates tion (19.5%) was recorded in the mixed shrubland and usually vary between 44% and 86% depending on habi- low-density pines and the lowest (7.3%) in dense pine tat type and species [27]; vegetation structure (i.e., micro plantations (Fig. 1). habitat) is a signifcant factor that may afect nest preda- tion [28–30]. Nest predator identifcation Pine encroachment to Mediterranean shrublands may Based on the 48 plaster eggs that we placed in artifcial have a similar efect to that of forest edges; edge efect is nests, we were able to identify four predator taxa accord- an ecological change that afects the community struc- ing to marks left on 18 plaster eggs, (Fig. 2). Te main ture in the boundaries of the habitat [31]. Forest edges predator group was medium size mammals (n = 8), fol- can change resource availability for insectivorous birds lowed by rodents (n = 7), birds (n = 2) and reptiles (n = 1) Ben‑David et al. BMC Ecol (2019) 19:52 Page 3 of 12 Fig.