Ex situ conservation of threatened plant species in island biodiversity hotspots: A case study from Hawai‘i

Highlights

• Hawaiian plant conservation can serve as a model for other biodiversity hotspots.

• In this system, micropropagation (tissue culture) is a critical conservation tool.

• Micropropagation is underutilized and it serves many important storage functions.

• Interorganizational alliances are essential for effective conservation outcomes.

• It is necessary to combine a diversity of approaches to meet zero-extinction goals.

Abstract

Global plant extinction rates have increased dramatically over the past 50 years. Conservation efforts are especially challenging across the Hawaiian archipelago, where habitat loss and competition with invasive species threaten the existence of native plant species. Currently, 238 endemic Hawaiian plant species have fewer than 50 individuals remaining in the wild. To counteract this daunting statistic, conservationists apply a suite of ex situ techniques to effectively safeguard the many threatened plant species from imminent extinction. This perspective piece highlights how an integrated conservation approach that utilizes a co-located seed bank, micropropagation laboratory, and greenhouse, has led to the successful rescue and conservation of many threatened Hawaiian plant species. We draw on specific examples from the long history of Hawaiian plant conservation to detail successes and ongoing challenges associated with the implementation of ex situ conservation techniques. In doing so we discuss how plant micropropagation has emerged as a critical ex situ conservation tool, and how this underutilized tool fits into plant conservation as a whole. We also emphasize the essential roles that partnerships with external organizations play in ensuring that effective conservation efforts are implemented. Last, using lessons learned from these examples we detail and discuss an ex situ plant conservation decision tree that is widely applicable to other plant diversity hotspots of conservation concern, in order to help ensure regional and global zero-extinction goals are met.

Introduction

Evidence indicates that rapid human alteration of global processes and the degradation of ecosystems worldwide are driving a sixth mass-extinction event (Ceballos et al., 2015). The loss of plant biodiversity has profound impacts on human livelihoods by negatively affecting ecosystem services (Balvanera et al., 2014; Cardinale et al., 2012) that play integral roles in the function of food production and natural systems (Tilman et al., 2014; Vitousek et al., 1997). By current estimates tropical plant species are generally twice as threatened as temperate species, due in part to high rates of anthropogenic habitat conversion (Brummitt et al., 2015). To counteract these effects, botanical gardens and arboreta around the world have led the charge in the conservation of threatened species (IUCN, 2019) through in situ (in natural habitat; Chen et al., 2009; Havens et al., 2014) and ex situ (outside natural habitat; Havens et al., 2006; Li and Pritchard, 2009; Mounce et al., 2017) programs that have successfully safeguarded thousands of plant species across the United States (Oldfield et al., 2019) and worldwide (Wyse Jackson and Kennedy, 2009). These programs have also pioneered the development of cutting-edge techniques that have led to insights on in and ex situ plant conservation (Donaldson, 2009; Smith, 2016), while also supporting plant reintroduction and restoration efforts (Kawelo et al., 2012; Miller et al., 2016). Nonetheless, there is still a critical need and great potential to expand the focus of these conservation efforts (Miller et al., 2016), and to conduct national (Havens et al., 2014) and global assessments (Pelletier et al., 2018) of the conservation status of plant species, to improve threatened plant conservation efforts worldwide (Corlett, 2016).

Although a diverse set of techniques are used to conserve threatened species, many ex situ plant conservation programs have traditionally focused on preserving these species in seed banks (Havens et al., 2004; O'Donnell and Sharrock, 2017). Conventional seed banking is used extensively as a conservation strategy because it is the simplest method for long-term germplasm storage. Seed storage is also relatively low maintenance and does not require specialized equipment when implemented on small scales. However, seed banking is not a viable option for some plant species (Fant et al., 2016), which are referred to in the literature as “exceptional species” (Pence, 2011). There is ongoing debate about how best to define exceptionality, so in this article we refer to plant species as “exceptional” if (a) they produce recalcitrant (desiccation-sensitive) or freeze-sensitive seeds that cannot be stored conventionally; or (b) existing populations produce few or no viable seeds (Pence, 2013). These factors make ex situ conservation very challenging and plant tissue culture, or micropropagation, has emerged as an important ex situ storage alternative for these species (Pence, 2011). Using these techniques, explants (i.e., small pieces of living plant tissue that have been removed for culturing), are placed in vitro and used to culture viable plantlets or clones (Fay, 1992). These clones are subsequently stored to maintain plant species' genetic lines. Over the past five decades these in vitro techniques have been developed and refined with the goal of putting exceptional species into a stable environment where they can be propagated and grown to complete full life cycles (Pence, 2013; Sugii and Lamoureux, 2004). Plant micropropagation has therefore become a key component of the “integrated plant conservation” approach (Falk, 1990), which uses a combination of in and ex situ approaches to ensure persistence of threatened plant species (Kramer et al., 2011).

Using this integrated approach to leverage all available conservation tools is especially important in island ecosystems, such as the Hawaiian archipelago, due to the fact that a majority of recorded plant extinctions occur on islands, where species tend to have small populations and are more vulnerable to disturbance events (Humphreys et al., 2019). For example, 45% of the species on the United States federal Threatened and Endangered species list are endemic to the state of Hawai‘i (424 out of 946 species; U.S. Fish and Wildlife Service, 2019). Some 238 Hawaiian endemic plant species (close to 25% of all native plants in the state) have fewer than 50 individuals (<100 for dioecious species) remaining in the wild (referred to as PEPP species throughout; Plant Extinction Prevention Program, 2019). These factors make plant conservation in Hawai‘i particularly pressing, but this has also promoted a surge of innovative developments for in and ex situ conservation techniques, and the creation of large collaborative organizational networks working towards common conservation goals (Keir and Weisenberger, 2014). These conservation networks focus a great deal of effort on the collection of propagules of threatened species for ex situ storage and propagation. Furthermore, seed banking (Weisenberger and Keir, 2014) and micropropagation (Sugii and Lamoureux, 2004) have been integrated seamlessly as critical components to ex situ plant conservation in this system.

The overall objective of this perspective piece is to detail the integrated and highly collaborative approach to threatened plant conservation that has been implemented in Hawai‘i. In doing so we highlight how micropropagation has emerged as a critical tool for plant conservation; the benefits and challenges associated with the application of these underutilized techniques; and future directions for their application. We draw on examples and historical perspectives from the Lyon Arboretum Hawaiian Rare Plant Program (HRPP) at the University of Hawai‘i, Mānoa and its partner organizations to underscore that combining multiple ex situ approaches has been essential to ensure the conservation of many threatened Hawaiian plant species. Last, we detail how micropropagation and other emerging approaches such as cryopreservation fit into an ex situ plant conservation decision tree that is widely applicable to other regions with high concentrations of threatened species. In this article we refer to plant species as threatened if they are experiencing rapid population decline and have ongoing threats to their existence; however, unless otherwise specified, not all these species have been assessed for the IUCN Red List or are currently listed on the United States Fish and Wildlife Service Threatened and Endangered species list.