Trans Situ Conservation of Crop Wild Relatives

Trans Situ Conservation in the Borderlands

Arizona and the United States–Mexico desert borderlands harbor important CWR diversity, including many species significant for food systems from local to continental scales (Table 4). The 62 CWR species conserved in situ comprise ∼6% of the over 1000 CWR and wild utilized plant taxa in Arizona (Khoury et al., 2013; Khoury and Nabhan, 2019). Notably, some of the in situ populations have been utilized by nearby Native American and Hispanic communities for centuries, with both oral histories and archaeology documenting the use of wild plants like chiltepins at Rock Corral Canyon (Nabhan, 1978).

The low number of CWR species documented in common between the two in situ sites is consistent with the high β diversity found throughout the Sonoran Desert, Chihuahuan Desert, and intervening Sky Island montane landscapes of the United States–Mexico borderlands (McLaughlin, 1986). This high species turnover has implications for planning optimal in situ CWR protection (e.g., reserve size and spacing). We recommend a binational, inter-agency conservation planning effort to improve the in situ protection of CWR diversity and connectivity in the borderlands.

With a few exceptions of common species, most of the CWR we evaluated were inadequately represented in ex situ collections, suggesting conservation gaps and limited availability of genetic resources. Perhaps most disconcerting, the species with the greatest in situ vulnerability had little to no ex situ representation in national genebanks. Although regional seed and living plant collections provide educational and research opportunities for some of these species, the protection these collections offer is likely insufficient given increasing in situ habitat loss and environmental change.

Improving the comprehensiveness of CWR conservation, through both in situ and ex situ measures, is critical given the mounting environmental, social, and political pressures in the United States–Mexico borderlands (Liverman et al., 1999; Peters et al., 2018). We argue that the desert borderlands are disproportionately important relative to their number of CWR species for the following reasons:

• 1. A number of borderland CWR have high conservation priority in North America due their close relationship to internationally important crops and limited representation in major ex situ collections (Castañeda-Álvarez et al., 2016; Greene et al., 2018). Examples include wild chile, pitseed goosefoot (Chenopodium berlandieri Moq.), and desert mountain manihot [Manihot angustiloba (Torr.) Müll. Arg.].
• 2. Compounding effects of climate change and accelerating habitat destruction and fragmentation in the borderlands are increasing in situ extinction risk (Peters et al., 2018). Some borderland CWR already have elevated in situ vulnerability rankings due to their limited distributions, rarity, or threatened status, such as the Santa Cruz striped agave and Arizona passionflower [Passiflora arizonica (Killip) D.H. Goldman].
• 3. Many borderland CWR have adaptations to heat, drought, salinity, or other abiotic and biotic stressors likely to be exacerbated in United States agriculture due to climate change (Table 4). These CWR, such as the common sunflower (Helianthus annuus L.), Arizona walnut, and wild tepary bean, hold potential as breeding materials, hardy rootstocks, or new “crops” in and of themselves.
• 4. Borderland populations of a number of CWR are at their northern range and climatic limits. Of these populations, many contain unique genetic variation or traits not found elsewhere in the species range (Votava et al., 2002). Furthermore, as access to germplasm collected from Mexico decreases, through loss of accession availability from genebanks or increasing restrictions on the movement of plant materials across international borders, these northern populations may become the only sources of genetic material available to plant breeders in the United States.
• 5. Borderland CWR have direct economic importance at local to regional scales (Table 4). Within the Santa Cruz River watershed, CWR and wild utilized species from 15 genera are being used in 80 different food products from nearly 50 microenterprises (Nabhan et al., 2019). Without proper in situ protection and management, harvesting could erode CWR genetic diversity and negatively affect resources for both direct local use and indirect use in plant breeding and crop improvement.

Trans Situ Conservation at Large

Integrated in situ protection and ex situ collection is increasingly proposed to conserve CWR genetic diversity and safeguard food security in the face of climate change (Dempewolf et al., 2014). Trans situ conservation goes one step further, calling for a more dynamic integration of multiple in situ and ex situ measures, from conservation to research to education, spanning local to global scales. Just what would a trans situ approach to the conservation, evaluation, and use of CWR add to the current mix of conservation strategies being used in the United States? The short answer can be summarized in three words: complementarity, redundancy, and synergy (Becker et al., 1998; Meilleur and Hodgkin, 2004).

Complementarity among in situ and ex situ strategies improves the conservation and availability of CWR genetic diversity for plant breeding and crop research (Engels et al., 2008). In situ conservation protects not just the target CWR species, but also the native environment within which the species continues to coevolve with its biotic associates. Some aspects of trait selection and crop diversification can only be answered by studying CWR in situ (Chen et al., 2017). Ex situ conservation of CWR genetic diversity in national and global genebanks, such as the NPGS, provide access to genetic materials for use in plant breeding and crop improvement (Byrne et al., 2018). Local and regional ex situ facilities (botanical gardens, arboreta, museums, and nurseries) located near in situ CWR populations offer complementary conservation, research, and education opportunities (O’Donnell and Sharrock, 2018). Their seed and living plant collections support the direct local use of appropriately adapted and regionally relevant CWR.

Trans situ conservation builds redundancy across strategies and buffers threats from climatic, political, and economic instabilities. Wild plants face a rising risk of extinction as climate change and human land use accelerate (Zhang et al., 2017b). Ex situ collections serve as an important insurance policy for increasingly threatened in situ CWR populations (Li and Pritchard, 2009). Ex situ sampling should aim to improve the representation of genetic and environmental diversity, and therefore the range of local adaptation, held in national genebanks and regional ex situ collections (Ramírez-Villegas et al., 2010; Hoban and Schlarbaum, 2014; Khoury et al., 2015, 2019). These “backups” require maintenance, however, as ex situ samples themselves are vulnerable to genetic erosion through genetic drift and viability selection (Fu, 2017). Ex situ samples and situ populations are never exact analogs of one another and diverge genetically through time.

Ex situ facilities must also cope with the effects of climate change. As documented in another arid zone, the Bekaa Valley of Lebanon, aquifer depletion and soil salinization are currently threatening years of successful seed regeneration partnerships and impacting germplasm repositories (Daghir, 2012; Duggan, 2017; Nabhan, unpublished data, 2019). Degradation or closure of ex situ facilities is emerging as a secondary effect of the interactions among climate change, social conflict, warfare, and the resulting economic instability of agricultural regions and institutions (Duggan, 2016, 2017). The loss of operations at the International Center for Agricultural Research in the Dry Areas (ICARDA) station near Aleppo, Syria, at the same time that drought and destruction of irrigation infrastructure occurred (Gleick, 2014; Duggan, 2016) produced a negative feedback loop. Increasing the redundancy of accessions within and among ex situ collections and facilities will help avert massive losses in CWR genetic diversity.

A number of synergies arise when integrating in situ and ex situ components. As illustrated by the wild chile research, integrating in situ and ex situ studies of CWR genetic diversity, adaptation, and ecological interactions can lead to advances in crop improvement and in situ management. Strengthening collaboration between regional ex situ facilities and national genebanks could improve the ex situ conservation and accessibility of CWR genetic resources. National genebanks may not have the resources to adequately regenerate the numerous CWR with potential for crop improvement but do have the infrastructure for large-scale germplasm distribution. Regional ex situ facilities with conditions similar to nearby in situ CWR populations are well positioned to research, regenerate, and regionally distribute locally adapted germplasm but may not be equipped for large-scale distribution. Widely varying infrastructure for genebanking at these facilities underscores a need for training and capacity building to support local and regional ex situ collections (O’Donnell and Sharrock, 2018).

Trans situ conservation must also address the occasional tensions that arise when multiple in situ and ex situ components are simultaneously functioning. For instance, in situ CWR conservation and management have historically received a miniscule proportion of the support provided to ex situ conservation and use initiatives. Our case study illustrates the different, and perhaps at times competing, cultural and economic uses of CWR (Table 4). It is unclear whether formal habitat protection impedes or, alternatively, safeguards traditional stewardship and use. Linking local community livelihoods and other rural development opportunities to local in situ conservation projects (Kux, 1991) may help alleviate some tensions. In the case of the Wild Chile Botanical Area, the right to harvest the wild chile by local families who traditionally used the area as gathering grounds was assured and external commercial extraction was controlled. Studying the effects of human harvest and management on CWR genetic diversity (González-Jara et al., 2011) can guide sustainable in situ use that supports both local economic productivity and crop improvement efforts.

Finally, there is one particular in situ conservation measure that remains understudied and underdeveloped: how can we more actively manage landscapes to favor the persistence and genetic diversity of CWR in situ? Historically, the USFS and USDA-ARS have had neither funds nor mandates to actively manage CWR like the wild chile or its biotic associates. Only recently have the two agencies begun collaborative efforts to support CWR conservation through active in situ management and ex situ conservation (USFS, 2014). Such dynamic management for CWR species has been recommended by Iriondo et al. (2008) and Maxted and Kell (2009), yet in the southern Arizona case study, we know little about which management practices most affect persistence of CWR in situ (Table 5). The presence of two in situ sites with different land use practices overseen by different agencies offers an opportunity to identify which agency is more disposed to actively manage CWR through a trans situ framework.