diversity Article Predicting the Future Distribution of Ara rubrogenys, an Endemic Endangered Bird Species of the Andes, Taking into Account Trophic Interactions Alain Hambuckers 1,* , Simon de Harenne 1,2 , Eberth Rocha Ledezma 3, Lilian Zúñiga Zeballos 1,4 and Louis François 2 1 Behavioural Biology Lab, Unit of Research SPHERES, University of Liège, Quai Van Beneden 22, , [email protected] (S.d.H.); [email protected] (L.Z.Z.) 2 Modelling of Climate and Biogeochemical Cycles, Unit of Research SPHERES, University of Liège, Sart Tilman, 4000 Liège, Belgium; [email protected] 3 Centro de Biodiversidad y Genética, Facultad de Ciencas y Tecnología, Universidad Mayor de San Simón, Cochabamba, Bolivia; [email protected] 4 Museo de Historia Natural Alcide d’Orbigny, Cochabamba, Bolivia * Correspondence: [email protected] Abstract: Species distribution models (SDMs) are commonly used with climate only to predict animal distribution changes. This approach however neglects the evolution of other components of the niche, like food resource availability. SDMs are also commonly used with plants. This also suffers limitations, notably an inability to capture the fertilizing effect of the rising CO2 concentration strengthening resilience to water stress. Alternatively, process-based dynamic vegetation models (DVMs) respond to CO2 concentration. To test the impact of the plant modelling method to model Citation: Hambuckers, A.; de plant resources of animals, we studied the distribution of a Bolivian macaw, assuming that, under Harenne, S.; Rocha Ledezma, E.; future climate, DVMs produce more conservative results than SDMs. We modelled the bird with an Zúñiga Zeballos, L.; François, L. Predicting the Future Distribution of SDM driven by climate. For the plant, we used SDMs or a DVM. Under future climates, the macaw Ara rubrogenys, an Endemic SDM showed increased probabilities of presence over the area of distribution and connected range Endangered Bird Species of the extensions. For plants, SDMs did not forecast overall response. By contrast, the DVM produced Andes, Taking into Account Trophic increases of productivity, occupancy and diversity, also towards higher altitudes. The results offered Interactions. Diversity 2021, 13, 94. positive perspectives for the macaw, more optimistic with the DVM than with the SDMs, than initially https://doi.org/10.3390/d13020094 assumed. Nevertheless, major common threats remain, challenging the short-term survival of the macaw. Academic Editor: Miguel Ferrer Keywords: red-fronted macaw; Andes; dynamic vegetation model; biotic interactions; climate Received: 22 January 2021 change; RCP2.6; RCP8.5 Accepted: 18 February 2021 Published: 21 February 2021 Publisher’s Note: MDPI stays neutral 1. Introduction with regard to jurisdictional claims in published maps and institutional affil- The problems of habitat destruction and climate change are the main threat to tropical iations. mountain birds. Mountain bird species in the tropics are particularly at risk because they are isolated by hotter lowland zones which often makes them sedentary. In addition, when shifting their distribution up to higher altitudes, the new area of occupancy narrows [1]. The structure of the mountains itself also appears to be a constraining factor limiting the distribution shift with possible decline of habitat quality, for instance, the absence of Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. suitable nesting sites or even vertical gaps between actual and potential future areas of This article is an open access article distribution [2]. distributed under the terms and The slopes of the Andes are recognized as supporting the highest avian diversity conditions of the Creative Commons in the world combined with high endemism rate but also more than 20% of threatened Attribution (CC BY) license (https:// species [3]. In Bolivia, the red-fronted macaw (Ara rubrogenys Lafresnaye, 1847) is one of creativecommons.org/licenses/by/ the 15 endemic species of this country [4]. Less than 30 years ago, A. rubrogenys was a 4.0/). little-known species [5]. It lives on the east Andean slopes of south-central Bolivia from Diversity 2021, 13, 94. https://doi.org/10.3390/d13020094 https://www.mdpi.com/journal/diversity Diversity 2021, 13, 94 2 of 20 Diversity 2021, 13, 94 2 of 20 known species [5]. It lives on the east Andean slopes of south‐central Bolivia from 553 m 553up mto up3094 to m 3094 a.s.l. m (Figure a.s.l. (Figure 1) and1) breeds and breeds between between 1188 and 1188 2696 and m 2696 [6]. m Its [ 6natural]. Its natural habitat habitatis mainly is mainly semi‐deciduous semi-deciduous dry forest dry but forest this but is most this isoften most severely often severely degraded degraded by pastoral by ‐ pastoralism and by timber extraction into thorny scrubs with scattered trees [7]. While it ism and by timber extraction into thorny scrubs with scattered trees [7]. While it was esti‐ was estimated that the threats were of limited extent in the early nineties [8], the status mated that the threats were of limited extent in the early nineties [8], the status of the of the species worsens over the course of time with land conversion for agriculture, with species worsens over the course of time with land conversion for agriculture, with poach‐ poaching for illegal trade, with killing by farmers who consider them a pest and with ing for illegal trade, with killing by farmers who consider them a pest and with poisoning poisoning with pesticides when they feed on the crops [6,9–11]. The small breeding with pesticides when they feed on the crops [6,9–11]. The small breeding population (only population (only 67 to 136 pairs) in eight close areas was also pointed out as major risk 67 to 136 pairs) in eight close areas was also pointed out as major risk which increases which increases their extinction risk due to correlated environmental fluctuations [6]. It their extinction risk due to correlated environmental fluctuations [6]. It was found that the was found that the birds use agriculture-scrub ecotones more than the forests for foraging, birds use agriculture‐scrub ecotones more than the forests for foraging, probably because probably because the forests do not offer enough resources. A. rubrogenys is now ranked as the forests do not offer enough resources. A. rubrogenys is now ranked as “Critically En‐ “Critically Endangered” in Bolivia [11] and on the International Union for Conservation dangered” in Bolivia [11] and on the International Union for Conservation of Nature Red of Nature Red list [12]. In addition, it could be particularly threatened by climate change. Inlist its [12]. area In of addition, distribution, it couldA. rubrogenys be particularlyuses only threatened terrains alongby climate river change. valleys forIn its roosting, area of feeding,distribution, resting A. and rubrogenys nesting uses [9]. Most only ofterrains the nesting along sites river are valleys located for in roosting, steep river feeding, cliffs butrest‐ suching and environments nesting [9]. are Most not of necessarily the nesting available sites are atlocated higher in altitudes steep river given cliffs the but magnitude such envi‐ ofronments warming are predictions. not necessarily Climate available change at ishigher supposed altitudes to particularly given the magnitude affect the of tropical warm‐ Andesing predictions. and notably Climate Bolivia change [13]; while is supposed warming to already particularly averaged affect 0.1 the◦C/decade tropical Andes between and 1939notably and 1998,Bolivia it accelerated[13]; while warming to 0.33 ◦C/decade already averaged between 0.1 1980 °C/decade and 2005. between Climate 1939 change and scenarios1998, it accelerated suggest warming to 0.33 as°C/decade high as 7.5 between◦C by 20801980 andand important2005. Climate modifications change scenarios of the precipitationsuggest warming regime as with high respect as 7.5 °C to pre-industrialby 2080 and important times. modifications of the precipita‐ tion regime with respect to pre‐industrial times. FigureFigure 1. 1.Distribution Distribution areaarea (alpha(alpha hull) in Bolivia of AraAra rubrogenys rubrogenys atat altitudes altitudes with with occurrences. occurrences. 96%96% of of the the pixels pixels over over the the area area have have an an altitude altitude between between 1100 1100 and and 3000 3000 m. m. SpeciesSpecies distribution distribution models models (SDMs) (SDMs) are are based based on on the the computation computation of of an an empirical empirical relationshiprelationship between between the the presence presence of of a a species species (a (a sample sample of of its its distribution) distribution) and and the the actual actual valuesvalues of of the the selected selected explaining explaining factors. factors. Range Range projections projections are are obtained obtained by by computing computing a a probability of presence over the study area using the relationship. The methodology has Diversity 2021, 13, 94 3 of 20 been applied to parrots several times with different objectives. For instance, comparing the projection of models fitted to historical data with actual ranges allowed to study the conservation status of Andean Pyrrhura in Colombia [14] or of Amazona in Venezuela [15]. Thanks to climate driven SDMs, the substitution of the actual climate with future climate allows projection of decreasing and shifting ranges in Amazona pretrei [16]. Climate driven SDMs also permitted computing