Galapagos Giant Tortoises

By Academic Press

Galapagos Giant Tortoises brings together researchers and conservationists to share the most up-to-date knowledge of Galapagos giant tortoises. Despite being icons of the world-famous Galapagos Archipelago and the target of more than 50 years of conservation research and management, Galapagos giant tortoise evolution and much of their ecology remained unknown until recently. This book documents the history, the pressing conservation issues, and success stories recovering several of the 15 different species of Galapagos tortoises from near extinction.The book begins with an overview of the history of the relationship between humans and Galapagos giant tortoises, starting from initial heavy exploitation of tortoises by pirates and whalers, and extending to the start of the modern conservation era in the 1960s. The book then shifts to biology, describing Galapagos tortoise evolution, taxonomy, ecology, habitats, reproduction, and behavior. Next the decades of conservation efforts and their results are reviewed, including issues of captive breeding, invasive species, introduced diseases, and de-extinction, as well as the current status and distribution of every species. The final portion of the book turns to four case studies of restoration, and then looks ahead to the future of all tortoise populations.The latest volume in the Biodiversity of the World: Conservation from Genes to Landscape series, Galapagos Giant Tortoises is a valuable resource for researchers and conservationists, as well as students of biology, wildlife conservation, and herpetology.

• Provides a comprehensive overview of the Galapagos giant tortoise species as written and edited by the world’s leading experts
• Presents examples of restoration of tortoise populations following the near extinction of many of them
• Describes conservation strategies to ensure the full recovery of all extant species
• Explores recent efforts using replacement tortoises for extinct species to restore island ecosystems

• Language: English
• Publisher: Academic Press
• Release date: Nov 7, 2020
• ISBN: 9780128175552

Book preview

chapter.

Section I

Overview

Outline

Chapter 1 The Galapagos: Island home of giant tortoises

Chapter 2 Galapagos tortoises: Protagonists in the spectacle of life on Earth

Chapter 1

The Galapagos: Island home of giant tortoises

Jack Frazier,    Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, D.C., United States

Abstract

Galapagos is at once inspiring and disheartening, given its complex history of discovery, exploration, overexploitation, colonization, extinctions, conservation challenges, and successes. Galapagos giant tortoises are central to each of these phases and developments. While suffering overexploitation and species loss, Galapagos tortoises are also the focus of dedicated, innovative efforts to restore these imperiled species and the ecosystems they inhabit. All told, Galapagos, and its tortoises, provide a microcosm of life on Earth, and the roles that humans play.

Keywords

Captive breeding; exploitation; genetics; Galapagos; habitat destruction; history; invasive species; overexploitation; restoration; threats; tortoise; tourism

Chapter outline

Outline

Putting Galapagos on the map 3

Darwin’s Great tortoises of the Galapagos: Phylogeny, taxonomy, and nomenclature 5

The history and status of Galapagos tortoises 6

Threats to Galapagos, the tortoises, and more 9

Introduced species: An early and increasing threat 9

Environmental change and habitat degradation 10

Reduced genetic diversity 11

Poaching and illegal trade 11

Tourism and affiliated issues 12

Conservation successes over the last 60 years 12

References 13

On March 10, 1535, after drifting west for 6 days from the coast of South America, the Bishop of Panama arrived at unknown islands. In recounting his discovery, Fray de Berlanga described enormous tortoises …galápagos tan grandes, que llevaba cada uno un ombre encima… […tortoises so great, that they {could carry} a man on top…] (de Berlanga 1884[1535]: 539), thus christening the toponym for which the islands would become known.

The history of Galapagos, one of the last archipelagoes discovered by humans, is romantic and inspiring, yet also tragic and disheartening, with tortoises interwoven throughout this complex saga. Before, and after, annexation by the Republic of Ecuador in 1832, the Archipelago was a renowned refuge for pirates, buccaneers, whalers, sealers, and tortoise oilers. Galapagos has also been a prime destination for adventurers, explorers, and naturalists, including Charles Darwin; and over the years ever more colonists, scientists, and tourists arrived. Central to these diverse travelers, from pirates to tourists, were the tortoises, sources of fresh meat, trade, livelihoods, wonder, and inspiration. This chapter gives an overview of the Galapagos tortoises in their island home, announcing subsequent chapters that delve into details about these chelonians and the extensive efforts to conserve and protect them and restore their populations.

Putting Galapagos on the map

Pre-Columbian maritime voyages occurred along the Pacific coast of the Americas (e.g., Anderson et al. 2016; Callaghan 2003; Dewan and Hosler 2008; Urban 2018). Yet, despite recurrent claims about pre-Columbian peoples reaching, even colonizing, Galapagos (e.g., Finnley 1966; Heyerdahl 1955; Heyerdahl and Skjölsvold 1956; Lothrop 1957), including legends of Inca Tupac Yupanqui conquering the Islands in the late 1400s (e.g., Clissold 1954: 79; Markham 1907: 135–137; McEwan 2006: 208, 217), there is no scientific evidence of any pre-Columbian presence on Galapagos (e.g., Anderson et al. 2016; Froyd et al. 2010). Nor is there any merit in an early 1500s account of a Spanish conquest of the Galapagos, circulated 19 years before the first recorded visit to the islands (Stahl et al. 2020: 14). The earliest cartographic evidence appears in the first world atlas, which listed ye [=islas] de los galopegos, meaning islands of the tortoises, located just north of the equator and some 14 degrees longitude west of South America (Ortelius 1570: folio 2; Fig. 3.1 in Chapter 3: Perceptions). The 17th-century British buccaneer William Ambrose Crowley produced the first known chart of the Archipelago in 1684, which appeared in Harris (1744–1748; Fig. 3.2 in Chapter 3: Perceptions).

Countless names have been applied to this archipelago of more than 120 volcanic islands, islets, and rocks. Since 1684, it seems that just about every visitor has brought along a new set of names, and at least one Island has collected some 11 of them … (Woram 1989: 25; see also, e.g., Crowley 1684 in Harris 1744–1748: 79; Jiménez de la Espada 1891; McEwen 1988; Melville 1856: 293). The profusion of toponyms conforms to a general pattern for this region: the Spaniards left primarily a fascinating array of names on the maps, some of which have since been erased (Dunmore 1991: xiv). Initially, Las Islas Encantadas (The Enchanted [bewitched] Islands) was popular, but in the end the enormous tortoises—galápagos in Spanish—prevailed, occasionally spelled Gallappagos or Gallipagos.

Nowadays, Galapagos draws people from around the world, some attracted by its natural beauty and mystery, others by a desire to live there or to take advantage of its livelihood options, and still others who are attracted to scientific questions. But it has not always been this way. Throughout their human history, Galapagos were frequently disparaged as less than useful real estate (Stahl et al. 2020: 13), a situation that changed dramatically in the mid-1900s, when the Archipelago evolved from unknown, dismissed volcanoes and rocks used as pirate hideouts and for penal colonies, into a legendary, world-famous, international tourism and research destination. Today, Galapagos plays a central role in understanding not only the Age of Discovery and unique island ecosystems, but also complex interactions between the environment and human societies and activities. The tortoises of Galapagos (Fig. 1.1) have been a primary attraction, a focal point for diverse activities and policies, and a flagship for the entire Archipelago and beyond (Chapter 17: History of Conservation).

Figure 1.1 The main islands of the Galapagos Archipelago, showing the typical adult form of each of the 14 named endemic species of Galapagos tortoise (that is, not including Santa Fe), alongside their respective island or volcano (in the case of Isabela Island). Extinct forms from Floreana, Pinta, and Santa Fe Islands indicated by †. See Table 1.1 for more details. Images: Alejandro Arteaga/Tropical Herping; Map: James P. Gibbs.

One of the most notable early visitors to Galapagos was Charles Darwin, who arrived aboard HMS Beagle on September 15, 1835 (Darwin 1839). During his 35-day visit, Darwin made observations that later nurtured his ideas about the origin of species and the process of evolution: arguably the greatest idea the human mind ever had (Berra 2009: 1). Hence, Galapagos and Darwin have been intimately linked ever since (Chapter 5: Darwin).

Yet, well before, and continuing after, Darwin’s short stay, numerous fascinating accounts of these faraway islands appeared in published writings of western mariners, including, for example, William Dampier, Woodes Rodgers, Amasa Delano, David Porter, Robert Fitzroy, and others (e.g., Burney 1902: 145 ff, 1816; Dunmore 1991; Harris 1744–1748; McEwen 1988; Pritchard 1996; Slevin 1959). Other narratives are found in unpublished logbooks of whaling ships as well as in lesser-known writings of mariners and adventurers (Townsend 1925). As notoriety of Galapagos increased, academic institutions, oceanographic and fisheries expeditions, zoological societies, naval organizations, natural historians, wealthy adventurers, and others made their way to the Enchanted Islands (e.g., Beck 1902; Beebe 1924; Pritchard 1996; Slevin 1959; Stahl et al. 2020)—with giant tortoises a primary lure (Chapter 3: Perceptions; Chapter 4: Exploitation; Chapter 6: Collectors).

Libraries around the world are replete with materials about Galapagos. Nearly 25 years ago—before a marked boom in publishing—a Galapagos bibliography that focused on natural history publications (Snell et al. 1996) identified 7531 references about the Archipelago, including 359 on just tortoises. Beyond their much-acclaimed inspiration for evolutionary sciences, natural history, geology, and conservation, the Islands have been a wellspring for literary works in which tortoises regularly feature (e.g., Chura 2015; Madison 1986; Robinson 1936; Tanyol 2007; Wilson 2000). Most famous is Herman Melville’s (1856) Las Encantadas, with its Two Sides to a Tortoise sketch. Such works have been as effective at putting Galapagos on the map as have many of the natural history studies.

Darwin’s Great tortoises of the Galapagos: Phylogeny, taxonomy, and nomenclature

Shortly after Darwin’s visit, it became known that beyond the Great tortoises, many other species of reptiles were endemic to Galapagos (e.g., Baur 1891; Heller 1903) —not to mention birds (Ridgway 1897) or plants (Hooker 1847a; Robinson 1902). Galapagos tortoises are routinely cited as remarkable examples of radiation and speciation on oceanic islands and often held out as a primary inspiration for Darwin’s development of the theory of the Origin of Species (e.g., Parham 2008: 15227; Russello et al. 2005: 287). What first most impressed Darwin, however, were the interisland differences seen in the mockingbirds (Mimus spp.). He was introduced to the idea of interisland differences among the tortoises while in the islands, but it was not until later, back in England, that the tortoises and later the finches (subfamily Geospizinae) became important components of his thinking (Berra 2009: 29 ff; Darwin 1846: 394–395; Chapter 5: Darwin). Moreover it is argued that 19 genera of Galapagos vascular plants held Darwin’s attention more and are, in fact, more remarkable examples of adaptive radiation than the animals (Porter 1979).

A total of 56 reptile taxa has been reported from Galapagos (Jiménez-Uzcátegui et al. 2013), including the 14 named and one, as yet, unnamed endemic tortoise species in the genus Chelonoidis (Table 1.1). Although tortoise taxa comprise little more than a quarter of Galapagos herpetofauna, their relative ecological, economic, historic, social, and conservation import are proportionally far greater (Chapter 3: Perceptions; Chapter 4: Exploitation; Chapter 17: History of Conservation). Although other places around the world host more turtle species than Galapagos (e.g., Buhlmann et al. 2009; Iverson 1992; Turtle Taxonomy Working Group 2017; van Dijk 2010), this Archipelago has the greatest diversity of chelonian taxa for any similar-sized area (Rhodin 2006: 21–22).

Table 1.1

aNomenclature follows Turtle Taxonomy Working Group (2017), with caveats explained in the footnotes for C. duncanensis [fn e], C. niger [fn f], and C. sp. indet. [fn g]

bPopulation size values from Chapter 20: Population Status.

cConservation status of the species as determined in the respective species account of The IUCN Red List of Threatened Species—see details in the respective species account: (1) Cayot et al. (2016a); (2) Caccone et al. (2017a); (3) Caccone et al. (2017b); (4) Cayot et al. (2016b); (5) Cayot et al. (2017a); (6) Cayot et al. (2017b); (7) Cayot et al. (2018a); (8) Cayot et al. (2017c); (9) Cayot et al. (2018b); (10) van Dijk et al. (2017); (11) Rhodin et al. (2018); (12) Cayot et al. (2017d); (13) Cayot et al. (2019a); (14) Cayot et al. (2019b).

dThe confirmation of a second native species on Santa Cruz Isalnd (Poulakakis et al. 2015) comes half a century after this possibility was raised (Snow 1964).

eThis taxon is also commonly referred to as C. ephippium (e.g., Poulakakis et al. 2015), originally Testudo ephippium Günther 1875 (see Cayot et al. 2017b: 1; Box 1.1).

fThere are compelling arguments (Olson 2015; Zug 1998) that Testudo nigra Quoy and Gaimard 1824 (now Chelonoidis niger) is a nomen dubium, and thus should not be used to refer to any taxon; this had been the custom until 1984 when nigra was revived casually in a popular article (Pritchard 1984) and later formalized (Pritchard 1996; Turtle Taxonomy Working Group 2009: 000.63). Moreover, strong arguments indicate that the long-questioned holotype of Testudo elephantopus Harlan 1827 was collected on Charles Island (=Floreana Island) (Olson and Humphrey 2017). If these points are accepted and put into practice, the binomen of the extinct Floreana tortoise would be Chelonoidis elephantopus (Harlan 1827), thus continuing the long-standing use of the name elephantopus for Galapagos tortoises (Olson 2015; Zug 1998) and also following recent nomenclatural usage for this taxon, which has been registered with the International Code of Zoological Nomenclature via ZooBank (e.g., Poulakakis et al. 2015: 6/18)].

gThe extinct tortoise of Santa Fe Island apparently was genetically distinct (Poulakakis et al. 2015: Fig. 2, Table 3, 2012) but has not been taxonomically described. Individuals of C. hoodensis first were introduced onto Santa Fe in 2015, as replacement tortoises, with nearly 500 tortoises now living on Santa Fe (Chapter 24: Santa Fe Island).

Galapagos tortoises are remarkable in diversity of taxa, morphotypes, habitats, and kinds of islands and environments where they live, from saddleback forms living on small, low-lying, arid islands to larger dome tortoises living in the humid highlands of large islands (Fig. 1.2, e.g., Fritts et al. 2000; Chapter 7: Evolution; Chapter 8: Morphology; Chapter 14: Habitats). After over a century of debate on the origin of the Galapagos Islands—whether continental or oceanic (e.g., Baur 1897, 1891, 1889; Dorst 1961: 55; Garman 1917; Hooker 1847b; Stewart 1915; Townsend 1925: 73; Vinton 1951), geological research confirms that these islands are seamounts, perched on the Galapagos Platform, peaks of undersea volcanoes estimated to have emerged between 0.3 and 3.5 million years ago (Mya) (Geist et al. 2014). They are part of the Galapagos Hotspot (Harpp et al. 2014), which played a major role in tectonic and biological evolution in the northern western hemisphere (Hoernle et al. 2002).

Figure 1.2 Galapagos tortoises exhibit a variety of shell shapes and sizes. The two principal shapes are dome (top row) and saddleback (bottom row). Dome tortoises generally grow to much larger sizes and are typical of larger islands with humid highlands. Saddleback tortoises are smaller than dome tortoises, with longer necks and legs, and are typical of low, arid islands. Top left = Chelonoidis donfaustoi on eastern Santa Cruz Island, top right = C. porteri on western Santa Cruz Island, bottom left and right = C. hoodensis from Española Island. Photos: top right – Linda Cayot; all others – GTRI.

Morphological and phylogenetic studies show that Chelonoidis chilensis, from southern South America, is the closest living relative to the Galapagos tortoise complex and that this clade derives from Africa—not Central and North America as was once postulated (Chapter 7: Evolution). Colonization by tortoises from mainland South America to the oldest of the Galapagos Islands is estimated to have occurred about 3.2 Mya (Poulakakis et al. 2012). Additionally, the presence of an elongated first thoracic centrum of the sub-Holocene Caribbean tortoise from Mona Island, Chelonoidis monensis (Williams 1952), aligns it as a member of the Galápagos tortoise complex (Vlachos 2018: 33–34), indicating a rarely studied phylogenetic link.

Galapagos tortoise taxonomy and nomenclature have been notoriously unstable, confused, and contentious (Box 1.1). The nomenclature and taxonomy shown in Table 1.1 have been selected by the editors of the present multiauthor volume based on majority agreement among many of the book’s authors and the coordinators of the most recent checklist of living chelonians (Turtle Taxonomy Working Group 2017); this reflects the nomenclature presently used in the IUCN Red List (Caccone et al. 2017a,b; Cayot et al. 2019a,b, 2018a,b, 2017a,b,c,d, 2016a,b; Rhodin et al. 2018; van Dijk et al. 2017).

Box 1.1

The centuries-long debate over Galapagos tortoise races and names: How many kinds of Galapagos tortoises are there?

Ongoing, centuries-old debates about the phylogenetic relationships, taxonomic status, and scientific names of Galapagos tortoises have generated conflicting opinions about the species, subspecies, and/or races, their origin, and names. Beginning in the late 1600s, various mariners’ accounts of Galapagos provided tidbits of natural history; some captains included general descriptions about Galapagos plants and animals, with particular attention to tortoises (e.g., Dampier 1697: 100–103). However, there was evidently no mention of different species, subspecies, or races of tortoises (Baur 1889): except for Captain David Porter, who compared shell shape, color, and size, stating: "[t]hose of James’ [Santiago] Island appear to be a species entirely distinct from those of Hood's [Española] and Charles’ [Floreana] Islands" (Porter 1815: 228: emphasis added). Remarkably, in his earliest publication on the voyage of the Beagle, Darwin (1839 [revised and republished in subsequent years]) recounted differences between tortoises from different islands, but stated (1839: 462) [t]here is one kind both of the turtle and tortoise…I will first describe the habits of the tortoise (Testudo Indicus) which has been so frequently alluded to. These animals are found, I believe, in all the islands of the Archipelago; certainly in the greater number. Hence, initially Darwin (1839) considered all Galapagos tortoises to belong to one (albeit incorrect) global species. Over time, with subsequent revisions of his general account of the Beagle’s voyage, he reported (e.g., 1846: 150) that there were different races of tortoises on different islands and that these belonged to a species endemic to Galapagos, Testudo nigra Quoy and Gaimard 1824.

From the mid-1800s to the early 1900s new tortoise species were named for different Galapagos Islands and discrete volcanoes of Isabela Island (e.g., Baur 1891, 1889; Duméril and Bibron 1835: 80, 115; Günther 1902, 1877, 1875; Parker 1934; Rothschild 1915a,b; 1903, 1902a,b,c; 1901; Rothschild and Hartert 1902; Van Denburgh 1914, 1907). Several decades later, the same allopatric forms were considered to be subspecies of a single species, comprising the Galapagos tortoise complex. Scores, likely hundreds, of publications—books, papers, reports, etc.—from the second half of the 1900s to the early 2000s treated Galapagos tortoises as subspecies of a single species (e.g., Caccone et al. 1999; Corley Smith 1977; Fritz and Havaš 2007; Hendrickson 1966; MacFarland et al. 1974; Marlow and Patton 1981; Mertens and Wermuth 1955; Pritchard 1996; Rhodin et al. 2008; Russello et al. 2007; Turtle Taxonomy Working Group 2007, Wermuth and Mertens 1961). Yet, numerous other works during the same period treated different island and discrete Isabela volcano populations as distinct species (e.g., Bour 1980; Crumly 1984; Ernst and Barbour 1989; Turtle Extinctions Working Group 2015; Turtle Taxonomy Working Group 2017, 2009). A third category of publications—especially those that dealt with tortoise phylogeny and taxonomy—explicitly recognized that the use of species or subspecies designations was actively debated, or they avoided assigning species or subspecies ranks, and instead referred to ESUs (evolutionarily significant units), lineage, morphotype, or taxa. In that way, they left the taxonomic designation open, or ambiguous, which implicitly acknowledged the contentious nature of Galapagos tortoise taxonomy (e.g., Beheregaray et al. 2004; Caccone et al. 2004; Chiari and Claude 2012, 2011; Chiari et al. 2009; Ciofi et al. 2009, Fritts 1984, Fritts et al. 2000; Milinkovitch et al. 2007; Parent et al. 2008; Powell and Caccone 2006; Russello et al. 2005; Zug 1998). Most recently, after extensive genetic work, employing numerous techniques and thousands of samples combined with detailed morphological studies, the trending view has returned to distinct species on different islands and Isabela volcanoes (e.g., Caccone et al. 2017a,b; Cayot et al. 2019a,b, 2018a,b, 2017a,b,c,d, 2016a,b; Garrick et al. 2015; Jensen et al. 2018a,b; Milinkovitch et al. 2013; Miller et al. 2018a,b; Parham 2008; Poulakakis et al. 2015; Quesada et al. 2019; Rhodin et al. 2018; Russello et al. 2010).

While taxonomic decisions were fluid, nomenclatural changes—at different levels—added more instability (e.g., Pritchard 1996: 34 ff). The generic name for Galapagos tortoises went from Testudo Linnaeus 1758 to Geochelone Fitzinger 1835, and then to Chelonoidis Fitzinger 1835 (Fritz and Havaš 2007). Additionally, the accustomed species name for the Galapagos tortoise complex had for years been elephantopus Harlan 1827. However, recently nigra Quoy and Gaimard 1824 has become more common (Pritchard 1996; Turtle Taxonomy Working Group 2017, 2009: 000.52–63). This major nomenclatural change has met with criticism and counterproposals (e.g., Olson 2015; Olson and Humphrey 2017; Zug 1998). Moreover, because of nomenclatural rules concerning the gender of Latinized names, Chelonoidis nigra had to be corrected to C. niger (Olson and David 2014) and C. phantastica, to C. phantasticus. Another nomenclatural issue involves the accustomed name for the tortoises of Pinzón (Duncan) Island: Testudo ephippium. It was argued (Baur 1889: 1040 ff; Garman 1917: 296; Pritchard 1996: 28 ff) that the type specimen of T. ephippium Günther 1875 is from Pinta (Abingdon) Island. And although ephippium is the senior synonym for the Pinta tortoise and therefore has priority for that taxon, it was proposed that abingdonii Günther 1877 be kept as the established name for the Pinta Island tortoise (although after more than a century there has still been no formal petition to the International Commission on Zoological Nomenclature to formalize this). Hence, duncanensis Garman 1917 (a nomen nudum) has been proposed as the replacement name for the Pinzón (Duncan) Island tortoise (Fritz and Havaš 2007; Pritchard 1996; Turtle Taxonomy Working Group 2017).

As a consequence of this nomenclatural instability, the many changes in generic and species names, as well as evolving perceptions about species and subspecies ranks, current authors and their Galapagos tortoise research teams have struggled with which names to use. Thus, recent publications have employed a variety of names for the same population. Perhaps Pritchard (1998: xii), who promoted some of the more recent and consequential nomenclatural changes (Pritchard 1996), said it best: I am the first to concede that both the biological and the nomenclatural status of the Galapagos tortoises are so complex that consensus is unlikely to be reached for some time to come—even on such fundamental issues as to whether one or several species exist—and if there is only one, what that one should be called. The names, nomenclature, and taxonomy for Galapagos tortoises used throughout the present volume are detailed in Table 1.1.

Throughout the extended taxonomic and nomenclatural debates, captive breeding, reintroductions, introductions (rewilding), and other tortoise conservation strategies, begun in the 1960s, have focused on populations or even subpopulations with no admixing of a general Galapagos stock (e.g., MacFarland et al. 1974: 119; Perry 1969: 275; Snow 1964: 278). In other words, conservation efforts have avoided grouping individual tortoises from different localities. As a result, the taxonomic uncertainties and ongoing nomenclatural debates have been largely irrelevant to tortoise conservation efforts (Chapter 17: History of Conservation).

The history and status of Galapagos tortoises

Although the existence of Galapagos tortoises was first recorded in 1535 (de Berlanga 1884[1535]: 539), known human impacts did not start until the late 1600s and early 1700s, when direct exploitation began (e.g., Baur 1891, 1889; Pritchard 1996; Slevin 1959). Henceforth, exploitation progressed from relatively low levels to much greater intensity, reaching the point of decimation, if not extermination, of most of the populations (Chapter 4: Exploitation). A classic example of overexploitation, the 15 species of Galapagos tortoises recognized today comprise three extinct, six critically endangered, three endangered, and three vulnerable taxa (Table 1.1).

The Galapagos Islands, the tortoises, and their history are unique; yet the general processes of species loss and environmental degradation and transformation are well-documented on other island groups around the world (e.g., Braje et al. 2017; Hastings et al. 2014; Kirch 2005; Kouvari and van der Geer 2018; Steadman and Martin 2003; Steadman et al. 2015; Chapter 2: Protagonists). Overexploitation, or overkill, especially on islands, is usually the most obvious human impact, as seen in Galapagos, but other anthropogenic effects, particularly introductions of invasive species, can be just as, or sometimes more, destructive over the long term. When these disturbances occur together the impacts are especially severe.

During the 1800s until the mid-1900s, 200–300 thousand tortoises are estimated to have been taken from Galapagos, with intense exploitation on several islands. This continued, at varying levels, even after the 1950s when there were repeated reports of tortoise killing (e.g., Bowman 1960; de Vries 1984; Eckhardt 1972; Hendrickson 1966; Slevin 1959; Chapter 4: Exploitation; Box 17.3 in Chapter 17: History of Conservation).

Making realistic estimates of numbers of tortoises taken during different times and by different actors is a challenge. Based on less than a year’s data (October 13, 1832–August 30, 1833) from visiting whalers at Floreana Island (then Charles Island), Baur (1889: 1057) estimated that [t]here is little doubt that about one hundred thousand tortoises were taken from the Galapagos Islands since their discovery—that is, 100,000 tortoises taken before 1890. Baur’s estimate has been reported—erroneously—as 10 million, evidently beginning with Garman (1917: 267); and subsequently repeated (e.g., Bowman 1960: 20; Dorst 1961: 57; Shaw 1967: 120; Snow 1964: 278; Townsend 1925: 65).

A review of 79 logbooks from American whaling vessels that visited Galapagos between 1831 and 1868 yielded a cumulative take of 13,013 tortoises (Townsend 1925). This value, however, is minimal, as it did not include turpining (tortoise hunting) from: (1) activities previous to 1831; (2) activities after 1868; (3) all of the United States-based whalers (of which there were more than 700); (4) whalers from other countries, particularly the United Kingdom, which had extensive whaling operations; (5) other vessel types including men-of-war, buccaneers, merchant vessels, visiting and resident sealers, and scientific vessels; (6) complete and accurate records in logbooks, which are commonly partial and incomplete; and (7) direct, often intense, tortoise exploitation by Galapagos residents mostly for meat and oil and for export to the South American continent (e.g., Colnett 1798; Schmitt 1935; Shuster 1983; Townsend 1925; Whitehead et al. 1997). Hence, it was estimated that just American whalers took at least 100,000 Galapagos tortoises since 1831 (Townsend 1925: 70); however, that value should also be viewed as a minimum of tortoises removed from the Archipelago (Chapter 4: Exploitation).

Not only were Galapagos tortoises taken by buccaneers, whalers, sealers, tortoise oilers, adventurers, zoological expeditions, other passing mariners, and island residents but, beginning in the late 1840s, vessels from California sailed to Galapagos specifically to bring back marine turtles and land tortoises to feed the growing population of immigrants that flourished there during the California Gold Rush. An often-ignored chapter of direct take, historic exploitation for transport to California is a significant contributing factor in the decimation of the tortoises (Conrad and Pastron 2014; Conrad et al. 2015). All told, the total number of tortoises taken from Galapagos is estimated to be 200–300 thousand (Chapter 4: Exploitation).

Prehistoric population sizes of Galapagos tortoises are unknowable, but today’s populations are clearly a remnant of what they once were. Current estimates for all populations (detailed in Table 1.1 and Chapter 20: Population Status) total to 35,035 tortoises. With three species extinct, six critically endangered, three endangered, and three others vulnerable, restoration of Galapagos tortoise populations—especially reestablishing their roles in ecosystem networks and processes—presents major challenges (Chapter 2: Protagonists; Chapter 17: History of Conservation; Section V: Restoration Case Studies).

Threats to Galapagos, the tortoises, and more

In 1959, the Galapagos National Park was established by the Government of Ecuador. That year a study by UNESCO/IUCN to, among other things, establish a research station, concluded that [t]he prospect for the future [of the tortoises] is not hopeful (Eibl-Eibesfeldt 1959). A few years later the findings of the fifth expedition of the New York Zoological Society to Galapagos were just as bleak (Dowling 1962), as was an update on tortoises included in the Proceedings of the 1964 Galápagos International Scientific Project (Hendrickson 1966: 236). Hence, efforts to protect and restore tortoise populations have addressed an ever-increasing number and variety of challenges. Some of the more conspicuous threats include introduced species, habitat degradation, reduced genetic diversity, poaching and illegal trade, and escalating tourism, combined with social conflict around conservation (Chapter 17: History of Conservation).

Introduced species: An early and increasing threat

As on most oceanic islands, alien species are a major problem in Galapagos, an issue identified over a century ago (e.g., Barnett 1986; Beck 1902; Schmitt 1935; Slevin in Van Denburgh 1914; Stevenson 2001; Chapter 19: Invasive Species). Complicating this is ever-increasing human mobility to and among the islands, primarily to provide increasing numbers of residents and tourists with goods and services (e.g., Taylor et al. 2008; Toral-Granda et al. 2017). By 2012, the number of exotic vertebrate species had risen to 40, half of them established, including 10 mammals, four birds, three reptiles, one amphibian, and two fishes (Phillips et al. 2012). The number of introduced insect species has also increased (e.g., Peck et al. 1998): in 2003 at least 463 alien insect species had been recorded, nearly a quarter of the number of endemic species (Causton et al. 2006). The group with the greatest number of exotics is terrestrial plants: 821 species, of which 810 are established in Galapagos. In total, at least 1579 alien species, plants and animals, including more than 63 pathogens, are documented in Galapagos; and introduction of new species continues (Toral-Granda et al. 2017).

In response to expanding environmental and social problems resulting from burgeoning resident and tourist populations, the Law for a Special Regime for the Conservation and Development of the Province of Galapagos was approved in 1998 (Bensted-Smith et al. 2000). Subsequently, biosecurity protocols (in 1999), a strategic plan for invasive species management (in 2007), and a biosecurity agency for Galapagos (in 2012) were established (Toral-Granda et al. 2017).

Since the establishment of the Galapagos National Park in 1959, numerous invasive mammals that threaten tortoises have been targeted for control and, in some cases, eradication: dogs, donkeys, goats, pigs, and rats (Chapter 17: History of Conservation; Chapter 19: Invasive Species). Pigs, rats, and dogs, in that order, have been major predators of various life stages of certain tortoise populations. Large herbivores, especially goats and donkeys, feed on the same plants as tortoises and cause significant—often catastrophic—alterations to tortoise habitat. Donkeys also trample tortoise nests, increasing egg and hatchling mortality. Solenopsis fire ants, evidently established on Galapagos in the early 1900s, are a common threat to native fauna (e.g., Boulton et al. 2019; Lubin 1984) and are the only introduced insect known to directly affect tortoises (Solenopsis prey on tortoise eggs and hatchlings and can damage vulnerable appendages such as the tail of adults, e.g., Herrera et al. 2013; Márquez et al. 2004; Tapia 2018; Wauters et al. 2018).

Contrary to concerns about introduced animals at the start of conservation efforts, relatively little attention was initially paid to alien plants (e.g., Macdonald et al. 1988; Porter 1973). Over 800 introduced species, nearly twice the number of native plant species, ranging from grasses and forbs to trees, are now recognized to have many and often severe impacts (e.g., Buddenhagen et al. 2004; Guézou et al. 2010; Jaramillo Díaz et al. 2017; Pollard et al. 2019; Tye 2006). Certain introduced plants present clear threats to tortoises. Blackberry (Rubus niveus Thunb.) is invasive in many parts of Galapagos and can become established quickly, forming tangled thickets (Rentería et al. 2012a,b), impenetrable even to tortoises, creatures notorious for their ability to break through barriers (Chapter 13: Movement Ecology). This problem occurs on San Cristóbal, Santiago, and Santa Cruz Islands, as well as on Cerro Azul and Sierra Negra Volcanoes on Isabela (Caccone et al. 2017b; Cayot et al. 2019b, 2018a, 2017d). Interactions between invasive animals and invasive plants, and how they affect the native flora and fauna, are poorly understood (Filek et al. 2018). Of concern is the potential for unintended consequences of mammal eradications, which can result in the release and spread of invasive plant species, for example, on Santiago Island (Chapter 20: Population Status).

Restoration of native flora and vegetation communities, especially in the arid ecosystems that dominate the terrestrial portion of Galapagos, may take decades, or centuries, to encompass growth, recruitment, recovery, and other processes subject to major climatic variations ranging from El Niño (ENSO) to global warming (Gibbs et al. 2014; Hunter and Gibbs 2014; Hunter et al. 2013). Full recovery to an earlier ecological state, more representative of conditions prior to the arrival of humans, may never be achievable (e.g., Hamann 2011; Chapter 14: Habitats). Yet, the floristic situation in Galapagos conforms to the generality on other oceanic islands: relatively few species extinctions have occurred, despite the native flora being strongly outnumbered by naturalized exotics (Jäger et al. 2009; Sax and Gaines 2008).

Thus, the prevailing view that native=good and introduced=bad needs reexamining. For example, certain introduced plant species provide tortoises with food, allowing them to maintain, even improve, body condition when seasonal native plant production is low; this is the case with Santa Cruz tortoises, C. donfaustoi and C. porteri (Blake et al. 2015: 254). On the other hand, certain native species, including tortoises, that benefit from invasive plants, also disperse their seeds, expanding their range and potentially impacting native vegetation (Carrión-Tacuri et al. 2012; Ellis-Soto et al. 2017).

Introduced diseases (vectors and pathogens) pose dire threats to Galapagos wildlife and humans (e.g., Bataille et al. 2012; Deem et al. 2012, 2011, 2010; Kilpatrick et al. 2006; Chapter 18: Health). There are studies of Galapagos tortoise parasites (e.g., Couch et al. 1996; Gibbons and Steffes 2013; Sevillano et al. 2019), but little is known of the tortoises’ blood parasites, which could arrive through introduced pathogens. Growing concerns include disease introductions such as West Nile virus (Kilpatrick et al. 2006), Ranavirus (Johnson et al. 2008; McKenzie et al. 2019; Wirth et al. 2018), and other recently investigated reptilian diseases, which could easily arrive in Galapagos and become serious threats to tortoises. Other potential risks include interactions between land use by humans and introduced diseases in native wildlife (Zylberberg et al. 2013), as well as introduced diseases that may affect native plants that are critical to certain tortoise populations, such as Opuntia spp., which provide high-moisture-content food and cover for refuge (Chapter 14: Habitats).

Environmental change and habitat degradation

Galapagos of today is a legacy of millennia of environmental changes; paleoecological research reveals major environmental changes over tens of thousands of years (e.g., Coffey et al. 2012; Collins et al. 2013; Conroy et al. 2015; Froyd et al. 2014; Thompson et al. 2017). Yet, it is claimed that human actions have had a far greater, and perhaps irreversible, influence on this island system than the preceding 2600 years of climate change (Restrepo et al. 2012: 1864). Habitat destruction, primarily on settled islands, is a major threat (Bensted-Smith et al. 2000) and is directly linked to introduced species. The situation with invasive plants and habitat degradation is complex. Several initiatives have focused on eradicating, or controlling, exotic plants (e.g., Buddenhagen and Yánez 2005; Buddenhagen et al. 2004; Jäger et al. 2017; Rentería et al. 2012a,b), and in some sites—particularly where goats have been eradicated—native vegetation is recovering (e.g., Gibbs et al. 2014, 2008; Hamann 1993, 1979; Hunter and Gibbs 2014; Hunter et al. 2013; Chapter 14: Habitats; Chapter 19: Invasive Species). However, many of these efforts, especially those aimed at control of invasive plants, have had limited, if any, success (e.g., Gardener et al. 2013, 2010; Hoffmann et al. 2010; Trueman et al. 2010).

Humid and very humid highland areas have declined since precolonial times, losing between 76% and 88% of area on Santa Cruz Island and between 94% and 100% on San Cristóbal Island (Watson et al. 2010). Paleoecological work indicates that aquatic highland habitats—now uncommon in Galapagos—were formerly important for tortoises; however, their loss on Santa Cruz Island evidently began centuries before intense human exploitation started (e.g., Coffey et al. 2012; Conroy et al. 2008; Fournier et al. 2016; Froyd et al. 2014). Understanding how anthropogenic activities have altered Galapagos vegetation and ecosystems requires more research (e.g., Trueman et al. 2014, 2013), particularly on ecological interactions between tortoises and their habitats (Chapter 13: Movement Ecology; Chapter 14: Habitats; Chapter 15: Role in Ecosystems).

Although the role of tortoises in Galapagos ecosystems is incompletely understood, they are known to have key functions. Galapagos tortoises are important for seed dispersal networks (Nogales et al. 2017). Tortoises are ecosystem engineers, dominant herbivores in their island homes (Chapter 2: Protagonists; Chapter 15: Role in Ecosystems). The reintroduction of endemic Chelonoidis hoodensis on Española Island and introduction of replacement tortoises on Pinta Island have facilitated partial habitat restoration, particularly recuperation of Opuntia (Gibbs et al. 2008; Hunter and Gibbs 2014; Hunter et al. 2013). Galapagos tortoises are ‘gardeners of the Galapagos’ not only via their role as seed dispersers but also by stimulating vegetation productivity at the scale of entire landscapes (Bastille-Rousseau et al. 2017: 8).

Another risk to Galapagos tortoises is volcanic activity, particularly lava flows and in some cases resulting fires. Tortoise population size on Fernandina Island (if indeed a population still exists) is limited by frequent volcanism, which destroys tortoise habitat and creates barriers to movement, as also occurs on Cerro Azul, Darwin, and Wolf Volcanoes on Isabela Island (Chapter 14: Habitats; Chapter 20: Population Status). Singularly low genetic diversity in the large population of Alcedo Volcano, Isabela Island, is attributed to repeated volcanism causing population die-offs, followed by population recovery by surviving individuals that passed through a bottleneck (Beheregaray et al. 2003). In addition, the few known instances of human-caused fires threatened tortoises on southern Isabela Island (Marquez 1986) and perhaps, historically, on Floreana Island (Chapter 4: Exploitation; Chapter 23: Floreana and Pinta Islands).

Many consequences of habitat destruction are quickly detectable, but some represent a debt—a future ecological cost of current habitat destruction (Tilman et al. 1994: 65; Triantis et al. 2010). Extinctions that occurred generations after habitat destruction had begun are classic examples of extinction debt (Jackson and Sax 2009; Loehle and Li 1996; Malanson 2008). Predicted threat of extinction debt is severe for island ecosystems, suggesting that island extinctions recorded to date may be a small proportion of what is to come, particularly for arthropods and pollination networks, but not necessarily plants (Sax and Gaines 2008; Triantis et al. 2010). This emphasizes the fundamental need to better understand tortoise ecology, in the broadest terms, to ensure the future of tortoise populations (Chapter 15: Role in Ecosystems).

Reduced genetic diversity

With five of the 12 surviving Galapagos tortoise populations estimated at less than 2000 individuals (Chapter 20: Population Status), and nine populations categorized by the IUCN as either critically endangered or endangered, reduced genetic diversity is a potential concern, because it may result in decreased capacity for adaptation to diverse threats, like new diseases and changing environments from climate change. Apparently, however, most Galapagos tortoise populations have survived for generations with relatively low genetic diversity, a characteristic common to many island forms (Garrick et al. 2015). Therefore, tortoise survival may be less sensitive to low heterozygosity than are many other vertebrates. Nevertheless, captive breeding programs for Galapagos tortoises have addressed genetic issues (e.g., Benavides et al. 2012; Edwards et al. 2013; Jensen et al. 2018a; Milinkovitch et al. 2013; Miller et al. 2018a; Poulakakis et al. 2008; Quinzin et al. 2019; Russello et al. 2010; Chapter 7: Evolution; Chapter 17: History of Conservation). These programs, however, are limited to finding, saving, and maintaining existing genetic diversity—not generating new alleles.

Poaching and illegal trade

Galapagos tortoises were legally protected by Ecuador in 1934, and again in 1959 and 1970 (Eibl-Eibesfeldt 1959; Gobierno del Ecuador 1970, 1959; MacFarland and Black 1971; Perry 1970). However, tortoise hunting has continued, albeit at much lower and varying intensities (e.g., Cayot and Louis 1994; Corley Smith 1977; Dowling 1962; Hendrickson 1966; Márquez et al. 2004). The motivations behind present-day tortoise killing are complex (Box 17.3 in Chapter 17: History of Conservation). Some tortoises have been taken on settled islands for food, others from more remote islands as an occasional amenity by fishers and mariners, and some tortoises are killed as a political act. For example, fishermen threatened and killed endangered tortoises to protest new fisheries regulations enacted after years of fisheries anarchy (e.g., Anon. 2005, 2004; Ferber 2000; Sitwell 1993). Ongoing poaching of Sierra Negra tortoises, Chelonoidis guntheri, done for a variety of reasons, is a most serious threat (Cayot et al. 2018a; Márquez et al. 2004): it could limit recovery of that population—once among the largest in Galapagos. Hence, restoring the tortoise population of Sierra Negra, in the face of ongoing poaching, presents one of the most vexing challenges to tortoise conservation (Chapter 20: Population Status).

Although Ecuadorian laws ban removal of live tortoises from Galapagos (Gobierno del Ecuador 1970: 1750 ff, 1959), illegal trade of wild Galapagos tortoises, for pets and collections, has continued for over a century (e.g., King 1968: 30; MacFarland and Black M 1971; MacFarland and Reeder 1975). Most recently, theft and trafficking of small tortoises from Tortoise Breeding Centers in Galapagos have occurred (Dasgupta 2018; Ministerio del Ambiente 2018; Phys.Org 2018, 2017; see Tatayah et al. 2018 for tortoise trafficking in Mauritius; Box 17.3 in Chapter 17: History of Conservation). Publicly available information on locations of newly described species and recovered nearly extinct populations poses a risk, because unscrupulous people can mine it to plan illegal activities. Although the impact of trafficking on wild Galapagos tortoise populations is unknown, with the massive international rare reptile trade (Stuart et al. 2006), government authorities and the conservation community must remain vigilant.

Tourism and affiliated issues

In Galapagos, tourism is the primary economic driver, and tortoises, its primary attraction. Planned tourism for Galapagos began in 1967, expanding from about 3000 tourists in 1969 to 275,817 in 2018; the last figure represents a 14% increase from the previous year (Taylor 2019). The industry pays for conservation in Galapagos because it sustains, directly or indirectly, most local economic activity and, hence, provides revenue to the government for reinvesting in conservation and local needs on the Islands. This includes park entrance fees and revenue from general economic activity. In addition, many donors to organizations throughout the world that support Galapagos conservation were first tourists to the Islands.

Yet, diverse problems are also associated with tourism, including threats to wildlife and habitats, as well as social and cultural conflicts between local residents and tourism and conservation activities (e.g., de Groot 1983; Hennessy 2014; MacFarland 2000; Rice 2007; Taylor et al. 2008). Aside from tour buses occasionally colliding with tortoises, there are few documented direct impacts of tourism on tortoises; however, indirect effects can be substantial for tortoise populations on settled islands, especially in humid highland areas. A primary threat, driven by tourism, is unbridled economic development that results in the conversion of tortoise habitats for human uses (e.g., tourist destinations, residential and commercial areas, and agricultural lands), with ever-larger fenced areas and expanding networks of roads. These land-use changes can affect the ability of tortoises to migrate, as is seen on Santa Cruz Island (Chapter 13: Movement Ecology). In some places, specific habitat features, such as ponds used by tortoises, are also affected (Box 15.3 in Chapter 15: Role in Ecosystems). Development in the highlands of Santa Cruz and San Cristóbal Islands, and on Sierra Negra Volcano on Isabela Island are expected to expand, as well as perhaps on Floreana Island, where the release of tortoises into the wild is planned (Chapter 23: Floreana and Pinta Islands), so tortoise–human conflicts in settled areas of these islands will likely become an increasing focus of tortoise conservation efforts in the future (Benitez-Capistros et al. 2018).

Conservation successes over the last 60 years

Despite the drastic reduction of Galapagos tortoise populations, with five now with less than 2000 individuals each, and three extinct (Table 1.1), major advances in conservation have been achieved. Conspicuous in scale and effort are the restoration of several tortoise populations, previously devastated by overexploitation and habitat destruction (Chapter 17: History of Conservation). The Española Island tortoise, C. hoodensis, has been rescued from near-certain extinction by captive breeding of the last remaining 15 individuals; tortoises reintroduced to the now goat-free island are breeding, with signs of reaching a self-sustaining population (Chapter 21: Española Island). The Pinzón Island tortoise population, C. duncanensis, formerly C. ephippium, now lives on a rat-free island, with hatchlings surviving and being recruited into a growing population for the first time in over a century (Chapter 22: Pinzón Island). Although the Pinta Island tortoise, C. abingdonii, and the Floreana tortoise, C. niger, are both declared extinct by the IUCN, their respective island homes are finally free of invasive goats, native ecosystems are being restored, and both islands await replacement tortoises, and at some future date the respective Pinta and Floreana lineages could be revived from hybrid tortoises (Chapter 23: Floreana and Pinta Islands). The unnamed Santa Fe Island tortoise, Chelonoidis sp. indet., exterminated by humans in the 1800s, has been replaced by Española tortoises, now on a goat-free island, in an effort to reestablish the lost ecological roles of the original tortoise population (Chapter 24: Santa Fe Island). And rewilding—a relatively recent procedure in conservation ecology—is advancing in Galapagos to the point of international recognition (Chapter 2: Protagonists). The recent confirmation of a long-suspected distinct species of tortoise from eastern Santa Cruz, C. donfaustoi, illustrates the ever-present horizons for discovery in Galapagos; despite being threatened, this population is now included in ongoing recovery efforts (Chapter 20: Population Status). Genetic research has been supporting tortoise conservation with phylogenetic and taxonomic insights; it also provides evidence-based recommendations on which individual tortoises to use in captive breeding groups and informs policies on reintroductions and lineage recovery. Few conservation programs anywhere, for any species, have so benefited from such a comprehensive and supportive genetic research program (Chapter 7: Evolution; Chapter 17: History of Conservation).

Although present-day Galapagos tortoise populations are vestiges of their original abundance and distribution, captive breeding, head-starting, repatriation, rewilding, and invasive species control have reversed the former trend. After decades of conservation intervention, several populations are poised to become self-sustaining and many remaining populations are on a trajectory toward recovery (Chapter 17: History of Conservation; Chapter 20: Population Status). Recovering tortoise populations and the subsequent reestablishment of lost ecological networks and processes have helped to stimulate the recovery of native vegetation on many islands, notably Española (Gibbs et al. 2014; Hunter and Gibbs 2014; Hunter et al. 2013) and Pinta (Hamann 1993, 1979; Chapter 2: Protagonists; Chapter 15: Role in Ecosystems). This synergistically promotes conservation of other native species and their habitats, as well as overall island restoration.

Some of the more aggressive invasive species problems—long the bane of Galapagos conservation—have been addressed: goats eradicated from most tortoise islands, namely Española, Floreana, northern Isabela, Pinta, Santa Fe, and Santiago; donkeys eliminated from Floreana, northern Isabela, Santiago, and San Cristóbal; pigs eradicated from Floreana and Santiago; and rats eradicated on Pinzón (Chapter 17: History of Conservation; Chapter 19: Invasive Species; Section V: Restoration Case Studies). These programs involved vast terrestrial areas, requiring complex, multi-million-dollar, often multidecade initiatives (Carrión et al. 2011).

Despite complex, long-standing challenges, interdisciplinary, community-based approaches are gaining ground at higher levels within the general conservation community, including promotion of improved local participation in decision making (e.g., Jupiter et al. 2017; Kelman 2017; Kueffer and Kinney 2017; Lauer 2017). Galapagos-based initiatives led the way with monitoring ecosystems, which had been initially conceived to focus on indigenous plants and animals, but are now expanded to also look at various elements of society, and encourage transparency and citizen participation (e.g., Gibbs 2015; Stevenson 2001). Various social sectors in Galapagos have adopted this approach, addressing natural history together with tourism, trade, transport, economy, and other social issues (e.g., Bensted-Smith 2002; Epler 2007; Gardener and Grenier 2011). Important advances include the collaboratively derived environmental research agenda (Izurieta et al. 2018) and exploring diverse attitudes of different sectors of Galapagos society in relation to tortoise conservation (Benitez-Capistros et al. 2018, 2016; Constantino 2012). These approaches promote the involvement of the whole of Galapagos society to be responsible stewards of their own resources, not just onlookers or antagonists, as has occurred at times in the past.

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