A Phylogenetic Approach to Conservation: Biodiversity and Ecosystem Functioning for a Changing Globe

Abstract

As late as the sixteenth century, the world was a matrix of primarily wildlands. But due to technology development and population growth, humans increasingly altered natural habitats and modified other organisms to suit our needs. The world became “all about people”—the rest of the natural world became enslaved to us. By the eighteenth and nineteenth centuries, calls emerged for conservation and the new field of ecology developed, resulting in legislation to form national parks and save endangered species (e.g., the Endangered Species Act in the US). This “one species at a time” approach can be credited with saving a number of individual taxa, but is insufficient to deal with the modern global biodiversity crisis given the urgent pressures on remaining natural lands. We argue that considerable expansion is needed in conservation biology, moving from the single species approach to an area based approach incorporating all species and a broad phylogenetic definition of biodiversity. Biodiversity should not be considered as just the arbitrary level at which species are named—instead it is the whole tree of life. We discuss newly developed approaches to multiple species habitat conservation plans and new spatial phylogenetic methods that take into account all levels in the tree of life when making conservation decisions. To protect biodiversity, we must use all the tools we have to identify and protect landscapes that allow for future dynamics, while considering the conditions of the past and present.

1 Introduction

Life on our planet has undergone dramatic swings throughout the past 4 billion years. New lineages have emerged and diversified, yet many large groups have also gone extinct. Some lineages are driven to near extinction due to environmental perturbation, only to re-emerge as dominant taxa. According to one hypothesis, our own lineage may be an example due to the Toba eruption bottleneck, about 75 millennia ago (Rampino and Self 1992). Luckily for us, our species was widespread enough that a population in South Africa persisted, and then re-spread around the globe. Homo sapiens probably reached our global carrying capacity some 8 millennia ago (e.g., Christian 2011). But, due to our capacity for technology development, our population continued to expand. This technological development allowed us not only to expand into new habitats, but also to alter them to suit our needs. We got into the habit of treating all other species of organisms as our servants, through habitat modification (e.g., burning) to facilitate organisms we prefer, and then by directly modifying their genetics through domestication and controlled breeding. The world increasingly became “all about people” and the rest of the natural world became enslaved by humans.

The agricultural revolution turned wildlands surrounding individual villages into altered production lands that in turn, enabled more human production requiring more land development; approaching an infinite do-loop of human growth and land utilization. As late as the sixteenth century, most of the world was a matrix of wildland forests, grasslands, and shrub lands with interspersed patches of villages and farmlands (e.g., Strauss 1976). But by the twentieth century, the vast majority of the globe was human-managed land interspersed with patches of wilderness. Nineteenth century paintings such as Thomas Cole's Catskill Creek show ravages of industrial depletion of the forest, and the paintings of Grandma Moses, such as Hoosick Valley, showing forests remaining only on the hilltops, riparian ribbons, and along stone fences. The extensive forest across the lowlands, supporting large populations of deer, moose, bear, wolves, and other large mammals have been replaced by crops and cattle. Even today, the largest white pines, Pinus strobus, are found along hillsides, where they established along stone fences and stone protections (see Thoreau Succession), instead of the ancient valley-bottom stands such as the Pisgah Forest in southern New Hampshire, destroyed in the 1938 hurricane.

By the eighteenth and nineteenth centuries, calls emerged for protecting the wild beyond just the king's hunting preserves. For example, among the most articulate, Henry David Thoreau said (Maine Woods 1864):

Why should not we, who have renounced the king’s authority, have our national preserves, where no villages need be destroyed, in which the bear and panther, and some even of the hunter race, may still exist, and not be “civilized off the face of the earth,”—our forests, not to hold the king’s game merely, but to hold and preserve the king himself also, the lord of creation,—not for idle sport or food, but for inspiration and our own true re-creation?

While protections of hunting preserves, such as the Białowieża Forest in Poland, have been ongoing since the Middle Ages, protections of unique landscapes and endangered animals such as the American Bison (Bison bison) began in March of 1872, when President Ulysses S. Grant signed the Yellowstone National Park Protection Act (1872) into law to protect “from injury or spoliation, of all timber, mineral deposits, natural curiosities, or wonders within said park, and their retention in their natural condition” (Sect. 2). Subsequent national and international parks through the twentieth century have been designed to protect animals as well as geological curiosities into the foreseeable future. A slowly growing number of people began to realize that nature, and the other species on the tree of life, might have their own intrinsic value distinct from human needs.

The next major fundamental step was the establishment of the field of ecology, ökologie, in 1866 by Ernst Haeckel—a fundamental integration of evolution by natural selection as outlined by Charles Darwin and Alfred Russell Wallace, with natural history, biology, and geology. This field recognized that all organisms, from microbes to vertebrates, form an integral and interactive complex of pieces that comprise the community.

2 Twentieth Century Approach and Recognition of Biodiversity

In the early twentieth century, Frederic Clements (1916) proposed the idea of a “climax” ecological community. Specifically, following disturbance 4 or 5 stages lead toward a climax community that was the natural, or primeval state based on soils and climate. Simultaneously, the recognition that many species important to our national identity, the Bald Eagle, the Grizzly Bear (on the flag of the State of California), and the American Bison, were undergoing extirpation, or even extinction. The Endangered Species Act (ESA), passed nearly unanimously in 1973, was intended to protect these symbols. The Bald Eagle, Haliaeetus leucocephalus, recovered largely due to the banning of DDT in the US and Canada, along with protections from illegal shooting and habitat protection.

Interestingly, management efforts and funding were applied in attempting to sustain or recover populations of endangered species. Wetlands, such as the Aransas National Wildlife Refuge on the Texas Coast and the Wood Buffalo National Park in the Northwest Territories of Canada, were managed for protecting wintering and breeding habitat for Whooping Cranes, Grus americana, along with refuges along the migratory route, like the Cheyenne Bottoms and Quivira National Wildlife Refuges. These lands were protected and managed, at considerable costs both for recreation and for the threatened taxa.

But the globe was rapidly changing. Since 1950, the global human population has increased from 2.5 to 7.8 billion and the USA from 152 to 331 million. Much of the remaining wildland matrix was reduced to small islands within the larger human landscapes. Since 1973, the ESA was applied to species such as the Snail Darter (Percina tanasi) and the Stephens’ kangaroo rats (Dipodomys stephensi), taxa that were not considered national icons. However, the broader recognition that protecting these few species provides umbrella protection to a much broader host of species living in the same ecosystems, meant that by late in the twentieth century, the ESA, coupled with numerous state laws, became the major land-use planning law nationally for protecting biodiversity, and formed the basis of many international laws and regulations. Thus, the ESA became the primary unplanned authority for constraining widespread land development (Scott et al. 2006).

Notably, there have been successes with the ESA approach to protecting taxa. The ESA has been credited with recovering 39 species, along with preventing extinction in 291 additional species (https://www.biologicaldiversity.org/campaigns/esa_wild_success/). However, protections for individual taxa are continually subject to political pressures. For example, the California gnatcatcher, Polioptila californica ssp. californica, is continually subject to criticism as to whether to include it as it is also found in Mexico, and whether it is distinct “enough” for protection. In some cases, patches of less than a HA are “protected” by fencing, such as the Otay tarplant, Hemizonia conjugens (Sullivan and Scott 2000).

While this “one species at a time” approach can be credited with saving a number of individual taxa, is it sufficient in view of the current global biodiversity crisis—is it the only future of conservation? The need is urgent with many pressures on the remaining natural lands. The ESA-type approach of listing large, charismatic “umbrella species” is slow because of the legal process involved, and in any case may not be the best way to prioritize conservation of remnant wildlands to sustain the maximum of total biodiversity. To proceed with highest efficiency in this crisis we need to clarify we mean by “biodiversity” and consider carefully the best methods for focusing our conservation actions.

3 Emerging Issues at the Turn of the Twenty-First Century

Allen, Mishler, and Moritz (American Institute of Biological Sciences 2004) produced a report for the Infrastructure for Biology at Regional to Continental Scales (IBRCS) Program. Here we defined Biodiversity as “the entire tree of life from the smallest gene lineage through its many nested branches of organisms and all their ecological interactions.” Note that we did not single out species as a fundamental unit. As Solbrig et al. (1991) noted, “The diversity found within species is the ultimate source of biodiversity at higher levels.” The Rio de Janeiro Convention on Biological Diversity noted ““Biological diversity” means the variability among living organisms from all sources… within species, between species and of ecosystems” and the NRC report states that “Biodiversity (or biological diversity)” refers to the number of species and extent of genetic variability in those species in a given site.

As the matrix shifts from wildland to anthropogenic ecosystems, individual populations will be lost as these populations become constrained and isolated, and wink out of smaller or more perturbed habitats. Many genetically-distinct populations, linked under the umbrella of a shared species name, are actually quite different. Many of these populations with unique traits play key roles in ecosystem function, and when a patch is lost to development or change, unique populations are lost because of the species concept accepted for that group.

Therefore, as pointed out by Mishler (2010) and Mishler and Wilkins (2018), biodiversity should not be considered as just the arbitrary level at which species are named—instead it is the whole tree of life. Species are not comparable between lineages. They comprise an arbitrary cut-off somewhere along a branch in the tree of life (Mishler 2021). There are clades smaller and larger than the traditional species level and they are all of potential importance to the functioning of ecosystems and worthy of conservation consideration.

In the remainder of this chapter, we first discuss an important shift in viewpoint to a multiple species conservation approach and contrast it with the limitations of focusing conservation on one species at a time. Finally, we advocate taking a phylogenetic approach that takes into account all levels in the tree of life when making conservation decisions. We argue that considerable expansion is needed in conservation biology, from a single species approach to an area-based approach incorporating all species and a broad phylogenetic definition of biodiversity.

4 The Reasons to Shift to a Multiple Species Approach

While we do not advocate abandoning the ESA, we strongly believe that other and often better tools are needed for prioritizing areas for conservation, because of several constraints that are present when depending on listing and protecting individual species. Modern approaches that take into account the full suite of species is an important step forward. Many concerns with single-species approaches were identified in putting together one of the largest of the habitat conservation plans (HCP), the Western Riverside County Multiple Species Habitat Conservation Plan (WRC-MSHCP), in southern California beginning in the late 1990s.

4.1 Lack of Distributional Knowledge

Many named species are only rarely found, but are they truly rare and in need of protection, or simply have not been looked for adequately? Distributional data requires extensive surveys independently through multiple simultaneous efforts. These data are crucial for a realistic estimate of the impact of take on a taxon (Kareiva et al. 1999). But obtaining adequate data (as per Kareiva et al. 1999; Rahn et al. 2006), is constrained both legally and temporally. Trespassing on private land in many countries, even for survey of potential species of concern, is illegal. Obtaining existing data records is challenging. For example, for species of interest in the WRC-MSHCP, Thomas Scott and a legion of students photocopied every survey throughout city and county offices to identify records of observations. Allen and postdocs queried museums for records locally to internationally. John Rotenberry and his lab created niche models where adequate data existed, to identify potential critical lands and to facilitate follow-up surveys where possible. Despite this effort, involving tens of conservation biologists, there were never enough data.

Some organisms are likely undergoing extinction but never reach a protected level of concern. Microorganisms are especially sensitive to this caveat, yet they carry on virtually every ecosystem process on Earth. Small organisms, including fungi, many of whom have macro-organismal fruiting structures (mushrooms), are challenging for protection in this regard (Raphael and Molina 2007). A few taxa, such as Boletus rhodopurpureus, a species existing only in older oak and beech stands in Eastern Europe, are well enough described to have obtained protection. In another case, Rhizopogon brunsii, a recently described southern California species, shows a limited range (Grubisha et al. 2005) and appears to be sensitive to nitrogen deposition and fertilization (Sirajuddin 2009). Another species, Rhizopogon mengei (Allen et al. 1999) was found in two locations, central California and southern California, with an unexpected host (Adenostoma fasciculatum), being usually found in association with conifers. It also has apparently only been found in the mid-1990s, during a series of wet years (warming ENSO signal). Species of Rhizopogon are important food sources for many small mammals and are critical in the recovery of ecosystems from fire (Glassman et al. 2016). In these cases, all of these collections have been found in protected locations, either research natural areas or as protected watersheds. How many such species have we completely missed elsewhere?

4.2 Political Constraints

There are numerous political constraints to listings. In part, this comes from current land management activities, and in part from projected needs. Because of political sensitivity, both the numbers of listings and the time scale for determinations have become far too long for efficient protection, with status reviews taking years to decades. As an example, we note the cases of the California Spotted Owl, Strix occidentalis occidentalis and one of its prey, the San Bernardino Flying Squirrel, Glaucomys sabrinus californicus. Both were listed as taxa of concern in the WRC-MSHCP in 2004. The range of both species includes the southern Sierras, the Transverse Ranges, and Mount San Jacinto down the Cuyumaca Mountains. In 2010, the Center for Biological Diversity proposed listing the San Bernardino Flying Squirrel (https://www.biologicaldiversity.org/species/mammals/San_Bernardino_flying_squirrel/endangered_species_act_profile.html). In 2012, the FWS reported a positive finding. But, in 2016 FWS reported that this species does not require protection under the ESA. The California Spotted Owl was proposed for listing in 2000. In 2012, this review resulted in a ruling that protection might be warranted. A review was initiated in 2015. In 2019, the FWS finding was that protection was not warranted. Their persistence is dependent on existing habitat supporting these taxa. The persistence of these taxa in some areas may be susceptible to factors that were not considered over the long review period. We will return to this system later.

4.3 Dynamic Distributions

Distributions are dynamic. But critical habitat locations are determined based on surveys, often at one or a few points in time. Critically, the “no surprises” rule provides that no new funds or land be required once approval is granted. This rule constrains new data, and even concepts. The impacts of climate change, disease, and air pollution were rarely documented for species of concern by the late twentieth century. Thus, conservation plans are largely static. In a few cases, changes can be documented in spatial dispersion through time, and as weather and vegetation change. For example, between 2004, when the western Riverside County Multiple Species Habitat Conservation (WRC-MSHCP) was signed, and 2012, following severe drought, the suitable habitat of California gnatcatcher Polioptila californica, shifted upward in elevation, oftentimes moving from protected lands into unprotected landscapes (Van Tassel et al. 2017). Across the longer time frames of many plans (75 years for the WRC-MSHCP), climate change is emerging as a major challenge. The spatial distribution of the Quino checkerspot butterfly (Euphydryas editha quino) has spatially shifted from an almost exclusively coastal range, up into foothills and mountains, buffered from drought (Preston et al. 2012), and models incorporating climate change into distribution patterns suggest this taxon may need a different design than is currently reflected in the WRC-MSHCP (Preston et al. 2008).

Many species exhibit metapopulation dynamics. Only some of the habitat patches across a landscape or region are occupied at any one survey period. An example is the Desert Bighorn Sheep, Ovis canadensis nelsoni. The desert bighorn sheep occupy isolated mountain ranges that result from the expansion of the Great Basin and faulting resulting in a Basin and Range desert mountain pattern. This species moves from mountain range to mountain range occupying first this range, then that, depending upon the numbers and the nearly random patterns of individual rainstorms. Thus, the occupation of long-term suitable habitat patches is not predictable but across time, all are occupied at some point. Desert lowlands distributed between mountain ranges, is not habitat, but the sheep do cross while traveling between ranges for sex or chasing past rains (Bleich et al. 1990). What this means is that the desert bighorns require maintenance of unoccupied habitat and corridors across which to migrate to persist.

4.4 Corridors: Environmental Change, Variability, and Disease

Corridors, or pathways of suitable habitat, become crucial to sustaining viable populations of many species. Yet most "critical habitat" lands depend on occupancy observations or models for determination. The corridors for the desert bighorn can sometimes be identified, but often animals that are migrating between suitable mountain ranges are found far from predicted locations. Building in suitable unoccupied and corridor habitats is scientifically difficult and politically challenging, even using current climate condition models. As temperatures increase with climate change and precipitation patterns shift determination of critical habitat becomes even more challenging (e.g., Allen et al. 2014). Again, in the case of the desert bighorn, an epizootic pneumonia, likely introduced by contact with domestic sheep may be responsible for much of the population losses. The contacts occur not necessarily in protected core mountain habitats, but during movement through unprotected areas.

In some cases, perturbations remote from “critical habitat” may be crucial. Protecting the habitat directly occupied is likely inadequate for protection of the species. The sand inputs to maintain the large dunes necessary for persistence of the Coachella Valley fringe-toed lizard, Uma inornata, comes from the nearby little San Bernardino mountains, from large rainstorms washing sand onto the valley floor, followed by aeolian movement to the current habitat. Human urban and exurban developments between the protected point of the Joshua Tree National Park (JTNP) and the protected dunes occupied by this lizard determine the size and persistence of the dunes critical to population persistence (Barrows and Allen 2007).

In other cases, far-away land use sets up challenging conflicts. Large-scale solar developments are designed to reduce greenhouse CO₂ production and its offshoot- global warming. But these developments also require water for energy production and site maintenance (Allen and McHughen 2010), potentially far more than is sustainable for maintaining groundwater. Yet locations downstream of proposed solar developments (for groundwater flow) where groundwater emerges, at least part of the year, is critical for plants, including endangered taxa (e.g., the Amargosa niterwort, Nitrophila mohavensis and ash meadows gum plant, Grindelia fraxino-pratensis). Groundwater emerging in springs is critical as waypoints for the desert bighorn, and is affected both by solar development and by climate change. While the transition to renewable energy is probably critical for groundwater over the long term, over the short-term, water use could be devastating for individual endangered and threatened species (Hernandez et al. 2015, 2019).

In other cases, climate change, whether long-term or shorter perturbations such as decadal-scale drought, alter organisms upon which a species of concern depends. For an example, we can return to the California Spotted Owl. In southern California, this taxon depends upon the San Bernardino flying squirrel. A large portion of the squirrel's diet is comprised of truffle fungi. One of us has studied these fungi for three decades in this region (e.g., Allen et al. 2005). Molecular surveys show the truffle taxa such as Melanogaster, Hymenogaster, and Tuber, on the roots of oaks from the oak woodlands up to the subalpine regions. But sporocarps, upon which the flying squirrels feed, are formed only during years of high precipitation or in wetter habitats such as high elevation regions of the San Bernardino Mountains and Orange County. The connecting populations of the spotted owl through the San Jacinto Mountains were found at 14 survey points (Biological Monitoring Program 2014, <https://www.wrc-rca.org/about-rca/monitoring/> , iNaturalist, <http://flyingsquirrels.sdnhm.org/>), at the higher elevation locations of the San Jacinto Mountains. However, they were not found in the Santa Ana Mountains or the southern San Bernardino Mountains bioregion. What happens, as extreme drought conditions increase and forest fires increase, remains unknown. Without corridors for species to move, and as protected habitat declines in quality and area, populations of taxa of concern will necessarily decline. Do these populations become examples of sky islands, where taxa slowly wink out with global warming? If so, how can the ESA protect critical habitat?

In summary, critical habitat for the protection of species of concern entails far more than identification of lands upon which a taxon is found at the time of determination, and takes far too much time and expense for current endangered species regulations. Furthermore, only rarely do we really know a species well enough to know where all it fits within the broader ecosystem and food chain structure, necessary for the persistence of that taxon and all others dependent upon it or upon whom it depends. The interconnections are simply too numerous and biodiversity too interdependent to focus only on specific taxa. We need instead in this crisis to shift our focus to a landscape perspective, looking at all biodiversity at once in an evolutionary context, using quantitative and spatially-explicit methods.

5 Advantages of a Multiple Species Planning Process

The end of the twentieth century and the dawn of the twenty-first century brings the opportunity to rethink the needs and mechanisms for approaching conservation. In the face of the current mass extinction wave, climate change, and bureaucratic lethargy, a single taxon approach, even when coupled into HCPs, will not overcome the biodiversity crisis. There were multiple calls for individual species protections in Riverside County. Even had those locations been set aside, a large number of taxa would have been extirpated between the initial planning and today. Moreover, a wide range of individual taxa in phyla from birds and mammals to fungi to microbes, would have already disappeared. As of this writing, the WRC-MSHCP has acquired approximately 82% of its land protection goal (https://www.wrc-rca.org/about-rca/newsletter/).

Importantly, both our principles of taxonomy and of land preservation precede the concept of evolution. The concept of NCCPs and MSHCPs arose at the same time when the Long-Term Ecological Research began to think beyond single site experiments (the Cross-Site competition) and began to construct the continent-wide scale National Ecological Observatory Network (NEON). As part of our discussion, a need to protect not only individual species, but clades with a limited number of taxa where evolutionary processes can ensue, was formulated (AIBS 2004). Once there were many taxa within the Hominidae. If H. sapiens goes extinct, there are no other taxa that can emerge with a similar niche. Alternatively, if the polar bear, Ursus maritimus, disappears from northern Alaska, a hybrid between it and Ursus arctos horribilis, could well survive and reoccupy that niche in the next ice age. We need to re-think not just protecting current space occupied by threatened species, but the range wherein biodiversity is sustainable ecologically and evolutionarily.

In many regions of the US and globally, federally- and state-listed species are widely distributed (Fig. 8.1). If we plot the distributions of all of the species of concern, almost every potential development, from housing to roads would contain a likely distribution point (Fig. 8.2). The RAND corporation (Dixon et al. 2008) estimated that for the 173,371 acres that are not under protection by other agencies (450,000 acres), the cost to protect them would be $5055 million. Allen estimated in 2003 that purchasing the parcels with known occupancy for Federally or State-listed species would be $5699 M. Moreover, based on modeled distributions that would include lands not yet surveyed, the cost for the eight federally-listed species alone would exceed $16,000 M. Thus, an MSHCP is fiscally prudent.

Fig. 8.1

Known spatial distribution of federally and state listed endangered species within the Western Riverside County multiple species habitat conservation plan area. Data mapped from known points compiled by the University of California-Riverside Center for Conservation Biology

Fig. 8.2

Known spatial distribution of species of concern identified during the planning process within the Western Riverside County multiple species habitat conservation plan area. Data mapped from known points compiled by the University of California-Riverside Center for Conservation Biology

5.1 Protecting Biodiversity Broadly Provides Multiple Ecosystem Services

Air and water quality benefit from the forests and native wildland and watersheds protected by habitat conservation plans such as the WRC MSHCP. Atmospheric CO₂ is also reduced by maintaining lands for biodiversity instead of development. For example, native vegetation protected under the WRC MSHCP sequesters between 59,000 and 175,000 (depending upon precipitation) tons of carbon annually. Using a $15/ton, market estimate, that means between $886,000 and $2.6 M worth of carbon (C) credits are provided. This compares with an estimated loss of 22,000 tons C per year directly, or up to 5,000,000 tons C per year indirect (water pumping, refineries, power plants, non-point source transportation) inputs to the atmosphere worth $75 M in carbon credits (Allen 2020). Habitat conservation plants are worth their costs.

5.2 Ecologically Effective Planning Incorporates Climate Change and Migration

The broader WRC-MSHCP coupled the federal MSHCP plan to the State of California NCCP (Natural Communities Conservation Protection) principles (Allen et al. 2003). Within this context, no taxon exists independently of its community. Indeed, one of the key approaches to understanding community ecology is embedded into impacts of the surrounding community on an individual organism (MacMahon et al. 1981, where a community is comprised of “The organisms which affect, directly or indirectly, the expected reproductive success of a reference organism.” By protecting communities, the breadth of biodiversity that contributes to the persistence of the taxon of concern, in theory, is protected. This protection entails two primary design concerns: design for persistence through perturbations, and persistence with change.

Persistence through perturbation is crucial, and often predictable. Drought, floods and fire, are all events that alter the dispersion of critical taxa and also the community of which they are a part. Going back to our earlier example, desert bighorn sheep persist as metapopulations, where small populations wink out of some mountain ranges, and move to nearby unoccupied ones dependent on the highly spatially unpredictable rainfall events. Thus, not only are both occupied and unoccupied core sites (or nodes using network theory terminology) necessary, but corridors (or linkages) between core sites must be conserved. In many cases, for taxa of concern, these are known, but not all. Understanding the natural history of biodiversity broadly becomes important.

Environmental changes poses a distinct challenge to taxon-based conservation, but can be addressed through predicted change analyses. Climate shift, pollution patterns, and exotic species are examples of threats imposed on a taxon approach to conservation. From our examples above, California gnatcatchers and Quino checkerspot butterflies are both examples of endangered taxa that are shifting their ranges (Preston et al. 2012; Van Tassel et al. 2017) in response to environmental change. While linkages (corridors) were integrated into the plan design, these are challenging for decision-makers to grasp and often the last elements to procure in a conservation plan. With and Crist (1995) noted that designing a conservation reserve with a low fractal dimension reduces the land area needed for conservation, allowing percolation of taxa across the landscape between nodes, and the WRC-MSHCP goal incorporated corridors expressly for this goal (Allen et al. 2003).

The California Spotted Owl is an example of the importance of community in protecting specific taxa. This taxon depends upon old-growth forest for nesting. Large, old-growth stands are sensitive to severe fires, that are increasingly common as a function of global climate change, Nitrogen (N) deposition, and stand densification. But the owl is also dependent upon the San Bernardino Flying Squirrel, and other small mammals that depend upon truffle and mushroom-producing fungi, that appear sensitive to drought and N deposition (see above discussion). Therefore, conserving the entire community from climate change and poor management practices remains a critical step for both taxon based and community-wide conservation.

At a broader scale, Jimenéz-Osornio et al. (2009) noted that Mexico maintains a widespread number of large reserves throughout the country. These include reserves across the Yucatán Peninsula comprising part of the MesoAmerican Biological Corridor Project, from Celestun to Ria Lagartos, and from Calakmul to Sian Ka'an, and linking down through Central America. To further link and sustain the high biodiversity of the region, they reported that both University-based Field Stations (e.g., the El Eden Ecological Reserve) and the local populace maintains multiple small community-scale reserves for many, if not most, of the local communities. These can be for religious observances, archeological sites, or simply rotational swidden agriculture. Together, these make a powerful network of large and small, interconnected networked suite of conserved lands resulting in a Regional Conservation Strategy. This strategy can include agroforestry lands, late seral forests, and even successional patches that support both taxa of concern and places for continued evolutionary processes. Just as importantly, many regions around the world have multiple conservation reserves supporting diverse elements from plants to animals, and even to fungi.

6 A Phylogenetic Approach to Biodiversity

Once we have made the step from single-species approaches to multi-species approaches, is there a way to add even more information for setting conservation priorities on the landscape? We argue that there is, by expanding the definition of biodiversity to include the phylogenetic relationships of all organisms in a spatial context, a field generally called spatial phylogenetics (Thornhill et al. 2016, 2017). The basic idea is to turn the tree of life into a GIS layer that can then be used with other layers in objective conservation assessments.

6.1 Phylogenetic Metrics of Biodiversity

This field is based on concepts that were largely initiated in Australia. Phylogenetic diversity (PD; Faith 1992) is the central metric of biodiversity used; it is defined as the sum of the branch lengths on the phylogeny connecting all organisms in a location. It is best expressed as a percent of the total phylogeny. In other words, if 12% of the branch length of an overarching phylogeny is located in a location, its PD is 0.12. Another important phylogenetic metric is phylogenetic endemism (PE, Rosauer et al. 2009); it is like PD but measured on a modified phylogeny where the topology is the same but each branch length on the phylogeny has been divided by its range size. Thus narrowly distributed branches contribute most to this metric, so a place with high PE has a lot of range-restricted branches. Two further metrics were developed while one of us (Mishler et al. 2014) was on sabbatical in Australia, relative phylogenetic diversity (RPD) and relative phylogenetic endemism (RPE). Both of these metrics are ratios comparing PD or PE measured using the observed tree, to PD or PE measured on a comparison tree where the topology is the same but each branch length is adjusted to be of equal length. Thus a location with high RPD (for example) contains branches that are longer than average.

In addition to these phylogenetic alpha diversity metrics, there is also a full suite of phylogenetic beta diversity (or turnover) metrics. These are similar to metrics used for species turnover (e.g., Sorenson and Jaccard indices) except that instead of shared and unshared species, the phylogenetic metrics use shared and unshared branches of the overarching phylogeny (Graham and Fine 2008). A pairwise matrix is built of all grid cells, then a clustering or ordination method is used to look at turnover patterns on the map.

A recent extension of both standard species-based and phylogeny-based turnover metrics (Laffan et al. 2016) takes into account the range-sizes of the species or lineages, thus applying a concept of relative endemism as described above for PE. The contribution of a species or lineage to the turnover score is inversely weighted by its range size; i.e., the smaller the range the larger the contribution. Turnover measured this way has been called range-weighted turnover, but it might more evocatively be called beta-endemism. Laffan et al. (2016) argued that this approach is better for several purposes, one of which is conservation evaluations (more below), since we are often concerned more with narrow-ranging taxa than with taxa that occur all over the map.

6.2 Statistical Tests

Mishler et al. (2014) also developed hypothesis tests based on a spatial randomization wherein the observed terminal taxon occurrences are randomly reassigned on the map, subject to two constraints: each grid cell maintains the same richness and each taxon retains the same range size (i.e., number of grid cells). Each of the phylogenetic metrics can be tested using the distribution resulting from many randomizations. For example, PD is tightly correlated with richness of terminal taxa in an area, since as you add more tips of the tree you necessarily add more branches. This would be particularly true if the taxa are co-occurring at random, representing the null hypothesis. Thus a grid cell that is significantly high in PD based on the randomization contains taxa that are more distantly related to each other than expected by chance (termed phylogenetic overdispersion; Webb et al. 2002). On the other hand, a grid cell that is significantly low in PD contains taxa that are more closely related to each other than expected by chance (termed phylogenetic clustering; Webb et al. 2002). Similarly, a grid cell that is significantly high in RPD contains branches that are significantly longer than average, while a grid cell that is significantly low in RPD contains branches that are significantly shorter than average. A particularly useful hypothesis test for conservation purposes is Catagorical Analysis of Neo- and Paleoendemism (CANAPE, Mishler et al. 2014). This is a two-step method to find centers of endemism and detect which are dominated by either neo- or paleoendemism. The first step is to locate cells that are significantly high (one-tailed test) in PE based on the randomization. The second step is to examine significance in RPE (two-tailed test) in those grids cells. A grid cell that is significantly high in RPE contains a concentration of range-restricted branches that are significantly longer than average (paleoendemism), while a grid cell that is significantly low in RPE contains a concentration of range-restricted branches that are significantly shorter than average (neoendemism).

6.3 Prioritizing Areas for Conservation

The metrics and statistical tests described above are, we argue, the best ways for characterizing biodiversity on the map. As compared to traditional spatial methods that simply use species richness and endemism as metrics, spatial phylogenetics adds a rich, evolutionary dimensionality to the picture. But while these methods are excellent descriptors of centers of diversity and endemism, some additional criteria need to be added for their application to conservation prioritization. Most important is the idea of complementarity (Justus and Sarkar 2002)—given what has been conserved so far, what is the maximum amount of currently unprotected biodiversity that can be protected by the next conservation action, then the next, and so on. In this way, conservation actions, often land acquisition but sometimes raising the protection status in management of existing reserves, can be prioritized to achieve maximum efficiency of time and money.

It can be seen that the turnover measures described above, particularly the range weighted version, are a critical part of the complementarity measurement. Kling et al (2018) used the California flora as a case study to develop the most sophisticated algorithm yet available to apply these criteria. They started with GIS layers for current protection status of land (using a novel quantitative scale instead of the usual binary yes/no), intactness of natural land cover (thus leaving out areas covered by urban development or agriculture), and biodiversity values (using the phylogenetic metrics described above). They then applied an algorithm addressing the question: Starting with the current protection status of the lands of California, what is the top priority grid cell to focus our next conservation efforts on, taking into account the presence of natural land cover and complementarity? This algorithm is applied iteratively; after the first action is take, the protection status and complementarity criteria are adjusted based on it, then the top priority for the second action is chosen, and so on. In this way, priority is given to poorly protected locations that have high intactness of natural land cover and high biodiversity value (i.e., contain many lineages that have small ranges and are not protected well elsewhere on the map). In summary, the overarching goal is to conserve as much of the phylogeny as possible. And to be efficient, actions are prioritized in order of how much they individually contribute to that goal.

Kling et al. (2018) further noted that the version of the phylogenetic tree that one uses to measure PD or PE gives different types of information each valuable for conservation consideration. They called these the facets of phylodiversity and suggested that each should be used separately with the algorithm described above. If one uses the topology where the branch lengths represent the inferred number of mutations (a phylogram) then PD measured on that tree is a good measure of genetic diversity in a region. If one uses a topology where the branch lengths have been scaled to time (a chronogram) then PD measured on that tree is a good measure of the amount of evolutionary survival time represented in a region. If one uses the topology where the branch lengths have been adjusted to all be the same length (a cladogram) then PD measured on that tree is a good measure of the net amount of diversification (speciation - extinction) represented in a region. Each facet gives a different yet important view into the history of the lineages in a place. In their case study of the California flora, Kling et al. (2018) looked at the prioritizations suggested by all three facets, and argued that the very top priority grid cells were ones that score high in all three.

This algorithm can be applied anywhere, on any scale, as long as there is a decent phylogeny of the organisms under consideration and good distributional information about the tips of the phylogeny. So far only applied to plants, it should be applied to animals as well, not to mention to microbes (see below). In addition, the algorithm should be extended beyond the factors that Kling et al. (2018) examined, for better priority setting, e.g., by adding GIS layers of land prices, threats from urban and agricultural trends, and predicted climate change.

The field of phylogenetic conservation biology is in its infancy and is worthy of intensive development to meet the current crises affecting biodiversity via land use changes, invasive species, and climate change. Including the history of biodiversity in conservation assessment helps us predict and assure its future.

6.4 Adding Microbes to the Mix

Microbial data, as for example gathered in metagenomic studies, is ideally suited for this phylogenetic approach, as species designations are particularly arbitrary and phylogenies readily available. This approach provides a means to include microbial groups when determining areas that are critical to protect. Today, most surveys of microbes, from Archea to fungi and nematodes, are based on DNA sequencing, not on morphological fruiting or feeding structures alone. The NEON program and many different studies, such as surveys on Mount St. Helens, are transitioning from morphological identification (Allen et al. 2018; Maltz et al. 2020), are undertaking wide-ranging assessments of microbial diversity. By studying particular perturbations, changes in phylogenetic metrics can be identified. For example, ectomycorrhizal (EM) fungi comprise a phylogenetically diverse suite of critical symbionts for trees. The different groups independently evolved, and each has a different suite of traits important to tree production and stress tolerance (Allen 2022). For example, in the San Bernardino Mountains, 145 different EM fungal taxa were sequenced (using the ITS region of the nuclear rRNA) from roots of Pinus ponderosa with different levels of N deposition and fertilization (Sirajuddin 2009). Some taxa were quite tolerant of N levels, such as the Thelephoraceae, a group well known for drought tolerance as well. Others, including taxa of Rhizopogon, a group known to be important in the mammal and owl food chain, and Russula, a common late seral taxon, virtually disappeared with N deposition or fertilization (Fig. 8.3). Protection of the fungal clades crucial for pines, flying squirrels, and spotted owls, by reducing air pollution, could play an important role for conserving biodiversity across the region.

Fig. 8.3

Ectomycorrhizal fungal site phylogeny and responses to N inputs (data from Sirajuddin (2009). Fungi were sequenced from ectomycorrhizal root tips of Pinus ponderosa in the San Bernardino Mountains USDA Forest Service research plots from the internal transcribed region of the nuclear rRNA. The blue clades are found only where N deposition was low, and no N fertilizer added

7 Synthesis and Summary: Integrating Evolutionary and Ecological Processes

Populations arise and some go extinct while others thrive—that is the essence of biodiversity. But mass extinction is of serious concern. While mass extinctions have occurred naturally in earth history, the current mass extinction is caused by the activity of one particular species, Homo sapiens. Given the current crisis and the urgent need to decide on conservation priorities immediately, probably the best approach to protecting biodiversity is not the protection of individual taxa one at a time. Instead, we have the tools to protect the geographic locations within which biodiversity as well as individual taxa of concern can persist and evolve. Biology is not static, but dynamic. Populations of organisms, communities in which they interact, and ecosystems in which they live, all change constantly. Ecosystems undergo climate change and change due to particular taxa.

To protect biodiversity, we must use all the tools we have to identify and protect landscapes that allow for future dynamics, not just the conditions of the past and present.

None of the approaches described above are mutually exclusive. We propose that the field should integrate the phylogenetic approach described above into reserve design built around multiple species habitat conservation plans (MSHCP), incorporating conservation principles of reserve design and ecosystem services (Allen et al. 2003). These approaches are cost effective, ecologically effective, and allow for evolutionary processes to continue supporting all biodiversity.

While protecting biodiversity, we are at the same time protecting ourselves. The emerging topic of ecosystem services clearly defines crucial benefits to humans for wildland protection. These include sequestering C, water purification, and pollutant mitigation. Much of the land managed by the US Forest Service in California was protected as a watershed for drinking water. Other recreation areas like the San Joaquin Wildlife Refuge is designed to use reclaimed water for wildlife, including species of special concern such as the White-faced ibis, a migratory species, and burrowing owls and tricolored blackbirds, around the large, seasonal wetland, Mystic Lake. Finally, protecting lands containing unique biodiversity maintains lands that sequester CO₂, as opposed to shifting these lands to developments that release greenhouse gases.

In summary, we gain as a species, biodiversity gains broadly, and we improve the stage for the future when we use all the tools, phylogenetics, ecology, and ecosystem services with emerging molecular and geospatial tools now at our call. Scientifically, we can certainly pivot; but can the political environment move as quickly?