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Home , Cycas edentata, Cycas rumphii, Cycas wadei, Zamia integrifolia, Zamia pumila

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Review Does Phytogeography Change with Shifts in Geopolitics? The Curious Case of in the United States

Benjamin E. Deloso 1 , Ulysses F. Ferreras 2 and Thomas E. Marler 1,*

1 Western Pacific Tropical Research Center, University of Guam, UOG Station, Mangilao, Guam 96923, USA; [email protected] 2 Philippine Native Conservation Society Inc., Ninoy Aquino Parks and Wildlife Center, Quezon City 1101, Philippines; [email protected] * Correspondence: [email protected]; Tel.: +1-671-735-2100

 Received: 23 October 2020; Accepted: 23 November 2020; Published: 25 November 2020 

Abstract: The United States is currently home to five native . We provide a discussion on these five cycad species to illuminate how evolutionary and geopolitical processes influence phytogeography and published checklists of threatened plants. The number of threatened species in need of protection within any given country is a product of speciation that is contingent with evolutionary processes. However, this number may change instantaneously along with shifting of geopolitical boundaries brought about by armed conflict between rival states and multilateral negotiations. There are five contemporary cycad species within the United States, and the various historical bilateral and multilateral agreements that have generated this list are reviewed. Three of these five cycad species are threatened and in need of urgent protection. A discussion on the history of United States cycads as a microcosm of worldwide conservation issues is presented, with a focus on how federal conservation endeavors of individual nations may influence the world’s biodiversity crisis.

Keywords: conservation science; cycad; Cycadaceae; Cycadales; ; Red List; United States; ;

1. Introduction Cycads are an ancient group of and are considered the most basal extant group of seed plants [1]. Often referred to as “living fossils”, recent research indicates the extant species of cycads are a result of evolutionary radiations occurring during the Miocene (23–5.3 MYA), although the crown group that constitutes the order Cycadales is much older, having split from Ginkgo in the late Permian (274.5 MYA) [2,3]. These contemporary 350+ species of cycads [4] are distributed among 10 accepted genera in 2 families. Among this expansive list, five extant cycad species are native to the United States and territories. The criteria required to define a species has been the subject of contention for many years since the founding of binomial by Carolus Linnaeus [5,6]. Indeed, there is no clear consensus among the scientific community on what defines a species. Taxonomists are constantly in disagreement on what characters merit more consideration in circumscribing and delimiting any given species. Despite subjective preferences, any discrete species can be considered distinct long before the taxonomic authority that formally described it existed. Linnaeus himself understood this concept when establishing the system of naming organisms so that humans could attempt to interpret the innumerable life forms on Earth and their relationships among each other. Our view herein is that the use of the term

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Diversity 2020, 12, x FOR PEER REVIEW 2 of 11 “new species” that precedes the formal description of each added binomial is an anthropocentric bias the use of the term “new species” that precedes the formal description of each added binomial is an and should be cautiously avoided [7]. In this review, we employ a distinction between actual taxa and anthropocentric bias and should be cautiously avoided [7]. In this review, we employ a distinction described taxa. between actual taxa and described taxa. The country in which each taxon resides may change when state boundaries are modified as an The country in which each taxon resides may change when state boundaries are modified as an offshootoffshoot of bilateral of bilateral and multilateral and multilateral negotiations. negotiations. Therefore, Therefore, the number the number of species of species that resides that reside withins a countrywithin during a country a specified during ayear specified may increase year may or increase decrease or along decrease with along these with geopolitical these geopolitical changes. This reviewchanges. describes This review the history describes of thethe botanicalhistory of and the geopoliticalbotanical and issues geopolitical related issues to the fiverelated cycad to the species five that currentlycycad species occur that in currently the United occur States. in the A thoroughUnited States review. A thorough of the history review of of cycad the history species of within cycad Unitedspecies States within territories United and States occupations territories would and be occupations an expansive would endeavor. be an For expansive example, endeavor. several cycad For speciesexample, would severalhave been cycad included species in would the unincorporated have been included territory in ofthe the unincorporated Panama Canal territory Zone and of the temporarilyPanama occupiedCanal Zone territories and the withintemporarily occupied following territories the Treaty within of Paris Cuba or Japanfollowing following the Treaty World of War II.Paris However, or Japan none following of these World species War are currently II. However, under none the of jurisdiction these species of the are United currently States. under For the purposesjurisdiction of simplicity of the United and brevity, States. we For restrict the purposes our endeavor of simplicity to the and history brevity, of events we restrict that our have endeavor created the fiveto the cycad history species of events that are that contemporary have created taxa the offive the cycad United species States. that are contemporary taxa of the United States. 2. The Contemporary Species of the United States 2. The Contemporary Species of the United States 2.1. L.f. 2.1. Zamia integrifolia L.f. This species is the only cycad native to the continental United States, ranging from southern toThis species with is fivethe subspeciesonly cycad currentlynative to the recognized continental [4]. United It was firstStates described, ranging in from 1789 southern by Carl von LinnGeorgiaé d. to y., Florida the son with of Carolus five subspecies Linnaeus. currently His name recognized latinized [4 is]. “ItLinnaeus was first filius described”, meaning in 178 Linnaeus9 by Carl the son,von and Linné the d. standard y., the author son of abbreviation Carolus Linnaeus. L.f. is His used name to indicate latinized him is as “Linnaeus the taxonomic filius”, authority. meaning In fact,Linnaeus the genus the Zamiason, andwas the named standard by author Linnaeus abbreviation himself, and L.f. thusis used the to naming indicate of him this as taxon the taxonomic could be describedauthority as a. fatherIn fact, and the genus son endeavor. Zamia was named by Linnaeus himself, and thus the naming of this taxon Locallycould be knowndescribed as as coontie, a father thisand son species endeavor. has had 17 synonyms, and prior to its most recent Locally known as coontie, this species has had 17 synonyms, and prior to its most recent circumscription was most recently known as Zamia floridana A.DC. [4]. The International Union for circumscription was most recently known as Zamia floridana A.DC. [4]. The International Union for Conservation of Nature (IUCN) currently gives this cycad a status of Near Threatened from the Conservation of Nature (IUCN) currently gives this cycad a status of Near Threatened from the latest latest assessment performed in 2009 by Dr. Dennis Stevenson, a world authority in cycad biology [8]. assessment performed in 2009 by Dr. Dennis Stevenson, a world authority in cycad biology [8]. Placement in this category means the species may be threatened with extinction in the near future, but Placement in this category means the species may be threatened with extinction in the near future, it doesbut not it does currently not currently qualify forqualify threatened for threatened status. status. ThisThis cycad cycad has ahas long a long history history of beingof being utilized utilized and and processed processed as as food-grade food-grade flour.flour. Unfortunately, entireentire plants plants were we excavatedre excavated for thisfor this purpose. purpose. The The peak peak production production years years were were in in the the latelate 1800s1800s andand earlyearly 1900s, 1900s an era, an thatera that decimated decimated the th wilde wild populations populations of of the the species species [9 [].9] The. The contemporary contemporary threatsthreats to Z.to integrifolia Z. integrifoliainclude include habitat habitat loss loss and and wild wild harvesting harvesting [8 ].[8]. The The showy showy small small plant isis anan excellentexcellent horticulturalhorticultural specimen specimen that that requires requires little little care care (Figure (Figure1a). 1a).

(a) (b)

FigureFigure 1. Two 1. T ofwo the of the cycad cycad species species native native to to the the United United States:States: ( (aa)) the the diminutive diminutive ZamiaZamia integrifolia integrifolia; (b); (b) thethe arborescent arborescentCycas micronesica..

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2.2. Zamia erosa O.F.Cook & G.N.Collins This cycad species is one of three taxa that are native to , being found on the northern coastal regions of the island. The taxon was described by Drs. Orator Fuller Cook and Guy N. Collins in 1903 [4]. The species is similar in appearance to Z. integrifolia but is distinguished by broader, apically erose-dentate leaflets, hence the name “erosa” [10]. The species is currently listed as Vulnerable by the IUCN following the most recent assessment in 2009 by Dr. Dennis Stevenson [11]. Placement in this category means the taxon is likely to be upgraded to Endangered status in the future unless the underlying threats to the wild populations are mitigated. The primary threats for this taxon are conversion of habitat to agriculture and construction of roads and railroads within its native habitat. A recent study indicated that Z. erosa may have originated from a separate colonization event from the other two Zamia taxa on the island due to allopatric speciation [12].

2.3. L. This cycad taxon has an indigenous range that includes Cuba, the , and Puerto Rico [4]. Originally described by Linnaeus himself, this is the type species for the genus Zamia, meaning it was the first species described for the genus. This species was originally thought to be one large, widespread, polymorphic species but recent research has confirmed that other cycad populations in the Caribbean are indeed different species and that the true Z. pumila is restricted to only three islands. The narrow range of Z. pumila in Puerto Rico increases the threat level, especially in consideration of habitat conversion. However, the species is listed as Near Threatened as of a 2009 assessment [13] as a result of the indigenous range including several islands. We contend that its threat status as a United States cycad species is acute due to the limited geographic range in Puerto Rico.

2.4. Zamia portoricensis Urb. The third United States taxon found only in Puerto Rico is located in the southwestern region of the island in the Susua State region. Known locally as marunguey, the species was formally described in 1899 by Ignatz Urban, a German botanist known for his contributions to the flora of the Caribbean and Brazil. It is currently classified as Endangered by the IUCN, with the most recent assessment performed in 2009 by Dr. Dennis Stevenson [14]. Placement in this category means the species is at a high risk of extinction in the future. The main threats to this species have been overcollection for the nursery trade, habitat degradation, and limited regeneration from the possible loss of the native pollinator [14].

2.5. Cycas micronesica K.D.Hill This arborescent Cycas species is the only cycad species native to the United States Territory of Guam and United States Commonwealth of the Northern Mariana Islands, with the indigenous range encompassing three island groups within four geopolitical boundaries [4,15]. It was previously lumped with L., but taxonomic revisions established this species as distinct [16]. Thus, the species was described by Dr. Ken Hill, an established Australian botanist, in 1994. One of the defining characteristics of this species, locally known as fadang, is the smooth devoid of spines; thus, many consider it a “user friendly” cycad. This species is a member of a complex that produces seeds that float, enabling oceanic seed dispersal. As a result, much of the areas of occupancy are coastal habitats (Figure1b). This cycad species is currently classified as Endangered by the IUCN, with the most recent assessment performed in 2009 by Thomas Marler, Jody Haynes, and Anders Lindström [15]. The species was added to the United States Endangered Species Act (US-ESA) in 2015 as Threatened [17]. As recently as 2002, the species was the most abundant tree species on the island of Guam [18]. The primary reason Diversity 2020, 12, 445 4 of 11 for the widespread mortality was the recent invasion of several specialist herbivores [19,20]. Such a drastic change in the threat status of a cycad species within such a short timeline has perhaps not been documented anywhere else in the world. The species remains at risk of extinction in the future in two of the four geopolitical regions it inhabits, both of which are under the jurisdiction of the United States. The University of Guam, the affiliation for two of the authors, is uniquely positioned within the native habitat for this cycad, with in situ plants existing on the institution’s property. As the only member of the genus Cycas that inhabits contemporary United States lands, conservation of this species is of paramount importance. The potential extinction of C. micronesica from United States lands would restrict the cycads native to the United States to the genus Zamia.

3. The Addition of Guam, the Philippines, and Puerto Rico The number of distinct cycad species under the unambiguous jurisdiction of the United States has changed due to consistent engagement in great power competition and militarist, territorial expansion more so than due to plant migration and evolution. When the Declaration of Independence was signed to formalize the establishment of the United States, the country was the natural habitat of Z. integrifolia, a single species in the southeast part of the continent (Table1). The states within which this cycad species resided were among the states that seceded in 1861 with the establishment of the Confederated States of America (CSA) [21]. This act of secession was never recognized by the United States or any foreign nation, and the CSA capitulated with the end of the Civil War in 1865. One could argue that Z. integrifolia was removed from the United States from 1861 to 1865, or from 1861 to 1868 when the post-war court cases and amnesty negotiations culminated.

Table1. The contemporary cycad species within the United States as influenced by historical treaties/accords.

Year of Change Number Described Taxa Number Actual Taxa Reason for Change <1776 0 0 1776 0 1 Declaration of Independence 1789 1 1 Zamia integrifolia described 1861 0 0 Confederates States of America 1865 1 1 Capitulation of CSA 1899 4 16 Treaty of Paris 1899 5 16 Zamia portoricensis described 1903 6 16 Zamia erosa described 1936 7 16 Cycas wadei described 1946 5 5 Treaty of Manila

The final stages of the Spanish–American War culminated in the signing of the Treaty of Paris in 1898, granting the United States possession of Guam, the Philippines, and Puerto Rico [22]. The treaty was formally adopted by both nations in 1899 [23], with all accompanying biodiversity being brought under the jurisdiction of the United States. Many historians consider this era as the end of Spanish imperialism ushering into world affairs the United States as the leading global hegemon. On the basis of current understanding, Puerto Rico is known to possess three distinct cycad taxa, Guam possesses a single taxon, and the Philippines possesses 11 taxa. Therefore, one of the unanticipated consequences of the Treaty of Paris was the artificial increase of the number of known cycad taxa within the United States from 1 to 16. Only three of these extra-continental taxa were described at the time, and thus the number of described cycad taxa within the United States increased from one to four in 1899. In that same year, Z. portoricensis was described; then, in 1903, Z. erosa was described. These discoveries increased the number of described taxa within the United States to six. In 1936, Cycas wadei Merrill was described from the Philippines, increasing the number of described taxa within the United States and its acquired territories to seven. Diversity 2020, 12, 445 5 of 11

The inhabitants of the three former Spanish colonies responded to the American occupation in a highly contrasting manner. The location of Puerto Rico did not fulfill strategic aims of the United States at that time, and thus the relationship with the United States has been relatively benign. The official relationship is described as a quasi-autonomous commonwealth under United States sovereignty [22]. In contrast, Guam’s location was of critical importance for power projection in the Pacific and regional hegemons in Asia, and thus the relationship to date has been anything but benign. The United States Department of the Navy stifled all efforts to formalize the relationship up until 1950, when the island officially became an unincorporated territory [23], a status that remains in force up to the present [24]. A great expanse of the private land area was expropriated as federal property during and following World War II, and many of these lands contained dense populations of C. micronesica. Of the three territories, the Philippines resisted the colonial standing with the most force and at the cost of human lives, and as a result, the United States concurred with the country’s independence after four decades. The onset of World War II postponed the official designation of independence, which was granted in 1946 with the Treaty of Manila (Table1). Most of the valid species descriptions within the Philippines occurred after 1946, and thus the number of described cycad species within the United States did not increase after 1936 when C. wadei was described, and then declined to five when the Philippines became independent.

4. Taxonomic Revisions Abound Nomenclatural changes that accompany taxonomic revisions of recognized taxa occur periodically to accommodate rapid advances in DNA sequencing and enhanced morphological understanding. All five of the contemporary United States cycad species provide examples of how these revisions can change the binomial that is assigned to a taxon. All four Zamia species within the United States had been previously lumped under Z. pumila, which for a long time was thought to be one highly polymorphic species encompassing all cycad populations found in Florida and the Caribbean [12]. In light of new genetic and morphological evidence, the cycad populations in these regions are now treated as separate species with the name Z. pumila retained but circumscribed only for one taxon with areas of occupancy on several Caribbean islands [25]. The Guam cycad species claims a similar history, formerly among the many cycad taxa that were lumped together under Cycas circinalis L. The type specimen that Linnaeus originally used to describe the genus Cycas was actually from a population that we now know has a restrictive endemic range in Southern . This endemic taxon is regarded as the true C. circinalis. The Guam cycad is among many that have been recognized as separate species in response to new morphological and molecular knowledge. The Guam and Philippine species that were formerly lumped with C. circinalis are now known as C. micronesica, Cycas edentata de Laub., and Cycas nitida K.D.Hill & A.Lindstr. [15,26]. The complications arising from recent taxonomic changes does not exempt continental United States cycads. As an example, the list of names that have been assigned to Florida’s cycad taxon is unusually long and taxonomically superfluous [4]. Zamia integrifolia emerges as a quintessential model for the need to record precise locality when biologists collect living plants and herbarium specimens. When ex situ plants and herbarium-vouchered specimens are stored with this precise geospatial data, taxonomists are provisioned with the information they need to clarify taxonomic revisions repetitively with accuracy.

5. The Philippine Taxa Diversity of Cycas within the Philippine islands is substantial, and the taxonomic revisions have been likewise confusing. Unlike other diverse regions where local radiations are evident, the diversity of the genus in the Philippines is largely due to disparate founding events and probable crustal rifting that brought continental biota to Palawan Province. The comprehensive descriptions of the Diversity 2020, 12, 445 6 of 11

Philippines Cycas prior to 2008 [27–30] included binomials and species separations that do not conform to contemporary knowledge, with the exception of C. wadei. The taxa that were identified prior to 2005 are currently described as Cycas curranii (J.Schust.) K.D.Hill, C. edentata, Cycas riuminiana Porte ex Regel, and C. wadei [26]. Cycas zambalensis Madulid & Agoo was described in 2005 [31]. Cycas aenigma K.D.Hill & A. Lindstr., C. nitida, Cycas saxatilis K.D.Hill & A. Lindstr., Cycas vespertilio A.J.Lindstr. & K.D.Hill, and Cycas lacrimans A.J.Lindstr. & K.D.Hill were described in 2008 [26]. Cycas sancti-lasallei Agoo & Madulid was described in 2012 [32]. Ongoing field work has identified more populations that are distinct on the basis of traditional morphological characters, and these plant populations are awaiting molecular analyses prior to description. These 11 distinct taxa were under the jurisdiction of the United States for more than four decades as a result of the same treaty that added Guam and Puerto Rico. If the bilateral Treaty of Manila had not granted the Philippines independence, all of them would be eligible for protection under the US-ESA and their contemporary conservation would be endorsed by the United States Fish and Wildlife Service (USFWS).

6. Potential Changes Three possible developments may change the list of cycad species native to the United States.

6.1. Change in Status for Guam or Puerto Rico The first potential development that may change United States cycads is if either Guam or Puerto Rico is granted independence. Historically, the United States has been more interested in preserving the status quo, and independence will not occur without a strong and organized independence movement supported by the majority from within these territories. The United Nations lists Guam as one among 17 non-self-governing territories remaining throughout the world [24]. The sustained territorial status of these insular colonies is arguably inconsistent with the principles of the United States Constitution and disregards the United States’ various international treaty commitments [22]. Four of the five cycad species described herein are useful for illuminating the fact that the United States and other members of the United Nations have pledged to active pursuit of decolonization by assisting peoples from non-self-governing territories in developing self-governance [33]. A recent example of how geopolitics affects the native range of a plant species is the independence of South Sudan in 2011 [34]. The endemic ranges of Encephalartos septentrionalis Schweinf. and Encephalartos mackenziei L.E.Newton were listed to occur exclusively in Sudan prior to 2011, but are exclusively within South Sudan at present [4]. The endemic range was not displaced, instead, the boundaries of accepted countries changed around the plants, along with a new federal government leading all conservation decisions for the entire endemic range of the species.

6.2. Taxonomic Revision The second development that may potentially impact the list of cycads in the United States is any forthcoming taxonomic revisions that focus on the Zamia populations within Puerto Rico and the continental United States. The number of described species may decrease if two or more of the four described species are lumped into one taxon. Contrarily, the number of described species may increase if some of the verifiable Z. integrifolia subspecies are elevated to species level. This taxonomic state of flux has been identified as a limitation that complicates the full appreciation of the IUCN Red List and the ability of state governments to utilize the IUCN information [35,36].

6.3. Local Extinction The third development that may alter the status of United States cycads is continued local extirpations that could lead to extinction of one or more taxa from United States lands. Unfortunately, the four United States Zamia species are not afforded any level of protection under the US-ESA. A formal Diversity 2020, 12, 445 7 of 11 assessment of Z. portoricensis is especially warranted, as this species occurs at a single location and has been listed as Endangered or Critically Endangered under the IUCN Red List since 2003 [14]. Cycas micronesica is the species that is at greatest risk of extinction within United States lands. When C. micronesica was formally listed on the US-ESA, the long history of funding allocated for international experts for conservation projects was abandoned and a shift in funding approaches ensued, which excluded species experts from conservation decisions and actions [37]. This history has caused recent consequential conservation mistakes as a result of the elimination of appropriate expertise from the management decisions [37–39]. During the five years after the formal listing of C. micronesica on the US-ESA, 36% mortality of the 2015 cycad population has occurred [20]. A copious amount of federal funding has been directed toward tree salvage from federal construction sites and transplantation to restoration sites during those same years. The primary threat for Guam’s cycad population is a consortium of native and non-native herbivores [37,40]. The publicly funded salvage projects have not addressed these acute biological threats in any capacity. In contrast, they may have exacerbated the threats at the local scale by transplanting unhealthy trees with compromised resistance to the ubiquitous insect herbivores into new areas. For example, Acalolepta marianarum Aurivillius (synonym = Dihammus marianarum Aurivillius) is the only native insect herbivore that is among the acute threats to the cycad populations in Guam [41]. The incidence of damage to C. micronesica stems by this stem borer increased dramatically following the added stress associated with tree excavation and transplantation (T.E.M., personal observations). Therefore, the conservation actions directly magnified the biological threats to the plant populations in and nearby the recipient restoration sites. This was particularly ill-conceived because the main recipient site for the transplants was positioned in the same area of occupancy with a permanent in situ conservation plot that was publicly funded to conserve the cycad genetic diversity in the area. Therefore, the transplantation recipient site became a brood site that directly threatened a previous conservation project by increasing the stem borer population in the area of occupancy. A 2017 conservation overview published by two of the recognized international experts for this taxon pointed out the need to use isolated recipient sites for salvaged trees as a means of avoiding any negative influences of the restoration site on nearby conspecific individuals [42]. Of the five original in situ plots that were constructed in 2013, this is the second plot that has been directly damaged by subsequent publicly funded projects. One other in situ plot that was positioned by a federal biologist was partially destroyed by military construction of a live fire range only 6 years after the cycad conservation plot was established, wasting the successful outcomes of 6 years of public funding for cycad conservation. Continued exclusion of international species expertise into the future will likely ensure continued missteps and minimal successes in mitigating the consequential threats to this unique species on the islands of Guam and Rota.

7. Transnational Distribution and Conservation The shifting of country borders often results in the changing of a taxon’s range to a different number of jurisdictions, and C. micronesica serves as an example. The northern limit of this taxon is the island of Rota in the Mariana Island Archipelago, while the southern limits are the islands that form the Palau Archipelago. Recent geopolitical developments had extended the indigenous range of the cycad taxon into the two political entities of Guam and the Trust Territory of the Pacific Islands when the areas of occupancy in Rota, Yap, and Palau were all placed under the Trust Territory in 1947 [43]. The areas of occupancy on Rota were removed from this status in 1978 when the Commonwealth of the Northern Mariana Islands was established [44], revising the indigenous range of the plant species into three political entities. The areas of occupancy in Yap were delisted from the Trust Territory status in 1979 when the Federated States of Micronesia was formed [45]. Finally, Palau became an independent country in 1994 [46]. Therefore, the indigenous range of this cycad species includes a United States Commonwealth (Rota), a United States Unincorporated Territory (Guam), the Federated States of Micronesia (Yap), and the Republic of Palau. The plant population of this taxon has not migrated, but Diversity 2020, 12, 445 8 of 11 the geopolitics of its home range has changed the national boundaries of its long-established areas of occupancy. The impact of these boundary and status rearrangements on conservation may be profound. For example, the level of protection provided by federal or local conservation regulations may be highly variable among different nations. Moreover, the devotion of federal conservation agents to respect international expert knowledge may influence national conservation policies, with nations embracing the need for species expertise better able to marshal resources to foster greater conservation successes. Federal rules that govern activities of non-citizens and the volume of international travel may also greatly affect tree conservation among insular habitats. For example, the number of visitor arrivals in Palau and Yap is minimal compared with arrivals in Guam. Visitors may enter and conduct observational research in forest habitat in Guam without a federal permit, but this is not allowed in Palau or Yap. The in situ areas of occupancy of C. micronesica in Palau are located in isolated islands with controlled access strictly enforced, thereby reducing the risk of inadvertent introduction of invasive species. The United States citizens living on Guam or Rota are not allowed to be involved in selection of the president or voting representatives in federal legislative bodies. However, they are required to abide by federal conservation policies and regulations created by these elected national leaders, bend to the oversight of federal agencies such as the USFWS and Environmental Protection Agency, and conform to the conservation agenda of federal agents who are empowered with public funds to create the programs for managing terrestrial resources on their islands. This form of disenfranchisement of conservation stakeholder citizens residing in the islands of Palau and Yap is not tolerated by those two federal governments, allowing their C. micronesica localities to be conserved with a collectivist, inclusive philosophy. Finally, the veracity of conservation ethos among citizens may contrast sharply among different nations. These and other differences among diverse nations may directly influence localized conservation successes of a tree species that spans multiple national boundaries.

8. The United States Is a Microcosm of the World These five contemporary cycad taxa of the United States provide a microcosm of biodiversity conservation worldwide. For example, all five species evolved mutualisms with insect pollinator species [1,47–50]. These cycads provide a clarion call for conservation actions designed to conserve the mutualisms as an approach for conserving each of the species. Moreover, the global threats of co-extinctions are illuminated by these cycad mutualisms. Three of the five taxa discussed in this review are listed in a threatened category by the IUCN Red List [11,14,15]. This percentage is remarkably similar to the recent assessments that 63% of ≈ all cycads are listed in a threatened category by the IUCN [36,51]. As threats to global biodiversity strengthen and magnify, extinction risk estimations of cycads and other plants increase in importance for informing conservation stratagems [52–54]. The IUCN approach for assessments is perhaps the most efficacious tool for quantifying the risk of extinction at the global scale [55]. This is partly because federal conservation assessments within each individual country do not include data from other countries in which a native species exists. This is also because specialist groups composed of generalist experts oversee the IUCN assessments and the actual assessors are specialist experts. This approach exemplifies analogies to the peer review system of the primary literature, where section editors that oversee the process of journals are generalist international experts and individual reviewers that determine accuracy and quality of a manuscript are specialist international experts. The cycads of the United States also exemplify the greatest worldwide threats to biodiversity. For example, one of the greatest global threats to in situ cycads is habitat loss. All five United States species are losing habitat at rapid rates because of human conversion of forested hectarage. A second international threat to cycad biodiversity is wild harvesting of plants. All four of the Zamia species within the United States suffer from this threat [8,11,13,14]. The declines in global biodiversity are also partly a consequence of invasive species, and C. micronesica provides an example of this acute threat [19,20,40]. As more invasive species become established throughout the world during global Diversity 2020, 12, 445 9 of 11 change, this United States cycad species emerges as a model for studying the successes and failures of conservation actions implemented by the empowered decision-makers.

Author Contributions: Conceptualization, T.E.M.; writing—original draft preparation, B.E.D. and T.E.M.; writing—review and editing, U.F.F. All authors have read and agreed to the published version of the manuscript. Funding: This research received no external funding. Acknowledgments: We thank Michael Calonje, Leonardo Co, Patrick Griffith, Chip Jones, Anders Lindström, Darin Penneys, William Tang, Irene Terry, and others for thought-provoking discussions about cycad biology, evolution, and taxonomy. Conflicts of Interest: The authors declare no conflict of interest.

References

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