Coupling people and nature: social-ecological lters of beetle functional diversity in local campesino and migrant homegardens of the southern Andes

Homegardens are coupled social-ecological systems that act as biodiversity reservoirs while contributing to local food sovereignty. These systems are characterized by their structural complexity, while involving management practices according to gardener’s cultural origin. Social-ecological processes in homegardens may act as lters of species’ functional traits, and thus inuence the species richness-functional diversity relationship of critical agroecosystem components like beetles (Coleoptera). We tested the species richness-functional diversity relationship of beetle communities and examined whether habitat structure across different levels, sociodemographic proles, and management practices act as lters in homegardens in a Global Biodiversity Hotspot, Chile. For 100 homegardens (50 campesino and 50 migrant), we sampled beetles and habitat attributes, and surveyed gardeners’ sociodemographic proles and management practices. We recorded 85 beetle species and found a positive relationship between species richness and functional richness that saturated when functionally similar species co-occur more often than expected by chance, indicating functional redundancy in species-rich homegardens. Gardener origin (campesino/migrant), homegarden area (m 2 ), structural complexity (index), and pest control strategy (natural, chemical, or none) were the most inuential social-ecological lters that selectively remove beetle species according to their functional traits. We discuss opportunities in homegarden management for strengthening local functional diversity and resilience under social-environmental changes. Our results support the notion that functional diversity is not only affected by the pool of species occurring in beetle communities (rst objective of our research: species richness–functional richness relationship). Beetle functional diversity is also inuenced by social-ecological lters, which are coupled human-nature factors that selectively remove species according to their functional traits, likely through shifting the intensity and magnitude of competition in biological communities 23,61,62 . In accordance with other studies, the observed relative spatial mismatch for diversity parameters in the study area challenge the use of any one diversity component as a surrogate for other parameters in agroecology, land-use planning, and biodiversity conservation 37,63 . This study found that gardener cultural origin (indigenous and non-indigenous campesino vs. lifestyle migrant) might inuence both the taxonomic and functional diversity of beetle communities in homegardens. This result supports previous studies exploring the role of gardener origin on the composition, structure, and functioning of homegardens, as the latter usually reect many aspects of the food system, tastes, and agricultural traditions of people co-occurring in an area 19,64 . For instance, differences in both crop species and intensity of management practices are associated with the gardener origin in Vietnamese homegardens 64 . Number of management practices and homegarden area are different among migrant and non-migrant homegardens and both social-ecological lters differentially inuence beetle functional groups in Indonesian homegardens 19 . While we acknowledge that homegarden attributes are likely inuenced by several factors beyond gardener origin 7 , our study shed light on some of the underlying social-ecological lters explaining variation in the taxonomic and functional diversity of beetles in campesino and migrant homegardens of the southern Andes. We found support to our prediction that homegarden area leads to an increase in beetle species richness, relative abundance, and functional richness, a result in accordance with the few studies dealing with taxonomic and functional diversity of beetle communities in homegardens 20,21 . The long-standing Island Biogeography provides a framework for examining the underlying forces shaping community and species loss in homegardens. For beetle in coupled social-ecological homegardens chiey local


Introduction
Biological and cultural diversity have been recognized as inextricably linked, particularly in those naturehuman coupled systems in which the interaction among multiple entities and actors allows their synergy 1,2 . However, poverty, population growth, power inequalities, climate change, and latest emerging diseases have in many places led to question how possible it is to nd and strengthen these synergies 3 .
Homegardens are peridomestic complex microenvironments in which useful plants are cultivated and are traditionally integrated within a larger coupled nature-human system 4 . These small-scale socialecological systems provide year-round resources for household needs such as nourishment, medicine, ornaments, and income generation opportunities, while involving speci c management practices 5,6 . Homegardens are composed by multiple farming components, which generate structurally complex habitats across vertical (e.g. multiple strata of roots and tubers, small annual and perennial plants, shrubs, and trees) and landscape levels (e.g. distance to a source of species) [7][8][9] . As such, structurally complex homegardens have the potential to play an important role as biodiversity reservoirs 10,11 .
Scholars have paid great attention to the diversity of plants grown in homegardens in different countries, mainly in tropical social-ecological systems 7 . However, the complex habitat structure of homegardens, the sociodemographic pro les of gardeners (e.g. cultural origin), and their different management practices (e.g. use of agrochemical or organic pesticides), can act as social-ecological lters in uencing the taxonomic diversity (e.g. species richness) of small animals, such as beetles (Arthropoda: Coleoptera), in many human biomes beyond the tropics [12][13][14][15] . These social-ecological lters are de ned as those coupled human-nature factors that selectively remove species according to their functional traits [16][17][18] . For example, homegarden area lters arthropod species and thus structure community assembly in homegardens of Indonesia 19 and India 20 . Furthermore, the diversi cation of management practices, including the use of pesticides, mediates the variation of beetle diversity in homegardens of Mexico 21 .
Beyond the in uence on species richness, social-ecological lters can also in uence the functional roles played by beetles in agricultural systems such as pollination, nutrient cycling, and pest control 19,20,22,23 . Thus, these lters determine the functional diversity of beetles, de ned as the value, range, and relative abundance of beetle functional traits in a community 12,24 . Theoretical and empirical studies have shown that species richness and functional richness (i.e. the volume of functional niche space lled by species in ecological communities), are expected to correlate from negligible to a one-to-one relationship 17,25 .
Species-rich communities are predicted to show a saturating "species richness-functional richness relationship" because of the presence of functional redundancy, which is the degree to which species resemble each other in their functional traits 26 . On the contrary, functional evenness (i.e. the regularity of density distribution in lled niche volume) is not expected to show any a priori relationship with species richness.
Homegarden social-ecological systems are places in constant adaptation to globalization and its associated environmental changes (e.g. climate, water scarcity, arrival of new species and technologies, etc) 27-29 . Globalization has shifted the relationship between urban and rural shifting from unidirectional migration (rural exodus) to bidirectional circulation 30 . As a result, in many locations it is possible to nd local indigenous and non-indigenous campesinos (i.e. peasants who were born and have been living and working in the territory most of their lives), co-inhabiting with recently arrived migrants. Lifestyle migrants are urban people who voluntarily relocate to rural areas pursuing a greater connection with nature and are rapidly settling in many rural locations worldwide 31 . Many lifestyle migrants have incorporated homegardens into their livelihoods, but their socio-demographic pro les and management practices may in uence contrasting patterns of both taxonomic and functional biodiversity in homegardens, in comparison to local campesinos 32,33 .
Andean temperate ecosystems, a Biodiversity Hotspot in south-central Chile 34 , are globally exceptional for their high rates of endemism while supporting a relatively species-poor fauna 35 . Here, studies on the relationship between species richness and functional diversity, only available for mammals and birds, have reported a low functional redundancy 36,37 . In these largely modi ed landscapes, homegardens may play a signi cant role in helping to sustain local livelihoods while maintaining the resilience of beetle diversity and ecosystem functioning. Beetles are essential functional components of ecosystems as they provide critical human-derived services 38,39 . However, this group is globally declining at an alarming rate 40,41 and information on species ecosystem functioning remains largely undocumented, especially in globally threatened ecoregions such as Andean temperate ecosystems [42][43][44][45][46] .
In this study we (i) test the species richness-functional diversity relationship of beetle communities and (ii) examine whether habitat structure across different levels, sociodemographic pro les, and management practices act as social-ecological lters in homegardens in southern Andean temperate ecosystems. We predicted that, because these temperate ecosystems are a species-poor system, homegardens will show an accelerating species richness-functional richness relationship and associated low functional richness and low redundancy in beetle communities. We also predicted that habitat structure, sociodemographic pro les, and management practices act as social-ecological lters in homegardens, and thus selectively remove species according to their functional traits in this Global Biodiversity Hotspot.
Beetle relative abundance (60.8 ± 71.8) ranged between 2 and 421 individuals per homegarden. The models with highest support for relative abundance contained area, origin, and pests as the most important social-ecological lters (Table 3b). Model selection showed that relative abundance was positively associated with homegarden area (m 2 ; Fig. 2d; best supported model with estimated β = 0.065). Best models also supported an association between gardener origin and relative abundance (Table 3a); the latter was higher and positive in campesino homegardens (mean ± SD = 77.9 ± 78.6; β = 79.26) and smaller and negative in migrant homegardens (43.2 ± 60.1; β = -38.32) (Fig. 2e). Beetle relative abundance was positively affected by using a natural (mechanical by hand or using biopreparations) pest control strategy (β = 78.00) and negatively affected by chemical control (β = -44.63), while no control did not have an effect on beetle relative abundance. Structural complexity did not have an effect on beetle relative abundance (Fig. 2f).
The resulting projections of beetle diversity graphically indicated a zone of high values for beetle relative abundance to the east of the study area (Fig. 3b). The spatial projections for beetle species richness and functional richness did not reveal a clear pattern of areas with high values for these parameters. Anyhow, this analysis indicated a relative spatial mismatch between estimates of beetle species richness, relative abundance, and functional richness in the study area (Fig. 3).

Discussion
This research extends previous research on the relationship between biodiversity and ecosystem functioning, acknowledging that homegardens are coupled social-ecological systems in which biodiversity has the potential to thrive. We found that several beetle species may be performing similar roles (i.e. are functionally redundant) in southern Andean homegardens with relatively high number of species. Thereby, if some go locally extinct (removed from a diverse homegarden) this will likely not produce substantial loss in agroecosystem function 47 . This result associates with the observed steep relationship between beetle species richness and functional richness, in relation to a random expectation, that started to saturate with relatively high beetle richness 48,49 . This nding suggest that homegardens with high functionally redundancy will be more resilient to shifts in social-ecological lters 50-52 . Beetle species richness-functional diversity relationship Our recorded total number of species is only a subset of the total species recorded or likely to occur in nearby temperate forest ecosystems [42][43][44][45]53 . However, remarkably and contrary to our expectations, we found that beetle communities have a relatively high functional richness and functional redundancy in southern Andean homegardens. This result is not characteristic of systems generally considered as "species-poor" 36,37,54,55 . Andean temperate ecosystems are relatively impoverished in terms of faunal species richness in comparison to other tropical, subtropical, Mediterranean, and temperate ecosystem types 43 . During the Pleistocene (most recent period of repeated glaciations), immigration of species from tropical latitudes was not able to compensate for the extinction of local biota resulting from the contractions on the distribution of temperate forests 56 . Climatic change and geographic barriers, such as the Andes mountain range and the Atacama Desert, resulted in a net loss of species during the Pleistocene, especially of faunal groups with tropical lineage 57 . While little is known about biogeographic distribution of beetles in the southern temperate ecoregion 42,58−60 , our study shows that small-scale patches of habitat, like homegardens, can be both taxonomically and functionally rich.

Social-ecological lters and beetle communities
Our results support the notion that functional diversity is not only affected by the pool of species occurring in beetle communities ( rst objective of our research: species richness-functional richness relationship). Beetle functional diversity is also in uenced by social-ecological lters, which are coupled human-nature factors that selectively remove species according to their functional traits, likely through shifting the intensity and magnitude of competition in biological communities 23,61,62 . In accordance with other studies, the observed relative spatial mismatch for diversity parameters in the study area challenge the use of any one diversity component as a surrogate for other parameters in agroecology, land-use planning, and biodiversity conservation 37,63 .
This study found that gardener cultural origin (indigenous and non-indigenous campesino vs. lifestyle migrant) might in uence both the taxonomic and functional diversity of beetle communities in homegardens. This result supports previous studies exploring the role of gardener origin on the composition, structure, and functioning of homegardens, as the latter usually re ect many aspects of the food system, tastes, and agricultural traditions of people co-occurring in an area 19,64 . For instance, differences in both crop species and intensity of management practices are associated with the gardener origin in Vietnamese homegardens 64 . Number of management practices and homegarden area are different among migrant and non-migrant homegardens and both social-ecological lters differentially in uence beetle functional groups in Indonesian homegardens 19 . While we acknowledge that homegarden attributes are likely in uenced by several factors beyond gardener origin 7 , our study shed light on some of the underlying social-ecological lters explaining variation in the taxonomic and functional diversity of beetles in campesino and migrant homegardens of the southern Andes.
We found support to our prediction that homegarden area leads to an increase in beetle species richness, relative abundance, and functional richness, a result in accordance with the few studies dealing with taxonomic and functional diversity of beetle communities in homegardens 20,21 . The long-standing Island Biogeography Theory 65 provides a framework for examining the underlying forces shaping community assembly and species loss in homegardens. For example, beetle communities shaped in coupled socialecological systems like homegardens may be chie y determined by local extinctions, with smaller homegardens likely exhibiting the highest extinction rates of species 41,66 .
Furthermore, the distribution of traits as a function of habitat area extends the Island Biogeography Theory beyond the traditional species-area relationship 67 . Social-ecological lters may perform as nonrandom processes that act on beetle species traits including the in uence of local habitat conditions on species' tness and ecological interactions, such as competition, mutualisms, and other trophic associations 23, 38,39,68 . For example, larger and heavier species that require relatively large territories or species with limited dispersal ability will have a higher likelihood of local extinction in response to a shrinking homegarden area 69,70 . Therefore, only subgroups of species sharing akin functional traits (i.e. appearing functionally clustered) will be able to persist or outcompete other species on small habitats 67,68 . In our study, for example, relatively large species like Apterodorcus bacchus and Calosoma vagans were never recorded in homegardens with an area smaller than 150 m 2 . In the southern Andes, homegarden area is de nitely a non-random process. While campesinos generally have properties that are still larger than migrant ones, historical and contemporary processes of encroachment into indigenous and non-indigenous campesino way of life and the land upon which they live has been associated with changes in the agricultural system and a decreasing trend in the area of homegardens 71 .
As shown, larger homegardens likely provide more resource opportunities and they should tend towards being more representative of the regional pool of species or if there is high habitat structural complexity 4,72 . Indeed, we found that homegarden structural complexity was positively associated with both taxonomic and functional diversity parameters. Generally, homegardens are complex microenvironments composed of multiple strata that generate diversi ed niches for multiple species and, likely, functional traits to coexist 19 . Interestingly, homegarden structural complexity was correlated with the homegarden age (Spearman > 0.6); the latter measured as the number of years that the homegarden has been located in the same spatial location. Therefore, the oldest homegardens are located in the farms that have the longest history of settlement in the study area. Older homegardens, managed by local campesinos who have inhabited longer in the area, will host more vegetation layers including annual crops and perennial trees than migrant homegardens, and will resemble the complex surrounding forest ecosystems 7 .
Structurally complex homegardens will not only increase the functional niche space lled by species in beetle communities and enhance bene cial organisms, such as pest-control predators, pollinators, and seed dispersers 13 , they will also be more important carbon sinks than those that are structurally simpli ed and lack trees 73 . In a complexity science context, this result suggests that these small-scale systems have a social-ecological memory in which older and structurally complex homegardens act as long-lived system entities whose presence continues to in uence compositional, structural, and functional states of the system over time 51 .
Using a natural (mechanical by hand or using biopreparations) pest control strategy positively in uenced beetle functional richness and relative abundance, while chemical pesticides negatively affected functional richness. These results should be viewed with caution because it may be interpreted that controlling insects using natural strategies can potentially increase phytophagous beetles. However, we have recorded that controlling beetles that damage crops by hand is a wide spread strategy (mostly to control Epicauta pilme) which reduces damage while increasing the relative abundance of bene c beetles (pollinators like Cantharis variabilis and pest controllers like Eriopis connexa; J. T. Ibarra Unpublished Data). The systematic use of pesticides in agriculture over the past decades has negatively impacted insect populations 74 , a pattern also reported for homegardens 20 , with persistent negative effects on biodiversity and biological control potential 75 . In our study area, campesinos report a higher use of pesticides than migrants because the former have been provided for decades with agro-chemicals (fertilizers, pesticides, herbicides, and hybrid seeds) by extension agents from governmental programs 33 . However, campesinos and migrants are progressively dismissing the use of agro-chemicals as a result of an increasing adoption of agroecological practices not only limited to chemical-free agriculture but also as an alternative movement for the defense and re-signi cation of rural areas 32,33 .
Recommendations for homegardening while sustaining beetle diversity Beetles are globally declining, principally, because of habitat loss and conversion to intensive agriculture. Paradoxically, beetles comprise many predator, pollinator, and saprophytic species of outstanding importance for agroecosystem functioning. Homegardens, usually multifaceted, can be oriented towards building synergies between local food sovereignty or income generation depending on the concerns of the family and biodiversity. Our results highlight the importance of increasing the size of homegardens as much as possible and promoting the cultivation of a multi-layered arrangement of crops (e.g. combination of roots and tubers, small annual and perennial plants, shrubs, and trees) that will increase habitat structural complexity across years, and thus resources for a diversity of beetle species, that will resemble with surrounding forests. Agricultural and environmental governmental agencies charged with supporting small-scale agriculture should discourage the use of pesticides to control beetles and other insects, as these chemicals likely have negative effects on ecosystem functioning and biological control potential. These measures may contribute to maintain ecosystem functioning, local livelihoods, and the resilience of beetle communities in times of rapid social-environmental changes.

Study area
The study was conducted in the Villarrica watershed in 30 different human settlements (localities) within the municipalities of Loncoche, Villarrica, Pucón, and Curarrehue in the Andean zone of the La Araucanía Region, southern Chile (39.42˚ S 71.94˚ W). The area has a temperate climate with a short dry season (< 4 months) during the southern hemisphere summer (December to March). Over the last decade, the mean annual temperature has been 12° C with temperatures varying from 0.8°C to 28°C and mean annual precipitations of 2143 mm (http://explorador.cr2.cl/). The area has volcanic and mountainous topography with vegetation dominated by Nothofagus obliqua at lower elevations (200-1000 m) and mixed deciduous Nothofagus pumilio with the conifer Araucaria araucana at higher elevations (1000-1500 m). The landscape, dominated by native temperate forests, comprises a mosaic where small-scale agroecosystems (homegardens, orchards, and potato elds) mix with pasture lands, lakes, rivers, nonnative tree monocultures as well as volcanoes and mountains 72 .

Study design
All methods were carried out in accordance with relevant guidelines and regulations. The study was approved by Scienti c Ethics Committee of the Ponti cia Universidad Católica de Chile (Resolution #160415004). We conducted surveys and interviews after obtaining prior informed consent from each gardener. Fieldwork was conducted in two eld seasons during the summer season between December and February of 2016-2017 and 2017-2018. In total, we studied 100 homegardens (50 homegardens from Mapuche indigenous and non-indigenous campesinos were surveyed the rst eld season and 50 homegardens from lifestyle migrants were surveyed the second eld season). Mapuche indigenous and non-indigenous campesinos were grouped together because the latter are people who were born, live, and work in the territory, often in close relationship with Mapuche families; their agriculture resembles and integrates the Mapuche traditional agricultural system 33 . For their part, lifestyle migrants are people who migrated during adulthood from an urban setting to the study area 32 . We used successive-referral sampling as our non-probability recruiting method 76,77 . The criteria for selecting a homegarden for study was that its main purpose was family consumption and that it was at least two years old.

Beetle sampling
We quanti ed beetle species richness (number of species per homegarden) and relative abundance (number of individuals per homegarden) using pitfall traps and sweeping nets to maximize the representation of the assemblage 19,42,78 . To determine an adequate sampling effort of beetles at each homegarden, we constructed sample-based rarefaction accumulation curves for both sampling methods. We considered an adequate sampling effort when there was no longer an increase in species as individuals accumulated 79 .
We randomly deployed four pitfall traps every 25 m 2 with a maximum of 16 traps (determined through accumulation curves) for three nights per homegarden 19 . We deployed traps between 8:00-11:00 am and were collected at the same time the fourth day. Each trap was buried 12 cm, had a diameter of 7.3 cm and was placed at the soil surface. Traps were lled to a third of their capacity with an ethylene glycol solution and covered by a suspended lid. For sweep netting, we performed one 10 m transect of 1.5 minutes every 25 m 2 of homegarden with 3 m between transects and a maximum of nine transects per homegarden (determined through accumulation curves; Lister and Garcia 2018). We performed sweep netting transects from 12:00 to 16:00 on clear days with temperatures ranging from 15° C to 25° C. We did not conduct sweep netting transects during cold (< 15° C), cloudy or rainy days. In total, we deployed 1.410 pitfall traps over 371 nights and conducted 371 sweep netting transects. We collected all beetle individuals and identi ed at the species level utilizing dichotomous keys in guides and the Coleoptera reference collection available at the Natural History Museum of Chile. Finally, we measured the length of a minimum of three individuals per species for functional trait analysis (below).
Homegarden habitat, sociodemographic pro les, and management practices Through guided walks with gardeners, we identi ed all the crop species intentionally cultivated in each of the 100 homegardens and estimated the ground cover (%) of each crop vertical stratum (Table 1; 81 ). We measured homegarden area (m 2 ) and used a handheld GPS to record the homegarden spatial location (geographic coordinates). We used Google Earth® images to measure the distance from the homegarden to the nearest native forest edge (normally seen as a clear-cut line between forest and a different land cover; e.g. pasture). We further conducted structured interviews with data on sociodemographic pro les and management practices, including gardener origin, age, gardening experience, number of family members, homegarden age, and pest control strategies (Table 1; 19,77,82 ).

Beetle traits and functional diversity
We used three traits of beetle species, including two categorical (foraging guild and habitat-use guild) and one continuous (body weight) measures (Table 2). These traits are associated with resource use by species and are mechanistically linked to ecosystem functioning (e.g. quantity, type, and strategies for obtaining resources by each species; Table 2). For example, foraging guild has been used for linking resource production and disruption to beetle diversity 83,84 . Data on foraging guild and habitat-use guild were extracted from 34 bibliographic references (including 85-93 , among others). For its part, body weight has been utilized to show how environmental change has indirectly precipitated a bottom-up trophic cascade and consequent collapse of the food-web structures 80 . Body weight for each beetle species was calculated from measured body lengths using the function proposed by (Johnson and Strong, (2000): According to their foraging guild, we classi ed each species as mainly bene cial (predator, pollinivorous, saprophagous, mycetophagous) or harmful (phytophagous, xylophagous) for homegarden production.
Finally, we quanti ed functional diversity using the metrics functional richness (FRic) and functional evenness (FEve) 24 . FRic was calculated using the beetle traits and the presence/absence of each species per homegarden. To calculate FEve, we combined species functional traits (Table 1) with the estimated species relative abundance. We calculated FRic and FEve using the program R-FD 95 .

Data analysis
We used Generalized Linear Mixed-Effect models 96 , implemented in the packages lmer 97 and AICcmodavg packages 98 in R 99 . We rst tested the species richness-functional diversity relationship by regressing species richness against FRic and against FEve. Then, we examine the association between a dependent variable and independent variables ( xed effects; social-ecological lters; Table 1) collected in grouped units at different levels (random effects; season and locality). We rst assessed collinearity to reduce the number of independent social-ecological lters presented in Table 1. With strongly correlated social-ecological lters (Spearman's r > 0.6), we kept for analysis either the one considered to be most ecologically in uential for the studied taxa or the most feasible to implement in management practices (Table 1). We examined the xed effect of homegarden area, crop richness, structural complexity, distance to forest, homegarden age, gardener origin, and pest control strategy on the following dependent variables: beetle species richness, relative abundance, and functional richness. To nd the best models for our dependent variables, we generated a candidate set of models based on model weights (w i ) and the precision of the estimated coe cients, using Akaike's Information Criterion (AIC; 100 . We considered models with a ΔAIC < 2 of the top model as the competitive set of best-supported models. For easier interpretation of our results and for categorizing taxonomically and functionally important biodiversity areas, we projected the observed values for beetle species richness, relative abundance, and functional richness utilizing the spatial interpolation toolbar Kriging 101