Rock cavity nesting as the norm: Breeding songbirds of the temperate High Andes

Organisms living and breeding in alpine habitats must cope with severe environmental challenges such as temperature extremes, storms, resource limitations and, sometimes, hypoxia, resulting in short windows and reduced opportunities to reproduce (Chamberlain et al., 2023; Martin, 2001; Martin et al., 2017; Martin & Wiebe, 2004). Alpine habitats are defined as the area above the climatic treeline where vegetation growth is limited to cold-tolerant grasses and forbs, low-lying shrubs, or small patches of stunted trees <3 m in height, resulting in less diverse niche space relative to below the treeline (Körner, 2012; Körner et al., 2011). Despite these constraints, as well as limited habitat availability above treeline relative to the total landmass (Nagy & Grabherr, 2009; Testolin et al., 2020), 12% of bird species breed in alpine habitats (de Zwaan et al., 2022a). Globally, our understanding of avian nesting biology is limited, with clutch size and nest structure documented for only 53% and 45% of species, respectively (Reynolds & Deeming, 2015). Additionally, nest descriptions tend to be biased toward low-elevation, Northern Hemisphere communities, with clear knowledge gaps for alpine breeding birds in south-temperate mountains. Here, we describe the nest and breeding traits of songbirds breeding above treeline in the temperate High Andes, many of which previously lacked detailed descriptions. We also provide natural history notes on breeding phenology, parental care, and resource competition to provide a baseline for future studies to build on within these data-deficient communities (Table 1). Finally, we compare the predominance of rock cavity-nesting species above treeline in the temperate Andes with other temperate alpine songbird communities using a global alpine breeding bird dataset (de Zwaan et al., 2022a, 2022b) and generate a hypothesis framework for investigating variation in nest traits among alpine communities. We located and monitored the nests of High-Andean or alpine breeding bird communities in the temperate Andes Tom as A. Altamirano and Devin R. de Zwaan are co-lead authors. Received: 8 July 2022 Revised: 1 September 2022 Accepted: 9 September 2022

Organisms living and breeding in alpine habitats must cope with severe environmental challenges such as temperature extremes, storms, resource limitations and, sometimes, hypoxia, resulting in short windows and reduced opportunities to reproduce (Chamberlain et al., 2023;Martin, 2001;Martin et al., 2017;Martin & Wiebe, 2004). Alpine habitats are defined as the area above the climatic treeline where vegetation growth is limited to cold-tolerant grasses and forbs, low-lying shrubs, or small patches of stunted trees <3 m in height, resulting in less diverse niche space relative to below the treeline (Körner, 2012;Körner et al., 2011). Despite these constraints, as well as limited habitat availability above treeline relative to the total landmass (Nagy & Grabherr, 2009;Testolin et al., 2020), $12% of bird species breed in alpine habitats (de Zwaan et al., 2022a).
Globally, our understanding of avian nesting biology is limited, with clutch size and nest structure documented for only 53% and 45% of species, respectively (Reynolds & Deeming, 2015). Additionally, nest descriptions tend to be biased toward low-elevation, Northern Hemisphere communities, with clear knowledge gaps for alpine breeding birds in south-temperate mountains. Here, we describe the nest and breeding traits of songbirds breeding above treeline in the temperate High Andes, many of which previously lacked detailed descriptions. We also provide natural history notes on breeding phenology, parental care, and resource competition to provide a baseline for future studies to build on within these data-deficient communities (Table 1). Finally, we compare the predominance of rock cavity-nesting species above treeline in the temperate Andes with other temperate alpine songbird communities using a global alpine breeding bird dataset (de Zwaan et al., 2022a(de Zwaan et al., , 2022b and generate a hypothesis framework for investigating variation in nest traits among alpine communities.
We located and monitored the nests of High-Andean or alpine breeding bird communities in the temperate Andes Tom as A. Altamirano and Devin R. de Zwaan are co-lead authors.

Species
Geositta rufipennis occupied the deepest rock cavities of the five focal species (Table 1), such that we were unable to observe the nest contents. This species nested primarily in open rock fields or scree and was one of the earliest species to initiate breeding. Nest materials consisted of down feathers, grass, small twigs, fur, and rootlets. Cinclodes oustaleti, another Furnariid, used narrower cavities in younger volcanic rock (Table 1). Nests were built closer to the entrance, primarily using grass with minimal other materials, including one cigarette. The nests of G. rufipennis and C. oustaleti lacked a defined cup structure, resembling a loosely assembled platform.
Muscisaxicola maclovianus, a Tyranid ground-tyrant, placed their nests mainly above rivers or streams in rock crevices (Table 1). Due to accessibility issues, we were unable to record all breeding parameters for M. maclovianus, but they used feathers and fur to insulate nests. Muscisaxicola albilora also nested in cliff crevices but was not associated with water (Table 1). Their nests consisted primarily of grass and rootlet cups lined with feathers. Despite being sister species, M. maclovianus and M. albilora appeared to have partitioned their nesting habitat niche, as both species were observed nesting or feeding frequently in the same general area, but never in close proximity.
Pygochelidon cyanoleuca nested in rock cavities with dimensions that varied widely among individuals relative to the other species (except perhaps G. rufipennis; Table 1), potentially indicating less reliance on a specific cavity shape. Nest cups consisted of broad-leaved grasses or sedges, with limited instances of feathers or rootlets and, in two cases, toilet paper. This species was the most colonial, with large numbers nesting in the same rock face.
We recorded multiple instances of interspecific competition at nest sites. Specifically, M. albilora was highly aggressive toward P. cyanoleuca, nesting in similar sites despite frequent territorial disputes, with aggressive exclusion behavior between species near rock cavity entrances. In contrast, M. maclovianus was tolerant of P. cyanoleuca and often co-associated in semicolonial aggregations. Less frequently, we observed competitive interactions between M. albilora and Melanodera xanthogramma (yellow-bridled finch), and between M. maclovianus and G. rufipennis. This behavior may suggest that rock cavities are a limiting factor for High-Andean bird populations, similar to tree cavity-nesting birds (Cockle et al., 2010). In the Italian Alps, similar competition for rock and artificial cavities (i.e., snowfinch nest boxes, ski lift pylons, buildings) has been documented among Montifringilla nivalis (white-winged snowfinch), Phoenicurus ochruros (black redstart), and Motacilla alba (white wagtail; Brambilla et al., 2019). Here, cavities experience within-season interspecific reuse (i.e., between early and late broods), as well as species turnover in occupancy across years. In contrast, despite evidence of competition, we did not observe cavity takeover or interspecific reuse in the High-Andean community. Another potential limiting resource is insulative nesting materials, which can improve nest success in alpine habitats (de Zwaan & Martin, 2018). We observed both Leptastenura aegithaloides (plain-mantled tit-spinetail) and G. rufipennis taking nesting material from an active C. oustaleti nest. Nest material kleptoparasitism is rarely reported outside of colonial-nesting species (Slager et al., 2012), and never before at high elevations.
At the microhabitat scale, all species nested in proximity to vegetation, predominantly Gaultheria pumila (closest for all species), Berberis empetrifolia, Cardamine chilensis, Chiliotrichum diffusum, Empetrum rubrum, Maytenus disticha, ferns, and grasses. Breeding success was relatively high across species but varied considerably (60%-100%; Table 1). Other than clutch size and provisioning rate, parental behaviors such as incubation recesses and food provisioned varied among species, potentially reflecting differences in phenology (i.e., peak in November or December) and the stage of offspring development (Table 1). Ample opportunities exist for future research to address variation in cavity dimensions, plant associations, and parental behaviors within and among species to investigate potential consequences for reproductive success.
Using a global dataset of alpine breeding birds (de Zwaan et al., 2022a(de Zwaan et al., , 2022b, we found that the proportion of passerines nesting in rock cavities was greater in the southern Andes (this study site; 54%; 13 of 24 species) than in other major temperate alpine communities globally (excluding species that breed above treeline rarely or incidentally). In the southern ranges of Europe (e.g., Alps, Pyrenees, Carpathians), 39% (12 of 31) of alpine breeding passerines nest in rock cavities, compared with 24% (9 of 38) in the coastal and Rocky Mountains of North America, and 22% (26 of 117) on the Qinghai-Tibetan Plateau. In the New Zealand Alps, which occur at a similar latitude to the temperate Andes, only one of four (25%) alpine passerine species nest in rock cavities.
The alpine breeding bird community in the southern Andes consists of ecologically and evolutionarily distinct species relative to lower elevations and other alpine communities globally (Altamirano et al., 2020;Martin et al., 2021). The underlying factors that drive the predominance of rock cavity-nesting behavior in alpine breeding birds of the temperate Andes is an intriguing question that could yield insights into the evolution and maintenance of life-history strategies in these rapidly changing environments (de Zwaan, Barras, et al., 2022). Here, we outline several nonmutually exclusive hypotheses that may explain the particularly high proportion of rock cavity nesters in the temperate Andes.
1. Evolutionary history. Avian communities above and below the treeline are more similar phylogenetically, or more closely related, in the temperate Andes than in the north temperate mountains of the Americas (Martin et al., 2021). Much of this similarity is driven by speciose families like Tyrannidae, which underwent rapid diversification relatively recently ($6 mya), about the same time as the Andes completed their uplift (Fjeldså et al., 2018). Given the high proportion of tree cavity-nesting birds below the treeline in the region (57%; 29 species; Altamirano et al., 2017), it is plausible that cavity-nesting species radiated into alpine habitats during a period of rapid niche diversification (Martin et al., 2021). 2. Cavity availability and snow dynamics. Temperate alpine habitats are strongly seasonal, with deep snow cover during winter (Nagy & Grabherr, 2009). In the southern Andes, rock ridges and outcrops are common due to recent and continuing volcanic activity, together with fluvial and glacial erosion. Rock substrates are the first to be exposed in spring as solar radiation warms the rock under the snow, contributing to faster snowmelt. Thus, in addition to potentially greater availability of rock cavities than in other temperate alpine habitats, rock cavities are also available earlier than the surrounding substrate, and thus may be more likely to be selected as a nesting resource especially given the short breeding seasons at high elevations (Altamirano et al., 2015). 3. Exposure to severe conditions. During the breeding season, relative humidity is low ($20%), temperatures are extreme and can fluctuate widely , and solar radiation is particularly strong in the High Andes (L opez-Angulo et al., 2020). Dehydration can be detrimental to egg viability, and UV-B radiation can damage developing embryos (Lahti & Ardia, 2016). Rock cavity nests may offer more benign microclimates to raise offspring, retaining greater levels of humidity, more consistent temperatures, and reducing UV-B incidence compared with exposed alpine nests (Potapov, 2004). 4. Predation risk. Nest predation is often high in passerines and can be a strong selective force. While there is little information on nest predation rates in alpine habitats, particularly in the Southern Hemisphere, raptors and mammalian carnivores are the main predators above the treeline in the temperate Andes, with birds making up $9%-17% of the diet of High-Andean canids and felids (Walker et al., 2007;Zúñiga et al., 2020). Most of these mesopredators cannot access subterranean nests, potentially driving selection for rock cavity nests. Interestingly, however, for two nests (C. oustaleti and P. cyanoleuca), we observed ants preying upon early-stage nestlings and potentially causing nest failure, suggesting other possible predation pressures in this system.
Temperate mountains and alpine habitats represent 5.5% and 2.6% of the global landmass excluding Antarctica and Greenland, respectively (Nagy & Grabherr, 2009;Testolin et al., 2020). These relatively small, isolated habitats and their associated biodiversity are also threatened by a rapidly warming climate and the potential for extirpation resulting from upslope, climate-driven range shifts (Freeman et al., 2018;Scridel et al., 2018). We highlight the unique breeding biology of alpine passerines in the temperate Andes, underlining the importance of documenting basic nest traits and breeding parameters for data-deficient and climate-sensitive communities. Improving our knowledge of life-history traits for these species is a prerequisite to understanding species resilience and the future of populations under climate change.