APPENDIX A Some Common Misconceptions About Galápagos

APPENDIX A

Some Common Misconceptions About Galápagos

1. Galápagos is one island, or a small handful of islands.Galápagos is an archipelago of many volcanic islands. There are 127 named islands and islets, of which 19 are over 1 km2 (0.4 square miles; Peck 2001, 2‒3). The total land area of all the islands is approximately 7,856 km2 (3,033 square miles), slightly larger thanthe U.S. state of Delaware. At 4,588 km2 (1,771 square miles), formed from the fusion of six volcanoes, Isabela’s area is greater than the rest of the islands combined. Thesecond largest island, Santa Cruz, at 986 km2 (381 square miles), was formed from one large volcano with many smaller, secondary eruptions. The wonderful new Atlas deGalápagos, Ecuador [Atlas of Galápagos, Ecuador] (CDF and WWF- Ecuador 2018) is a useful spatial guide to the islands.

2. Galápagos has few, if any, human inhabitants besides park rangers.A 2015 census of population and housing in Galápagos counted a total of 25,244 residents, not including tourists (INEC 2017). Of that total, 15,701 (62%) live in and around Puerto Ayora, Santa Cruz Island, the largest town, which hosts the Charles Darwin ResearchStation and the Galapagos National Park Directorate. Another 7,199 (29%) live in andnear Puerto Baquerizo Moreno, San Cristóbal Island, the Provincial capital of Galápagos. And 2,344 (9%) live in and near Puerto Villamil, Isabela Island. Fewer than 100 peoplelive on Floreana Island. The population of Galápagos has grown steadily since 2015, and, in 2020, many officials estimate there are 30,000 to 35,000 inhabitants. Livelihoods areearned largely through tourism, services, fishing, and agriculture.

3. Galápagos was known and visited by Native Americans before Columbus.There is no convincing evidence for human activity in Galápagos in the pre-Columbian period. The first visit for which there is solid evidence came in 1535: it was accidental and short- lived. In that year, a ship carrying the Bishop of Panama, Tomásde Berlanga, to Peru was becalmed at sea, and drifted to Galápagos. The Bishop’s letter to the King of Spain contains the oldest available description of the islands and didnot make it sound inviting or habitable (see Chapter 4). Untold numbers of ships,many carrying buccaneers and whalers, visited the islands in the 17th to 19th centu-ries, harvesting whales, marine mammals, and giant tortoises. The first documentedinhabitant, Patrick Watkins, was marooned alone on Charles (Floreana) Island, from1806 to 1809, exchanging potatoes he grew in the highlands for rum from visitingships. In 1832, the first colony, of about 120 people, was founded on Charles Island by Ecuadorian General José Villamil.

3. Galápagos lies southeast of the United States.Galápagos lies 1,000 km (600 miles) west of Ecuador’s coast, putting it 3,400 km (2,135 miles) straight south of the U.S. city of New Orleans, and 4,400 km (2,733 miles)straight south of St. Louis. The equator passes right through the archipelago, crossingthe “nose” of Isabela Island’s seahorse shape.

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2 Appendix A

4. Galápagos has a typical tropical- island climate with warm ocean temperatures.The climate of Galápagos is anything but typical for an equatorial area, for it is surrounded most of the time by unusually cold seas. The cold water comes from the Humboldt Current that flows up the western coast of South America and con-tinues out to the archipelago. The Humboldt Current also makes the Galápagos “de-sert dry” at sea level, in stark contrast to other tropical islands. Only on islands with tall volcanoes does one find a “humid zone” with dense vegetation (see Chapter 4) as often found on tropical islands. Another unusual feature of the archipelago’s cli-mate relates to the El Niño- Southern Oscillation (ENSO), and most especially to the warm- water phase called El Niño. Many of the climate changes wrought by ENSO relate to the circulation patterns of trade winds and ocean currents along the equator in the eastern Pacific, which puts Galápagos smack in the center of region most af-fected by ENSO (see Chapter 2). There are biologically significant consequences of ENSO in almost every single case study presented in this book, including some of the most dramatic examples of adaptation and resilience.

5. Galápagos is pristine, much like Darwin found it.While 95% of native species do remain, human activity since 1535 has brought a whop-ping 1,579 new species to Galápagos as of 2017 (Toral- Granda et al. 2017). That’s an av-erage of roughly 3.3 species annually, of which 1,476 have become established and have reproducing populations, including dogs, cats, rats, goats, and many others. Humans have brought nearly 1.5 times as many introduced plants as there were natives and endemics. We have brought 50 vertebrates, of which 27 are established, including 20 mammal species, compared to eight native mammals (one bat and seven rodents). We have introduced 545 insect species (Toral- Granda et al. 2017), compared with 736 en-demic and 818 native species— 1,554 total (Peck 2008). Only two islands have roughly the same flora and fauna as when Darwin visited: Genovesa and Fernandina.

6. Visitors pay high park entrance fees for Galápagos.Although the cost of a Galápagos visit can be expensive from remote points of or-igin, the current (2020) Galápagos visitor’s fee is only $100 per person for as long as one stays. For the range and quality of experiences available, this is substantially underpriced and could reasonably be much higher. Compare, for example, with the Ngorongoro Conservation Area of Northern Tanzania, which offers comparably di-verse, high- quality experiences: it charges $60 per day ($420 per week; see discussion in Chapter 9).

7. “Tortoise” and “Turtle” mean the same thing.Tortoises and turtles are members of the Order Chelonii (reptiles with a protective ex-terior shell). Most authorities use “turtle” for water- dwelling Chelonii, and “tortoise” for land- dwelling Chelonii. To reduce confusion in referring to Galápagos, we nor-mally speak of giant tortoises on land and sea turtles in the water.

8. Darwin spent a major portion of the Beagle voyage in Galápagos, which is why these islands were so impressive to him.The Beagle voyage lasted nearly 5 years (from December 27, 1831, to October 2, 1836). Darwin was in Galápagos only 5 weeks (from September 16 to October 20, 1835), 2% of the voyage, and he personally went ashore on only four islands (San Cristóbal, Floreana, Isabela, and Santiago). Of the four, he spent the most time on Santiago: 9 days.


Appendix A 3

9. Of all birds Darwin saw in Galápagos, he was most impressed with the finches, now called “Darwin’s finches.”As noted in Chapter 6, Darwin (1836 [1963], 261) felt “an inexplicable confusion” about the finches he observed and collected in the archipelago. When British orni-thologist John Gould later confirmed that Darwin’s collection held 13 previously unknown species, they became part of the latter’s accumulating evidence for evo-lutionary change in the islands. But during his time in the islands, Darwin was more affected by the mockingbirds he found, because they looked much like the mockingbirds he had seen in Chile— and why was that? Moreover, he noted that their morphologies (i.e., visible features) varied consistently among the first three islands he visited— also puzzling. As the Beagle sailed on from Galápagos, Darwin wrote about the three forms in his notes, “I must suspect they are only varieties,” other-wise “such facts would undermine the stability of species” (1836 [1963], 262). Back in England, when Gould confirmed that Darwin’s mockingbirds were indeed three new species, Darwin puzzled over what had produced their differences, a puzzle that eventually led to his theory of evolution by natural selection. It is clear from his notes that Darwin did not discover evolution in a “eureka” moment in Galápagos, but only later, in England. Today we recognize four species of mockingbirds in Galápagos— all of them close genetic relatives of the Chilean mockingbird.

10. Blue- footed boobies occur primarily in Galápagos.Although iconic of the islands, blue- footed boobies also occur naturally over a broad geographic area outside the archipelago. They are found along the Pacific Coast of Mexico, especially in the Gulf of California, as well as along the coasts of Central America, Colombia, and Ecuador. In 2013, during a sardine shortage in tropical wa-ters, blue- footed boobies were seen as far north as Santa Cruz, California. For many years, Galápagos has had the world’s largest population of these unusual birds. In the text I propose the hypothesis, as yet untested, that blue- foots evolved their blue feet in Galápagos while feeding on sardines.

11. Seals are common on the shores of Galápagos.The marine mammals seen on the beaches and rocky shores of various islands are two species of sea lions, not seals. The telltale feature is external ear flaps, which true seals do not have. Galápagos sea lions (Zalophus wollebaeki) are closely related to California sea lions, but notably smaller. Fur sea lions (Arctocephalus galapagoensis), whose closest relatives are in Patagonia, were once a much larger population in the archipelago, but were greatly reduced by human hunters. Though sometimes called “fur seals,” they, too, are sea lions with external ear flaps. The presence of these two sea lion species in Galápagos, of Californian and Patagonian origins, is dramatic tes-timonial to the role of major coastal currents, from the north and south, in bringing colonizing species to Galápagos.

12. Most terrestrial organisms are easy for visitors to see because there are very few threats or predators in the islands.It is true that Galápagos lacks native terrestrial predators larger than centipedes, snakes, and lava lizards, which means that most native species are unafraid of people. If one carefully stays at least 2 m (7 ft) away (National Park rules), most animals go about their business unconcerned by human presence. However, Galápagos does have avian predators (Galápagos hawks, short- eared owls, barn


4 Appendix A

owls, and frigatebirds). So, some small ground birds (e.g., the Galápagos rail) do fear large birds and thus almost any moving object that approaches from above. Galápagos organisms are threatened by a variety of additional factors, including disease (e.g., avian pox, malaria), introduced predators (e.g., cats, dogs, goats, donkeys), and parasites (e.g., Philornis downsi, currently the scourge of Darwin’s finches)— for information on these afflictions, see Parker (2018). Finally, they are threatened by habitat destruction (see Trueman et al. 2013) and irresponsible tourism (see González- Pérez and Cubero- Pardo 2010).

13. In such an isolated and remote location, it must be very difficult to conduct scientific research up to the standards of today.While there remain plenty of challenges to research in the archipelago, Galápagos is home to two major centers of research activity, each with libraries, labs, vehicles, and full- plus part- time research staff. These centers make the work of national and in-ternational scientists in the islands a lot easier than it would otherwise be. Moreover, they also offer educational programs and public outreach activities of benefit far be-yond the community of scientists.

The larger center, located on the outskirts of Puerto Ayora, Santa Cruz Island, includes the adjacent headquarters of the Galápagos National Park Directorate (GNPD) and the Charles Darwin Research Station (CDRS), run by the Charles Darwin Foundation (CDF). Although independent and separately funded organ-izations, the Park Directorate and the Research Station have worked closely to-gether since both were founded when the National Park was created in 1959. Nearly all the research described in this book has been vetted and facilitated by these two institutions. They have jointly carried out many of the conservation efforts described in the text (for example, tortoise breeding programs in Chapter 3, invasive species campaigns in Chapter 4). Both research and conservation are featured in their public outreach efforts and in the open- to- all CDRS Exhibition Center.

The smaller center, but still top quality, is in Puerto Baquerizo Moreno on San Cristóbal Island, home to the Galápagos Science Center (GSC). The GSC began in 2006 as a partnership between two universities, the Ecuadorian Universidad San Francisco de Quito (USFQ) and the University of North Carolina at Chapel Hill (UNC- Chapel Hill). USFQ has run an extension campus in Galápagos since 2002, with its own facilities and classrooms on San Cristóbal. In 2011, the part-ners worked together to add a lovely research facility to the extension campus, including laboratories for marine ecology, terrestrial ecology, microbiology, and spatial analysis and modeling. UNC- Chapel Hill also maintains a Center for Galápagos Studies (CGS) at its home campus, which offers Galápagos- related teaching, research, and outreach opportunities in Chapel Hill and administers those on San Cristóbal.

Component institutions at both centers maintain accessible, informative websites about their missions, programs, social outreach, and special opportunities that are highly recommended:

https:// www.galapagos.gob.ec/ en/ https:// www.darwinfoundation.org/ en/ https:// www.usfq.edu.ec/ en/ galapagos- science- center- gschttps:// galapagos.unc.edu/ gsc/


Appendix A 5

14. Because the human inhabitants of Galápagos have been exposed to generations of scholars working in the islands, evolution is widely accepted among local people.Although many local residents are well versed in the evolutionary history of life, some— especially those self- identifying as evangelical protestants— do not accept ev-olution and actively proselytize an anti- evolution theology. Underscoring the point, the Seventh Day Adventist Church of Ecuador, with local sanctuaries on Santa Cruz and San Cristóbal Islands, recently opened a creation museum and research center on Santa Cruz. An article on the church’s website describes the opening:

The Origins Museum of Nature, located on the main Charles Darwin Avenue in Puerto Ayora, the tourist hub of the Galápagos, combines touchscreen televisions and virtual- reality headsets with fossils and giant tortoise shells to offer visitors an interactive experience where they can study the rich natural history of the legendary Pacific islands. Away from the exhibit hall, two mu-seum rooms have been dedicated for scientific research. . . . In an interview, South American Division president Erton Kölher described the Origins mu-seum as “an invitation to think about something different. . . . After visiting, [people] might start to realize that a special hand must be behind the pro-cesses of nature. . . .” L. James Gibson, a scientist and director of the Adventist Church’s California- based Geoscience Research Institute, noted that conser-vation is a hot topic among scientists on Galápagos, and he voiced hope that the museum’s research center might provide an opportunity to connect care for the environment to the Creation story. (https:// www.adventistmission.org/ state- of- the- art- adventist- museum- opens- on- Galápagos)

More generally, Basset (2009) has an informative chapter about the activities of creationists in Galápagos, including interviews with several creationist guides who lead tours for visitors (Chapter 15). Happily, recent surveys of Galápagos high school teachers (Cotner et al. 2016, 118) indicated that evolution is still strongly represented in schools: “87% of the biology teachers in the islands state that they enjoy teaching about evolution; 89% are proud of the connections between Galápagos and evolu-tion; and 95% confirm that they specifically enjoy teaching about Galápagos and the history of evolutionary thought.”

16. Because of the scientific importance of Galápagos, research and conservation activity there must be well funded.Because the topic of funding is vast and complicated, let me focus simply on the ex-ample of the Charles Darwin Research Station (CDRS), which is the partner orga-nization to the Galápagos National Park Directorate and which is managed by the Charles Darwin Foundation (CDF). Most visitors are surprised to learn that CDRS receives no financial support from the Government of Ecuador or from the Park’s ad-mission fees, and that it sometimes struggles to maintain adequate funding. The years 2011 through 2014, for instance, were particularly difficult for the CDRS, with many research and outreach cutbacks and staff reductions. It rebounded by 2017, when the Foundation’s total income was US$4.64M, up 13.2% from 2016, which is very modest given the scale of its personnel, facilities, research projects, outreach activities, and exhibit areas for the public. CDF relies heavily on external sources— over 60% from grants and 32% from donations— with just 6% to 7% of its budget from endowments


6 Appendix A

and internal resources. Key support comes from the Galápagos Conservancy (of the United States), Galápagos Conservation Trust (of the United Kingdom), the Zoological Society of Frankfurt, COmON Foundation, Helmsley Charitable Trust, Lindblad Expeditions/ National Geographic, Ecoventura, and IGTOA (International Galápagos Tour Operators Association). One way to help with research and conser-vation efforts in the islands is to think of ways to help support CDF. The same can be said for other nongovernmental entities working in Galapagos.

17. In recent decades, there have been too many tourists in Galápagos each year, overcrowding its visitor sites and facilities.Asserting there to be too many tourists in Galápagos in 2018, the Fodor company, for example, placed Galápagos on the list of “Fodor’s Top 10 Places To Not Go in 2018” (Fodor’s Travel 2017). Although the growth in total tourism was alarming before the coronavirus epidemic, and must be capped in any event, responsible educational tourism still warrants promotion. What will help Galápagos toward sustainability is more visitors who are genuinely conscientious ecotourists, supporting both con-servation efforts and local human livelihoods. These are folks who have done their homework and come ready to learn, to enjoy making sense of what they see, and to help in some concrete way. As argued in this book, responsible ecotourism is one of the most sustainable livelihood options for Galápagos.


APPENDIX B

Key Processes in the Giant Tortoise Radiation

Enough is known from both genetics and geology to piece together a broad outline of the processes that led to separation of populations in the adaptive radiation of Galápagos tortoises described in Chapter 3. The following summary is based on the ground-breaking analyses done by Poulakakis et al. (2012 and 2020), using both phylogenetic techniques and paleogeographic reconstructions of the islands to highlight three main processes: dispersal— the migration of some number, generally small, of colonists to form a new population, vicariance— the splitting of a population by physical means into two or more subpopulations, and extinction. To date, the analyses are based on mitochondrial DNA (mtDNA) which has a higher mutation rate than nuclear DNA (owing to inefficient DNA repair), thus providing more variability for analysis.

In their first analysis of small segments of tortoise mtDNA, Poulakakis et al. (2012) dated the colonization of tortoises from the mainland to 3.2 MYA, on either the Española or San Cristóbal islands of the time (Figure B1.A). The population survived, many years passed, the Nazca plate moved slowly east, and a major volcanic event sometime before 2 MYA created a new western island in the archipelago— an island that would later become the separate islands of Floreana, Santa Cruz, and Pinzón. This first study estimated that the large island was colonized by dispersal from San Cristóbal about 1.74 MYA (Figure B1.B). In later work, Poulakakis et al. (2020) revised that estimate to 1.54 MYA.

(A) Pliocene; 3 million years

San Cristobal

Espanola3.20

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Figure B1. Early dispersal and vicariance events in Galápagos tortoise evolution. In these reconstructions, ranging from 3 MYA (left) to 1 MYA (right), the large dark “bowl” (upper left) marks Fernandina’s current location, a surrogate for the volcanic hot spot; black trapezoids mark volcanoes active at the given time. A, About 3.2 MYA (large arow), giant tortoises from the mainland succeeded in colonizing a first island, assumed here to be San Cristóbal. B, Then, sometime before 2 MYA, a volcanic event created a large island to the west (shown as Santa Cruz and Floreana), which received tortoises by dispersal from San Cristóbal around 1.74 MYA (dispersal events are represented here by small arrows). Approximately 0.82 MYA, there was a dispersal from Española to Santa Fé. C, At 1.38 MYA, a successful dispersal took


8 Appendix B

place from San Cristóbal to Santiago, which later broke away from Santa Cruz. Around 1.26 MYA, a vicariance event split Pinzón’s population from the large island, and around 0.85 MYA, another vicariance event split off Floreana’s population. In this way, a mix of dispersal and vicariance distributed tortoises widely over the changing islands of the archipelago, setting up their eventual differentiation into 15 distinct tortoise species. Source: Republished with slight modifications by permission of N. Poulakakis from N. Poulakakis et al. 2012. “Unravelling the Peculiarities of Island Life: Vicariance, Dispersal and the Diversification of the Extinct and Extant Giant Galápagos Tortoises.” Molecular Ecology 21, no. 1: 160– 73. Permission of John Wiley and Sons conveyed by Copyright Clearance Center, Inc.

Figure B1. Continued

But dispersals were far from the full story. The data suggest that a first vicariance event about 1.26 MYA separated off Pinzón volcano with its own sister tortoise population (Figure B1.C). A second vicariance event, at roughly 0.85 MYA, separated the Floreana tortoise population from that of Santa Cruz. These vicariance events formed the separate tortoise populations on the islands known today as Pinzón, Floreana, and Santa Cruz. Eventually, Santiago split from Santa Cruz with its local tortoise population.

As the phylogeographic scenario continues, the number of dispersals rises, both be-cause more islands had colonies by this point and because more volcanoes continued to emerge from the seafloor. Tortoises continued to disperse from Española: to Santiago at 1.38 MYA, to Santa Fé at 0.82 MYA, to San Cristóbal at 0.65 MYA, and, at 0.3 MYA, all the way to Pinta following the current (see text, Figure 3.7). Once the volcanos of Isabela began emerging, as much as 0.8 MYA (Geist et al. 2014), dispersals also took place from Floreana to Sierra Negra (0.65 MYA) and Santiago to Wolf Volcano, both on Isabela Island (0.28 MYA). Internal terrestrial dispersals followed (about 0.47 MYA) as lava flows filled in between volcanoes and Isabela took on its present configuration. One more no-table dispersal from San Cristóbal, at 0.43 MYA, brought a second colonization to Santa Cruz, giving rise to the second tortoise species there today, C. donfaustoi. By this analysis, today’s diversity of Galápagos tortoises is a product of both dispersal and vicariance.

Poulakakis et al. (2020) have more recently repeated the analysis using the complete tortoise mtDNA genome, providing more detail and more accurate date estimates. This new work revealed four major discrepancies with the earlier analysis. First, the site of the original colonization

“was not San Cristóbal or Española, but a [prior] proto- island that later gave rise to San Cristóbal and Española. The second is that the species currently living on Española (C. hoodensis) did not derive directly from the ancestral lineage living on this proto- island, but resulted from a more recent colonization event from San Cristóbal, well after the two islands separated. The third discrepancy has to do with the source of colonization of southern Isabela, which according to [the new] study was western Santa Cruz rather than Floreana. The fourth discrepancy involves the lineages on the islands of Santa Cruz, Pinzón, and Floreana, which were proposed in Poulakakis et al. (2012) to have [arisen] through vicariance. . . with the isolation of Pinzón Island (C. duncanensis; 1.02 Mya), and Floreana Island (C. niger; 0.55 Mya) from the remnant landmass of Santa Cruz (C. porteri). The scenario supported by our analyses here instead involves three dispersal events and one extinction event (one dispersal from San Cristóbal/ Española to the united landmass Santa Cruz, Floreana, and Pinzón, one extinction from Santa Cruz, Floreana, and subsequent dispersal events from Pinzón to Santa Cruz, and then Santa Cruz to Floreana).”


Appendix B 9

In this newer scenario, vicariance plays a role only via extinction: evolving tortoise populations on Santa Cruz and Floreana evidently went extinct after they separated from Pinzón. Later, by this account, Santa Cruz was recolonized from Pinzón, and Floreana then from Santa Cruz.

Given the ocean currents of the archipelago, it is hard not to be a least slightly skeptical of these last findings: they require floating tortoises to colonize against the strong, pre-dominant current in one case (from Pinzón to Santa Cruz) and across that current in the other (from Santa Cruz to Floreana). Could both have occurred during slack currents of El Niño events? Such issues guarantee that tortoise phylogenetics will remain a promising arena for future research.


APPENDIX C

Why Only One Marine Iguana Species?

Chapter 5 reviews evidence indicating that the evolutionary radiation of marine iguanas generated only subspecies differences among the branches, not full species differences, as in land iguanas. The question is, “Why not?”

One possible answer could be that there was “not enough time.” But this answer flies in the face of genetic evidence: the split of the ancestral lines leading to marine and land iguanas took place about 4.5 MYA (see Figure 5.2B), leaving plenty of time for evolution to work its wonders with the separate marine lineage. In tortoises, for comparison, 3.2 MY since colonization was adequate for evolutionary radiation from one ancestor into 15 dis-tinct species. Moreover, marine iguanas’ average generation time is about one- twelfth that of the tortoises (5 years for a female marine iguana vs. 60 for a Wolf Volcano tortoise— see IUCN 2004a, 2004b). That means more opportunity for intergenerational evolutionary processes to take place. In addition, 4.5 MY was enough for the differentiation of three species of land iguanas (Figure 5.4). Why has Amblyrhynchus cristatus remained a single lineage across more than 4 MY, with only subspecies differences, and even those have emerged only recently (within a maximum of 230,000 years; Figure 5.2B)?

A number of creative hypotheses have been proposed to explain this intriguing phenomenon:

Hypothesis A: Sex differences in interisland iguana migration impede differenti-ation. Rassmann et al. (1997a) found contrasting patterns for mitochondrial ge-netic (mtDNA) markers and nuclear markers among marine iguana populations on different islands. Since mtDNA is maternally inherited, the differences seemed to point to male migration:

The interisland migration rates of male marine iguanas appear to be higher than those of the females and seem to homogenize the nuclear gene pools of iguana populations throughout large parts of the archipelago. This finding is particularly interesting because the island populations of all other Galápagos lizards, i.e., the land iguanas (Conolophus), lava lizards (Tropidurus) and geckos (Phyllodactylus), are thought to be genetically isolated (Wright 1983; Snell et al. 1984). The marine iguanas differ from these taxa especially in that they regularly and voluntarily enter the sea to forage, and this may be the most significant factor enhancing the nuclear ge-netic cohesion of this species. (Rassmann et al. 1997a, 449, emphasis added)

But then why did the pattern change enough around 230,000 years ago for subspecies differences to appear? Did something at the time impede male migration? Geological evidence indicates that islands became more numerous and closer together over the same interval (Geist et al. 2014), which would likely increase migration. Following up on Rassmann (1997a), Steinfartz et al. (2009, 14) found, using new genetic analysis techniques, that “[none produced] significant evidence for sex- biased dispersal in ma-rine iguanas.” Instead, they proposed a different hypothesis for the “extremely shallow divergences within Amblyrhynchus” as follows (MacLeod et al. 2015, 4).


Appendix C 11

Hypothesis B: Inter- island migration of both sexes leads to frequent hybridization and “masks speciation in the evolutionary history of the marine iguana” (MacLeod et al. 2015, 1). There is much to recommend this line of reasoning. First, we have evidence from the “natural experiment” of sister land iguana species (whose round tails impede efficient aquatic mobility) that did differentiate, from the very same beginning, into three surviving species. Second, we also know that marine iguanas do migrate between islands, and one seems to have made it as far as Isla de la Plata, 1,000 km away.1 In their sample of 454 iguanas on San Cristóbal Island, MacLeod et al. (2015) found 10 iguanas (2.2%) to be immigrants from Española or Santa Cruz— all the more impressive because they must have swum up- current for much of the journey.2 In the same study, moreover, they found evidence of incipient within- island speciation between iguanas from the northeast and southwest. The two findings suggested the conclusion that “hybridization with individuals from other islands prevents the completion of this process” of within- island species for-mation (p. 7) As they see it.

two distinct evolutionary processes are acting in parallel on San Cristóbal: Incipient within- island speciation is evident, but at the same time introgressive hybridization with individuals from other islands prevents the completion of this [speciation] pro-cess on an archipelago- wide scale. . . . Thus, although A. cristatus appears as a single phylogenetic species, incipient speciation events, made visible here . . . [in the] snap-shot provided by highly variable markers, may well have also occurred in the evolu-tionary past of this species. (MacLeod et al. 2015, 7)

In this view, interisland hybridization is a force for “lineage fusion” or “de- speciation,” much as also described recently among Darwin’s finches on Daphne Major (Grant and Grant 2014) and among Wolf Volcano tortoises (Garrick et al. 2014). The full implications of the argument were highlighted in a review by Miralles et al. (2017, 28):

It seems therefore likely that local adaptation and speciation in Amblyrhynchus [have] been continuously arrested and masked by hybridization. We hypothesize that this evolutionary mechanism enhances evolutionary potential and facilitates marine iguana survival across the archipelago, in the context of extreme climatic fluctuations which can result in dramatic starvation events on the different is-lands. . . . The marine iguana therefore appears to remain as a single species over an evolutionary time scale, but one which absorbs adaptations from local specia-tion events across various populations into a common gene pool via hybridization (MacLeod et al. 2015). In turn, this suggests that maintaining the genetic diversity of marine iguana populations is vital for their long- term survival.

1 This documented case, of a marine iguana showing up on Isla de la Plata, Ecuador, 1,000 km east of Galápagos along the coast of the mainland (Arteaga et al. 2019, 24), is especially impressive given the force of normal ocean currents in the region. 2 Galápagos currents slacken or stop during El Niño events, in principle facilitating interisland migration. But as Chapter 5 emphasizes, instead, starvation is a major problem for marine iguanas at those times.


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12 Appendix C

But is hybridization among marine iguanas so frequent and reliable across time as to prevent even one speciation event in over 4 MY of marine iguana history? That’s suggesting that marine iguana ancestors migrated out across the millennia to diverse is-lands of the archipelago, including Darwin and Wolf over 150 km (90 miles) to the north of Isabela, that they began evolving distinct local adaptations, and then, in all cases, that subsequent hybridization assimilated variants back into the common gene pool. Over those distances, not even one exception in 4 MY? It seems too good to be true. And so that leads me to propose two other hypotheses.

Hypothesis C: Today’s marine iguanas are the sole surviving lineage of earlier colonizations that died back in one or more local catastrophic events in the last few million years. By this hypothesis, marine iguana ancestors evolved a competent set of adaptations for the marine niche, and then colonized a number of diverse islands of Galápagos, where they prospered and differentiated into some number of incip-ient or completed species. Then, a catastrophic event or several— devastating El Niños, widespread eruptions, new diseases, or other widespread calamities, singly or in combination— killed off all iguana populations but one. That one population somehow persevered— maybe by virtue of a novel adaptation, the specifics of its lo-cation, or merely chance— and then rebounded from the bottleneck to become the sole surviving lineage. The last of these archipelago- wide catastrophes would have ended by 230,000 years before the present, allowing the surviving lineage to then di-versify into subspecies with the “starburst” pattern we see today.

This hypothesis has a lot going for it. Widespread calamities do befall Galápagos organisms, and species do go extinct, or nearly so, under the influence of repeated vol-canic eruptions, El Niño events, parasites, and disease. It is often argued that Fernandina’s endemic tortoises were devastated by recent lava flows, to the point where one last indi-vidual was found and carried off after taxidermy by the 1905‒1906 California Academy expedition (see James 2017; a second tortoise was found on Fernandina in 2019, but its au-thenticity has not yet been established). Beheregaray et al. (2003) provided an additional example: today’s Alcedo Volcano tortoises on Isabela survived a major dieback when the volcano erupted violently about 100,000 years ago. Even a small change in the duration or intensity of that eruption could well have killed them all. For another example, models show that El Niño has the potential to cause archipelago- wide extinction of Galápagos penguins (Chapter 8). The same is true for West Nile disease and land birds (see Kilpatrick et al. 2006; Eastwood et al. 2014) and for the parasitic fly Philornis downsi and various species of Darwin’s finches (Chapter 6). Any one of these calamities could co- occur with others, elevating the probability of archipelago- wide die- off. Extinction is a fact of life in island populations, ranking on par with colonization as one of the most basic processes in “island biogeography,” as discussed in Chapter 3.

Proponents of Hypothesis B did consider alternative C, only to dismiss it. As they say, the really recent divergence of marine iguanas, compared to that of sister- genus Conolophus, “could imply that marine iguanas experienced a massive archipelago- wide decline in the Pleistocene. Despite records of catastrophic crashes of Amblyrhynchus populations through El Niño events [citing Laurie 1990], the effects vary greatly between islands [citing Steinfartz et al. 2007], making an archipelago- wide extinction rather un-likely” (MacLeod et al. 2015, 5‒6). But to reach this conclusion, they ignore two impor-tant considerations. First, El Niños vary widely in frequency, intensity, and duration. In their study, Steinfartz et al. (2007) focused on a single El Niño in 1997‒1998. Given great


Appendix C 13

variability in the El Niño phenomenon, it is surely misleading to generalize from a sample of one. Second, they ignore an important conclusion of their own earlier work (Steinfartz et al. 2007, 1): “studies that seek to evaluate the [population or] genetic impact of El Niño must also consider the confounding or potentially synergistic effect of other environ-mental and biological forces shaping populations.” The near- extinction in the 1990s of marine iguanas on Marchena Island is a case in point: the 1997‒1998 El Niño event caused a major bottleneck on Marchena, all the more serious because it closely followed a major eruption on the island. Further research is warranted: available data do not yet reject Hypothesis C.

Hypothesis D: Marine iguanas were “delayed by adaptation” to their new algal feeding niche. By this hypothesis, the ancestral marine iguana colonists arrived early on one island, or a few adjacent islands, in the eastern archipelago. They established a small but viable population that fed on the novel diet of low- tide seaweed. The pop-ulation numbers and distribution would have increased, if only slightly, with every incremental advantage in foraging and seaworthiness as, over generations, natural selection generated tail flattening, sharper front teeth, improved snorting, and en-dosymbiont tolerance of salt water, enabling access to submerged algae.3 Along the way, they could well have experienced intermittent diebacks caused by the calamities of Hypothesis C. El Niño would have affected them severely, especially compared to their “sister lineage” of land iguanas.4 These iguanas would have remained a single population for millennia, much like the Galápagos cormorant (Chapter 8), which also underwent radical lifestyle changes in Galápagos and remains constrained to this day to small numbers and a restricted range. As with cormorants, the Equatorial Undercurrent (EUC) might initially have played a key role for the ancestral iguana population, providing a geographically localized extra- rich supply of edible algae.5

Today we think of marine iguanas as fully seaworthy animals with impressive survival and reproductive resilience. Hypothesis D suggests that the full constellation of these features took many years to evolve to their current forms. Only after aiding iguanas to surmount their incessant challenges— of feeding on algae, swimming/ diving for better access, coping with cold water, ridding themselves of salt, enduring El Niños, etc.— would their evolved features have offered, as a byproduct, improved interisland colonizing ability. It is tempting to speculate that their hormone- mediated shrinkage in the face of food scarcity was the culminating adaptation making them fully capable colonizers. But

3 During this time, introgression with the sister lineage on land must have been rare. They do hy-bridize today on South Plaza Island, although there’s a general suspicion that the hybrids are infertile (see Rassmann et al. 1997b). 4 Consider El Niño: rain and warm temperatures are no big deal for land iguanas, who, as a result, surely end up with a greater supply of food even as marine iguanas are starving. Comparable priva-tion for land iguanas would come during La Niña dry spells but, even then, they have an advantage. Land iguanas are major consumers of Opuntia cactus, and Opuntia is specifically adapted to pro-longed desert conditions. So even in the worst of ENSO events, land iguanas have at least this one food source. 5 The paleogeological reconstruction of Galápagos 5 MYA by Geist et al. (2014, 157) shows several small islands that could have worked as a first home for marine iguanas. Following the arguments of Karnauskas et al. (2017), these islands would also have experienced at this time the strong, nutrient- rich upwelling of the EUC on their western shores, which would greatly enhance the food supply for marine iguanas, as it does near Isabela today.


14 Appendix C

it was more likely the whole host of adaptations working in concert that enabled their ex-pansion out to diverse islands.

Hypotheses C and D are appealing for different reasons, but current data seem to me insufficient so far to decide between them. One last finding is intriguing in connection with Hypothesis D. Additional evidence from MacLeod et al. (2015, 4) suggests that di-vergence among extant marine iguana populations is actually “exceedingly young,” more like 0.03 MYA (CI 0.02‒0.06). From a paleogeography perspective, this refined estimate puts marine iguana divergence at or near the time range of the last glacial maximum (LGM, roughly 20,000 to 30,000 years before present). Back then, the polar ice caps grew large enough that sea level in Galápagos fell more than 120 m below its current level. At the LGM, “There were many more islands, the cumulative [area above sea level] of the archipelago was greater, and many of the islands were connected” (Geist et al. 2014, 155), including, perhaps, Santa Cruz, Isabela, and Fernandina. Receding ocean levels would have exposed more coastal plains and provided more easily accessible algae, thus fueling the large population expansion suggested by genetic data (see Steinfartz et al. 2009, 10). Since there were many more islands, average distances between them would have been less, surely increasing the rate of successful interisland colonization. LGM timing thus fits nicely with Hypothesis D and may help to explain the iguana’s sudden diversification at that time. From Hypothesis C’s perspective, LGM’s timing would have been a simple coincidence— except in the case of disease transmission, which would have been facili-tated by the increased proximity of islands.

Whatever the case, Hypotheses C and D seem to me to be the “best horses in the race.” Further genetic analysis is needed to distinguish between them and to help us understand the more than 4 million years that marine iguanas existed as a monospecific lineage.


APPENDIX D

Methods and Sources for Interaction Analysis (Chapter 6)

Appendix D1: The Interaction Matrices

A key analysis in Chapter 6 rests on a database of interactions among plants and birds as reported in the literature. There are both advantages and disadvantages to using such a database. One advantage is that the data draw upon the expertise of a group of field workers who know very well the organisms and habitats involved in the study. Another advantage is that the hypothesis in the mind of the analyst cannot even unconsciously bias the recorded interactions (although, of course, there may be a similar bias on the part of the reporting observers). A disadvantage, however, is that such a study may tell us more about the interests and behavior of scientists (e.g., what they study and where) than it tells us about the flora and fauna under study. An interaction may not be reported simply because it has not attracted interest, rather than because it does not occur. This fact must always be borne in mind when interpreting results and is another reason why I prefer the term “exploratory” for the hypothesis tests of the chapter. A series of field experiments with test plant seeds and controls would help to fully convince us about the preliminary conclusions offered here.

Another issue presented by this database is what I call “discontiguous distributions:” a given bird cannot possibly interact with a cactus or a daisy that is not present on the same island. That occurrence should not be treated the same as when the bird and plant species do not interact although both are present in a place. Fitting examples are provided by the grey and olive warbler finches: one or the other species occurs on all the islands included in the data set, but their distributions are discontiguous, with zero overlap. If the species were listed separately in Figures 6.8 to 6.10, large spurious “holes” (with zero shading) would show in the matrix for every plant that is not on the same island with a given warbler finch. The spurious holes disappear if the data for both warbler finch species are combined as I have done here (thus the label “warbler finches”), for then there is one warbler finch on every island with a plant species in the figure. I used this same solution for the entry “cactus finches,” combining tallies from cactus finch, medium cactus finch, and large cactus finch species, since they do not co- occur on the same islands. Similarly, the “mockingbirds” entry in the figures is a composite of four species, because three of them occur on only one island each, which would generate many spurious “holes” of zero shading if each species were tallied separately. Finally, a similar solution was used for a plant entry in Traveset et al. (2015) given as “Scalesia spp.” (unspecified Scalesia spe-cies). I have assumed that “Scalesia spp.” is S. pedunculata for this analysis to minimize the number of potentially spurious holes in the figures. Although I thereby changed the number of different interactions slightly, the overall pattern of interactions remains unaf-fected by this assumption.


16 Appendix D

On the advice of Dr. Lynn Gale, statistician, tallies of the interactions shown in this appendix were converted to proportional shading using the 0% to 100% brightness scale available in Microsoft Excel. Below are three figures— D1, D2 and D3— one for each in-teraction analysis in Chapter 6, featuring the arid zone, humid zone, and both zones to-gether (without control plants). The figures include the kinds of interactions reported (designated by letters) as well their source, keyed by number to the bibliography in Appendix D2.

Figure D1. Arid- zone interaction matrix. Summarized here are the arid- zone interactions described in the literature between sample bird species (at left) and plant species (across top). Both birds and plants include “test species,” hypothesized to interact heavily with each other, plus “control species,” predicted to show many fewer interactions. Each form of interaction is represented by a letter (key below), and by subscript numbers referring to numbered sources in the accompanying bibliography (Appendix D2). This figure confirms that the group of ground finches (Geospiza) have many and diverse interactions— a “thicket” of them, we might say (outlined in green)– with the four Opuntia test species, plus unspecified “Opuntia species” (at top). Within the ground finches, there is an especially high density of interactions between cactus finches and test Opuntias. There are many fewer interactions between ground finches and control trees, Parkinsonia aculeata and unspecified Acacia species. Interactions are also less dense between control birds and Opuntias (outlined in orange). A total of 174 interactions are included. Notes: For simplicity, all members of the tree finch clade are shown as Camarhynchus. In other sources, vegetarian finches and woodpecker finches are sometimes split out under the genus names Cactospiza or Platyspiza. “CERT.” refers to the genus name of warbler finches, Certhidea. “S-b ground finches” refers to sharp-beaked ground finches. Subscript numbers refer to numbered references in Appendix D2. Key: F = frugivory; P = pollination (includes pollen transport, flower- feeding); S = seed predation; D = seed dispersal; N = nests built; I = insects foraged; O = other feeding (cactus pad, etc.).


Appendix D 17

Figure D2. Humid- zone interaction matrix. The array of species follows the form of the previous figure: birds at left, trees across the top. Here, however, the test birds are the tree finch group (Camarhynchus), minus the vegetarian finch (a control), plus the warbler finches (Certhidea). The test plant is the tree species Scalesia pedunculata— we were unable to locate adequate data for other tree Scalesia species. Key findings of this analysis are the “thickets” of interactions (outlined in green) between warbler finches and Scalesias, and between the tree finch group, minus the vegetarian finch, and Scalesias. The figure includes 54 humid- zone interactions, of which 28 (52%) are with tree finches, and another 9 (17%) are with warbler finches, for a total of 37 (68.5%) with humid- zone test birds. Only one interaction was reported for the vegetarian finch, with the Pisonia floribunda control species. Key: F = frugivory; P = pollination (pollen transport, flower- feeding); S = seed predation; D = seed dispersal; N = nests built; I = insects foraged; O = other feeding (cactus pad, etc.). Subscript numbers refer to numbered references in Appendix D2.


18 Appendix D

Appendix D2: Sources for Figures D1, D2, D3, and Corresponding Figures in Chapter 6

The source numbers below are keyed to the interactions listed in Figures D1 to D3. 1. Abbott, Ian, L. K. Abbott, and P. R. Grant. 1977. “Comparative Ecology of Galápagos

Ground Finches (Geospiza Gould): Evaluation of the Importance of Floristic Diversity and Interspecific Competition.” Ecological Monographs 47, no. 2: 151– 84.

2. Boag, Peter T., and Peter R. Grant. 1984. “Darwin’s Finches (Geospiza) on Isla Daphne Major, Galápagos: Breeding and Feeding Ecology in a Climatically Variable Environment.” Ecological Monographs, 54, no. 4: 463– 89.

3. Chamorro, Susana, Ruben Heleno, Jens M. Olesen, Conley K. McMullen, and Anna Traveset. 2012. “Pollination Patterns and Plant Breeding Systems in the Galápagos: A Review.” Annals of Botany 110, no. 7: 1489– 1501. https:// doi.org/ 10.1093/ aob/ mcs132.

4. Christensen, Rebekah, and Sonia Kleindorfer. 2009. “Jack- of- All- Trades or Master of One? Variation in Foraging Specialisation across Years in Darwin’s Tree Finches (Camarhynchus spp.).” Journal of Ornithology 150, no. 2: 383– 91.

Figure D3. Summary interaction matrix for arid and humid zones together, excluding interactions with control plants for both zones. Green boxes represent dense “thickets” of interaction, and control species interactions are outlined in orange. Boxes labeled “Controls 1” show interactions between arid- zone plants and tree finches plus control birds; “Controls 2” show interactions between humid- zone plants and ground finches plus control birds. A total of 200 interactions are tallied here, of which 41 (20.5%) pertain to the humid zone, leaving 159 (79.5%) in the arid zone. “Controls 2” interactions in the upper panel are particularly sparse. Key: F = frugivory; P = pollination (pollen transport, flower- feeding); S = seed predation; D = seed dispersal; N = nests built; I = insects foraged; O = other feeding (cactus pad, etc.). Subscript numbers refer to numbered references in Appendix D2.


Appendix D 19

5. Cimadom, Arno, Angel Ulloa, Patrick Meidl, Markus Zöttl, Elisabet Zöttl, Birgit Fessl, Erwin Nemeth, Michael Dvorak, Francesca Cunninghame, and Sabine Tebbich. 2014. “Invasive Parasites, Habitat Change and Heavy Rainfall Reduce Breeding Success in Darwin’s Finches.” PLOS One 9, no. 9: e107518. https:// doi.org/ 10.1371/ journal.pone.0107518.

6. Dudaniec, Rachael Y., Birgit Fessl, and Sonia Kleindorfer. 2007. “Interannual and Interspecific Variation in Intensity of the Parasitic Fly, Philornis downsi, in Darwin’s Finches.” Biological Conservation 139, no. 3/ 4: 325– 32.

7. Fessl, Birgit, Sonia Kleindorfer, and Sabine Tebbich. 2006. “An Experimental Study on the Effects of an Introduced Parasite in Darwin’s Finches.” Biological Conservation 127, no. 1: 55– 61.

8. Fessl, Birgit, and Sabine Tebbich. 2002. “Philornis downsi— A Recently Discovered Parasite on the Galápagos Archipelago— A Threat for Darwin’s Finches?” Ibis 144, no. 3: 445– 51.

9. Grant, B. Rosemary. 1996. “Pollen Digestion by Darwin’s Finches and Its Importance for Early Breeding.” Ecology 77, no. 2: 489– 99.

10. Grant, B. Rosemary, and Peter R. Grant. 1981. “Exploitation of Opuntia Cactus by Birds on the Galápagos.” Oecologia 49, no. 2: 179– 87.

11. Grant, B. Rosemary, and Peter R. Grant. 1996. “High Survival of Darwin’s Finch Hybrids: Effects of Beak Morphology and Diets.” Ecology 77, no. 2: 500– 509.

12. Grant, B. Rosemary, and Peter R. Grant. 1982. “Niche Shifts and Competition in Darwin’s Finches: Geospiza conirostris and Congeners.” Evolution 36, no. 4: 637– 57.

13. Grant, Peter R., James N. M. Smith, B. Rosemary Grant, I. J. Abbott, and L. K. Abbott. 1975. “Finch Numbers, Owl Predation and Plant Dispersal on Isla Daphne Major, Galápagos.” Oecologia 19, no. 3: 239– 57.

14. Grant, Peter R., and B. Rosemary Grant. 1980. “The Breeding and Feeding Characteristics of Darwin’s Finches on Isla Genovesa, Galápagos.” Ecological Monographs 50, no. 3: 381– 410.

15. Grant, Peter R., and B. Rosemary Grant. 1987. “The Extraordinary El Niño Event of 1982‒83: Effects on Darwin’s Finches on Isla Genovesa, Galápagos.” Oikos 49, no. 1: 55– 66.

16. Grant, Peter R., and K. Thalia Grant. 1979. “Breeding and Feeding Ecology of the Galápagos Dove.” Condor 81, no. 4: 397– 403.

17. Grant, Peter R., and Nicola Grant. 1979. “Breeding and Feeding of Galápagos Mockingbirds, Nesomimus parvulus.” The Auk 96, no. 4: 723– 36.

18. Grant, Peter R., and B. Rosemary Grant. 1997. “Hybridization, Sexual Imprinting, and Mate Choice.” American Naturalist 149, no. 1: 1– 28.

19. Guerrero, Ana Mireya, and Alan Tye. 2009. “Darwin’s Finches as Seed Predators and Dispersers.” Wilson Journal of Ornithology, 121, no. 4: 752– 64.

20. Heleno, Ruben, Stephen Blake, Patricia Jaramillo, Anna Traveset, Pablo Vargas, and Manuel Nogales. 2011. “Frugivory and Seed Dispersal in the Galápagos: What Is the State of the Art?” Integrative Zoology 6, no. 2: 110– 29. https:// doi.org/ 10.1111/ j.1749- 4877.2011.00236.x.

21. Kleindorfer, Sonia, Katharina J. Peters, Georgina Custance, Rachael Y. Dudaniec, and Jody A. O’Connor. 2014. “Changes in Philornis Infestation Behavior Threaten


20 Appendix D

Darwin’s Finch Survival.” Current Zoology 60, no. 4: 542– 50. https:// doi.org/ 10.1093/ czoolo/ 60.4.542.

22. Kleindorfer, Sonia. 2007a. “The Ecology of Clutch Size Variation in Darwin’s Small Ground Finch, Geospiza fuliginosa: Comparison between Lowland and Highland Habitats.” Ibis 149, no. 4: 730– 41.

23. Kleindorfer, Sonia. 2007b. “Nesting Success in Darwin’s Small Tree Finch, Camarhynchus parvulus: Evidence of Female Preference for Older Males and More Concealed Nests.” Animal Behaviour 74, no. 4: 795– 804.

24. Kleindorfer, Sonia, and Rachael Y. Dudaniec. 2009. “Love Thy Neighbour? Social Nesting Pattern, Host Mass and Nest Size Affect Ectoparasite Intensity in Darwin’s Tree Finches.” Behavioral Ecology and Sociobiology 63, no. 5: 731– 39.

25. Koop, Jennifer A. H., Sarah K. Huber, Sean M. Laverty, and Dale H. Clayton. 2011. “Experimental Demonstration of the Fitness Consequences of an Introduced Parasite of Darwin’s Finches.” PLOS One 6, no. 5: e19706. https:// doi.org/ 10.1371/ journal.pone.0019706.

26. De León, L. F., J. Podos, T. Gardezi, A. Herrel, and A. P. Hendry. 2014. “Darwin’s Finches and Their Diet Niches: The Sympatric Coexistence of Imperfect Generalists.” Journal of Evolutionary Biology 27, no. 6: 1093– 1104. https:// doi.org/ 10.1111/ jeb.12383.

27. McMullen, Conley K. 1987. “Breeding Systems of Selected Galápagos Islands Angiosperms.” American Journal of Botany 74, no. 11: 1694– 1705.

28. Merlen, Godfrey, and Gayle Davis- Merlen. 2000. “Whish: More Than a Tool- Using Finch.” Noticias de Galápagos 61: 2– 8.

29. Millington, S. J., and Peter R. Grant. 1983. “Feeding Ecology and Territoriality of the Cactus Finch Geospiza scandens on Isla Daphne Major, Galápagos.” Oecologia 58, no. 1: 76– 83.

30. Nogales, M., R. Heleno, B. Rumeu, A. González- Castro, A. Traveset, P. Vargas, and J. M. Olesen. 2016. “Seed- Dispersal Networks on the Canaries and the Galápagos Archipelagos: Interaction Modules as Biogeographical Entities.” Global Ecology and Biogeography 25, no. 7: 912– 22. https:// doi.org/ 10.1111/ geb.12315.

31. O’Connor, Jody A., Frank J. Sulloway, Jeremy Robertson, and Sonia Kleindorfer. 2010. “Philornis downsi Parasitism Is the Primary Cause of Nestling Mortality in the Critically Endangered Darwin’s Medium Tree Finch (Camarhynchus pauper).” Biodiversity and Conservation 19, no. 3: 853– 66.

32. O’Connor, Jody A., Rachael Y. Dudaniec, and Sonia Kleindorfer. 2010. “Parasite Infestation and Predation in Darwin’s Small Ground Finch: Contrasting Two Elevational Habitats between Islands.” Journal of Tropical Ecology 26, no. 3: 285– 92.

33. O’Connor, Jody A., Frank J. Sulloway, and Sonia Kleindorfer. 2010. “Avian Population Survey in the Floreana Highlands: Is Darwin’s Medium Tree Finch Declining in Remnant Patches of Scalesia Forest?” Bird Conservation International 20, no. 4: 343– 53.

34. Peters, Katharina J., and Sonia Kleindorfer. 2015. “Divergent Foraging Behavior in a Hybrid Zone: Darwin’s Tree Finches (Camarhynchus spp.) on Floreana Island.” Current Zoology 61, no. 1: 181– 90.

35. Price, Trevor. 1987. “Diet Variation in a Population of Darwin’s Finches.” Ecology 68, no. 4: 1015– 28.

36. Price, Trevor D. 1984. “Sexual Selection on Body Size, Territory and Plumage Variables in a Population of Darwin’s Finches.” Evolution 38, no. 2: 327– 41.


Appendix D 21

37. Racine, Charles H., and Jerry F. Downhower. 1974. “Vegetative and Reproductive Strategies of Opuntia (Cactaceae) in the Galápagos Islands.” Biotropica (1974): 175– 186.

38. Schluter, Dolph. 1982. “Distributions of Galápagos Ground Finches along an Altitudinal Gradient: The Importance of Food Supply.” Ecology 63, no. 5: 1504– 17.

39. Schluter, Dolph, and Peter R. Grant. 1984. “Ecological Correlates of Morphological Evolution in a Darwin’s Finch, Geospiza difficilis.” Evolution 38, no. 4: 856– 69.

40. Tebbich, Sabine, Michael Taborsky, Birgit Fessl, Michael Dvorak, and Hans Winkler. 2004. “Feeding Behavior of Four Arboreal Darwin’s Finches: Adaptations to Spatial and Seasonal Variability.” The Condor 106, no. 1: 95– 105. https:// doi.org/ 10.1650/ 7293.

41. Tebbich, Sabine, Teschke Irmgard, Cartmill Erica, and Stankewitz Sophia. 2012. “Use of a Barbed Tool by an Adult and a Juvenile Woodpecker Finch (Cactospiza pallida).” Behavioural Processes 89, no. 2: 166– 71. https:// doi.org/ 10.1016/ j.beproc.2011.10.016.

42. Traveset, Anna, Jens M. Olesen, Manuel Nogales, Pablo Vargas, Patricia Jaramillo, Elena Antolín, María Mar Trigo, and Ruben Heleno. 2015. “Bird‒Flower Visitation Networks in the Galápagos Unveil a Widespread Interaction Release.” Nature Communications 6 (March): 6376. https:// doi.org/ 10.1038/ ncomms7376.

43. Villavicencio, Vanessa Coronel. 2002. “Distribución y re- establecimiento de Opuntia megasperma var. orientalis Howell (Cactaceae) en Punta Cevallos, Isla Española – Galápagos.” Thesis, Universidad de Azuay.


APPENDIX E

Methods and Sources for Population Analysis (Chapter 8)

Appendix E1. Exploratory Tests of Penguin and Cormorant Hypotheses

This appendix offers supporting material for the tests of Hypotheses 1 to 3 in Chapter 8, using the available cormorant and penguin census data. The following figures summa-rize the responses of the two species to ENSO conditions— first hypothetically, to clarify theoretical expectations of the chapter’s hypotheses in graphical form, as may be helpful to readers unfamiliar with analyses of population growth. And then I provide figures with Galápagos data, using four decades of census tallies prepared as described in section E2, together with the Oceanic Niño Index (ONI), designed by the National Oceanic and Atmospheric Administration (NOAA) to represent the warm- and cold- water swings of El Niño and La Niña, respectively.

As in Chapter 8, here I use an inverted y- axis scale on the right- hand side of each figure, such that El Niño events show as orange spikes downward— “stalactites”— and La Niña events are shown as purple spikes upward. With this arrangement, we expect the stalactites of El Niño warming— devastating to the birds’ food supply— to be roughly con-gruous with downward changes in population for cormorants and penguins. Conversely, we expect the peaks of La Niña cooling— quickly restoring the food supply— to be roughly congruous with upward changes in population for both species. We thus expect ENSO spikes, measured by ONI, and seabird counts to move in parallel, making the plots easier to interpret.

Figure E1 provides a simplified graphical illustration of the expectations from the three hypotheses. Figure E1A summarizes the predictions of Hypothesis 1, using a hypothetical solid curve for the cormorants and a hypothetical broken (dashed) curve for penguins. It shows that both cormorant and penguin populations are expected to respond to El Niño conditions (orange stalactite below the blue band of neutral ONI values) with popula-tion decreases. It also shows both populations responding to La Niña conditions (purple, above the blue band) by population growth.

Figure E1B summarizes the predictions of Hypothesis 2, using hypothetical per capita rates of population change. A positive rate of change means the population has increased since the prior census and thus is growing. A negative rate of change means the popu-lation has decreased since the last tally, and thus is declining. Per capita rates have the advantage of controlling for the different population sizes of the two species. Figure E1B shows that the penguin population is expected to change slightly more rapidly per capita than the cormorant population, both in the decreases expected with El Niño conditions and in the increases expected with La Niña events.

Figure E1C summarizes the predictions of Hypothesis 3, showing more directly how per capita rates of population change are expected to vary in response to ENSO conditions.


Appendix E 23

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Figure E1. Graphical representation of predictions from Hypotheses 1 to 3 of Chapter 8. Both species are represented by hypothetical population numbers or growth rates (left- hand scale): cormorants (C, solid curves) and penguins (P, broken curves). Hypothetical El Niño events (orange) and La Niña events (purple) are shown on the inverted ONI scale (right) against an ENSO- neutral band (middle). A, Hypothesis 1 predicts that both populations will decrease in response to El Niño events and increase in response to La Niña events. B, Hypothesis 2 predicts that Galápagos cormorants will have lower rates of population flux


24 Appendix E

Because ONI is a monthly index, but per capita rates of population change span a year, the plot uses a composite variable, cONI, developed with the assistance of Dr. Lynn Gale, statistician, to summarize an organism’s ENSO experience during the full census year (see Appendix E2). The broken curve represents penguins who show relatively high re-sponse rates across the range of cONI values (from La Niña conditions, left of cONI = 0.0, to El Niño conditions, right). The solid cormorant curve has a similar shape but less mag-nitude across the cONI range. In the middle of both curves lies a hypothetical “zone of resilience” predicting that penguins and cormorants will maintain, largely by behavioral responses (e.g., fishing deeper, behavioral thermoregulation), low per capita rates of pop-ulation decrease in the face of mild El Niños (“3a”), and similarly low per capita growth rates in the face of mild La Niñas (“3b”). Note that, by Hypothesis 3, adjustments made by the birds facing mild ENSO events effectively extend their “ENSO neutral” zone.

The exploratory tests that follow here and in Chapter 8 for each hypothesis consist of comparing the expected responses, like those in Figure E1, with actual responses using data from Galápagos, spanning various ENSO events and most of four decades.

Chapter 8 treats Hypothesis 1 in some detail. Here let me jump right to Hypothesis 2, which proposes that penguins show a sharper, more pronounced response to ENSO events than cormorants. For an exploratory test of this hypothesis, I opted to work with per capita rates of population change over the same four decades of time as in Figure 8.6. Per capita rates give the rate of change per year per individual bird, which thus controls for differences in the population sizes of the two species. Figure E2 displays the results of this exploratory test, using the data set prepared as described in Appendix E2. As in Figure E1, the solid curve corresponds to cormorants, while the broken or dashed curve represents penguins.

Unfortunately, there are more gaps in the penguin data for this time period than for the cormorants. Where there are comparable figures following El Niño years, like 1997‒1998 (very strong El Niño), 2002‒2003 (weak to moderate El Niño), and 2006‒2007 (weak El Niño), Figure E2 shows that the cormorant per capita rates of change are less negative or even slightly positive compared to penguin declines. When a La Niña event comes along, as in 1985 and 1998‒2001, the penguin per capita rates of change reach slightly higher

compared to penguins, positive and negative, in the face of ENSO events. The prediction is based on calculating the annual changes of both populations in A as per capita rates (smoothed for clarity). The horizontal reference line marks per capita rate of population change = 0.0. C, Hypothetical relationships between per capita rates of population change for each species and the composite ENSO indicator, cONI. Horizontal line again marks the 0.0 rate of per capita population change. Hypothesis 3 predicts that cormorants and penguins will show some “El Niño resilience” (labeled “3a”) during mild El Niño events and some “La Niña resilience” (“3b”) during mild La Niñas. In these intervals, per capita rates of population change for each species are expected to remain slightly positive, or only slightly negative. The overall penguin and cormorant curves are not symmetrical: the positive responses to La Niña (left side) below the resilience interval 3b are expected to taper as reproductive limits are reached, whereas the negative responses to El Niño outside resilience interval 3a show no limit until each population reaches zero. Note that during mild El Niños both curves only dip to become seriously negative at the star. Per Hypothesis 2, the cormorant curve is slightly flatter (less responsive) than the penguin curve.

Figure E1. Continued.


Appendix E 25

positive levels, as shown, compared to the cormorant rates. In short, the prediction of Hypothesis 2, that cormorant rates of change will be relatively buffered on the way down (Hypothesis 2a) and on the way up (Hypothesis 2b), compared to penguins, receives sup-port from these data.

As a related test of Hypothesis 2, and a first exploratory test for Hypothesis 3— that both cormorants and penguins have evolved forms of resilience in the face of ENSO— I use a different kind of graph. This one plots per capita rates of population change as a function of the cONI for every census year, a number that handily summarizes the ENSO conditions experienced by organisms during the year since the previous census (cONI is explained in Appendix E2).

Figure E3 shows the results of this third test for penguins (only), again using smoothed curves to represent the general trend of plotted points. As expected, the curve moves from positive rates of per capita change at negative cONI values (La Niña conditions) to negative rates of change at positive cONI values (El Niño). The overall curve nicely

Seabird Per Capita Rates of Population Change by Year, 1970–2009

0.6

0.4

0.2

0.0

–0.2

Per c

apita

rate

of p

opul

atio

n ch

ange

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1970 1975 1980 1985 1990 1995 2000 2005 2010

2

1

0

War

mer

Col

der

–1

–2ONIPenguins (N = 20)

Cormorants (N = 28)ENSO event

ColdWarm

Vertical ref lines mark strongest EI Nino years (1972–73, 1982–83, 1997–98)~

Figure E2. Per capita rates of change in the Galápagos cormorant (solid curve) and penguin populations (broken curve) for the decades 1970‒2010. This figure offers an exploratory test of Hypothesis 2, predicting that cormorants will show less population flux relative to penguins in the face of ENSO events. Smoothed curves are shown, fitted to census data points (using a LOESS algorithm, see Appendix E2). In response to the 1997‒1998 El Niño (third vertical dotted line from left), both curves dip, but penguins dip considerably more, to a rate of – 0.23 on the smoothed curve. In response to two La Niña events (1985, 1999‒2001), the penguin rate of increase also rebounds more steeply. Where there are complete census data for both species (N = 19), their rank orders show moderate correlation (Spearman’s rho is 0.57, p = 0.012), but the penguins generally vary slightly more rapidly. The plot provides substantial support for Hypothesis 2. Sources and methods: Appendix E2.


26 Appendix E

summarizes the penguin population’s responses to ENSO— increasing when waters are cool, decreasing when warm. The fairly steep negative slope overall echoes the rapid pop-ulation response seen above: the penguin population size shifts quickly in response to ENSO conditions. But the slopes of the curves are steeper on the El Niño side (right) of the graph than they are for La Niñas (left), indicating that stronger or more frequent La Niñas would be necessary to counteract El Niños of a given magnitude. Unfortunately, since the start of ONI data in the 1950s (not shown), strong El Niños have been twice as common as strong La Niñas (eight versus four, respectively). Sadly, the ENSO conditions that reduce penguin populations occur more frequently today than the conditions that help them grow.

Weak Mod. Strong Very S.ENSO NeutralWeakMod.Strong

0.685

9405

83

98

99

00

8996 84

01 09

0602 04

9507 03

97

0.4

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–1 0 1 2

1980

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Census

Composite ONI

Zone of Resilience

Per c

apita

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of p

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+0.25

–0.35

00

86

Figure E3. Per capita rates of population change in Galápagos penguins (smoothed, broken line) as a function of the ENSO indicator, Composite ONI or “cONI,” for the 12 month- triads of each census year. The “ENSO Neutral” zone extends from cONI = – 0.5 to cONI = 0.5. The plot has an overall negative slope: the per capita growth rate of the penguin population increases with decreasing cONI, reaching its highest value (+0.25) at the most negative cONI value (– 1.45), when the sea- surface temperature (SST) is cool (left blue arrow), and reaching its lowest value (– 0.35) during very strong El Niños (cONI > 2.0) when SST is very warm (right blue arrow). Additionally, there is an impressive “zone of resilience” (blue box) in which penguins maintain positive per capita growth rates with increasing cONI all the way to ~0.8 in the weak El Niño zone. Finally, the slope of the curve above cONI = 1.0 is steeper than the slope to the left of cONI = 0.0. Penguins are greatly affected by warm ocean temperatures and moderate or stronger El Niños. Inter- census per capita growth rates are color- coded by year. The gray band is a 0.95 confidence band, providing a representation of uncertainty around the smoothed curve. Sources and methods: See Appendix E2. (N = 20 plotted points for penguins.)


Appendix E 27

The figure also provides support for a “zone of resilience” (3a) in response to mild El Niño events, as hypothesized in Figure E1C, confirming the efficacy of penguin adaptations for coping with moderately warm ocean temperatures. Around the blue box, the curve of declining per capita growth in penguins deflects: left of the box, the curve appears headed close to y = 0 at x = 0, that is, for nearly zero growth rate at ENSO- neutral conditions, and from there to negative growth rates for positive values of cONI. Instead, the curve remains positive out to cONI = 0.8. Penguins “get by” quite well up to cONI = 1.0 (the start of moderate El Niño conditions), most likely by thermoregulatory behavior and diving deeper than usual for prey. In Chapter 8, Figure 8.7 adds the equivalent cormorant curve to the penguin curve, enabling the comparisons discussed there.

Appendix E2. Data Sources and Methods of Analysis for Chapter 8

This appendix explains the data sources and methods used in Chapter 8 for exploratory tests of its three hypotheses. I am grateful for the painstaking efforts of scientists and rangers in Galápagos who carried out censuses of both penguins and cormorants across the 40- year span of this analysis. Alava and Haase (2011) compiled much of the penguin and cormorant census data for 1969 to 2009, including from the Darwin Station archives. I am grateful to them for sharing their compilation with me.6 Regular annual censuses only began in 1993, so many earlier population estimates for one or both seabirds were missing from these data.

To fill in a gap in cormorant data from 1970 to 1979, I supplemented the Alava and Haase data set with data from Tindle et al. (2013). Because the Tindle data included juveniles for most years, and I wanted to include juveniles all years for consistency, I used their direct cormorant tallies for 1970– 1973 and 1977– 1979 (interpolated from Tindle et al. 2013, Figure 2A). Their tallies for 1974– 1975 included no juveniles, so I substituted their “derived numbers”— that is, estimates for the study colony produced from their marked- recapture analysis of cormorants in a wider area. Their derived population num-bers include estimates for total number of adult males and females, plus an estimate for juveniles and immigration. Because they found, on average, only a single net immigrant per year, that correction was easily made, and I thus had a consistent cormorant data set for the 1970s (excepting 1976). I multiplied each value obtained from Tindle et al. (2013) by 9, based on their own estimates that the population they studied represented between 10% (Valle 1995) and 12% (Tindle et al. 2013) of the total Galápagos cormorant popu-lation. Later testing suggested that the estimates I used for this period are slightly con-servative, which seems appropriate. To fill another small gap, I used the figure of 727 cormorants in 1998 (Travis et al. 2006), a previously unpublished census count.

6 Due to several inconsistencies in their early 1980s tallies, I turned to values derived from Valle and Coulter (1987, 277) for the 1980– 1984 cormorants sequence, as follows. I used Valle and Coulter’s 1980 and 1983 tallies for cormorants multiplied by Valle’s (1995) average “correction index” of 1.211. For 1981– 1982, there are no data because there were no censuses on record for either sea-bird. I estimated the 1984 population based on Valle and Coulter’s (1987, 278) number of 143 nesting pairs, multiplied by the average number of fledglings recruited into the population per pair in an ENSO- neutral year, 1.4 (from Harris 1977), yielding an estimated gain in the population of 200 indi-viduals. So I estimated the 1984 population as Valle and Coulter’s 1983 estimate, 409 plus the increase of 200, or 609 cormorants, multiplied by Valle’s average correction index of 1.211, yielding 737.5.


28 Appendix E

I followed the advice of Vargas et al. (2005) in correcting the published penguin census data. Their study used “capture- mark- resighting” techniques to estimate census underreporting, finding that censuses reach only about 57% of the total penguin popula-tion. For 1983 to 2009 (except 1997, see below; and 2008, a missing value in the Alava and Haase data set), I used the numbers in Boersma et al. (2013, 300, Table 16.3), corrected as Vargas et al. (2005) suggested for converting census tallies to full population estimates. For the years 1970, 1971, 1980, and 1997, I used the Boersma et al. (2013) data from Table 16.3 without the Vargas correction, because those tallies employed a more complete census method and could not be corrected the same way.

These various efforts produced a data set, with gaps, of roughly four decades of estimates for each species— a small but analytically tractable database.7 I had decided that it would be helpful to analyze per capita rates of population increase for each species and not just total internnual rates of change, because cormorant and penguin population sizes are almost always different, making it difficult to compare simple rates of change or slopes of the curves. For each year, the per capita rate of change was calculated as the population difference from the previous census (positive, negative, or zero) divided by the initial pop-ulation size, and adjusted by division for the difference in years between the censuses (1 if consecutive years, up to 3 for a 2- year gap, the maximum we allowed).

To measure ENSO swings, I use the Oceanic Niño Index (ONI), produced by the National Oceanic and Atmospheric Administration (NOAA), obtained on 8/ 6/ 17 from Golden Gate Weather Services.8 ONI divides the calendar into 3- month averages centered on the middle month (a technique that smooths what might otherwise be overwhelming monthly variation). These 3- month means are conveniently called “month- triads.” Thus, the month- triad “ASO” refers to the three- month average for August, September, and October, used as the referent datum for the month of September. Golden Gate Weather Services (2017) further describes ONI as follows:

The Oceanic Niño Index (ONI) has become the de facto standard that NOAA uses for identifying El Niño (warm) and La Niña (cool) events in the tropical Pacific. It is the running 3- month mean SST anomaly for the Niño 3.4 region (i.e., 5oN– 5oS, 120o– 170oW). Events are defined as 5 consecutive overlapping 3- month periods at or above the +0.5o anomaly for warm (El Niño) events and at or below the – 0.5 anomaly for cold (La Niña) events. The threshold is further broken down into Weak (with a 0.5 to 0.9 SST anomaly), Moderate (1.0 to 1.4), Strong (1.5 to 1.9) and Very Strong (≥ 2.0) events. . . . For an event to be categorized as weak, moderate, strong or very strong it must have equaled or exceeded the threshold for at least 3 consecutive overlapping 3- month periods.

As noted, the El Niño 3.4 region begins at longitude 120° W, roughly 3,300 km (2,000 miles) west of Galápagos, and runs to 170° W (8,900 km, 5,500 miles from Galápagos).

7 The data were limited in several ways that affected subsequent analysis. There were gaps for both species in the sequence of census years; fewer penguin than cormorant censuses (24 versus 30, re-spectively), and an imperfect match of census years with ENSO events. Although the analysis uses the longest time span available, it still produced only three very strong El Niños— happily for the organisms, but challenging for the analyst— and only penguin censuses for two of those. 8 Because of climate change, the calculation of ONI has been revised since the values used here were downloaded, probably making our data set slightly conservative. For an explanation of the change and further updates, see http:// origin.cpc.ncep.noaa.gov/ products/ analysis_ monitoring/ ensostuff/ ONI_ change.shtml


Appendix E 29

Because warm waters at the start of El Niño flow or “slosh” across the Pacific from west to east, there is inevitably a delay of some days between warm- water peaks in the Niño 3.4 region and the corresponding peaks in Galápagos. This variable time lag contributes to small temporal differences between spikes in ONI data and population responses in Galápagos.

Five consecutive overlapping 3- month periods must fall outside a given threshold to qualify as an El Niño or La Niña event. To facilitate interpretation, the first two figures in Chapter 8 ignore the ragged “sawtooth” of ONI variation between – 0.5 and +0.5— the “neutral” years— and show only events that extend beyond those values. I follow suit in Figure E1, representing ENSO- neutral conditions by a horizontal blue band. In addition, because seabird populations generally decline with food scarcity from El Niño conditions, the ENSO events of Chapter 8 show El Niño below the ONI = 0 mark, and La Niña above the ONI = 0 mark. Although this requires an inverted ONI axis on the right side, I believe it also makes the plots easier to interpret.

For the analysis and statistical graphics of Chapter 8, I was very fortunate to have assis-tance from Dr. Lynn Gale, career statistician, formerly of the Center for Advanced Study in the Behavioral Sciences at Stanford. Using R for statistical computing and graphics (R Core Team 2017), she produced the graphical displays in Figures 8.7 and 8.8.9 In Figures 8.7 and E2, for each species, smooth LOESS curves (locally weighted polynomial regressions) were fitted to the census data points (plotted using the left- side axis). We chose not to extrapolate census data gaps of more than two consecutive years, and so fitted two separate smoothed curves for each species, as shown in Figures 8.7 and E2.

In Figure 8.7, the LOESS curve for the few points of the early penguin years was fitted with span = 1.0 (due to algorithm constraints); the other three curves, with sufficient data points, were visually fitted using span = 0.5 (allowing more “wiggle”). In Figure E2, three smooth curves employed span = 0.4, based on visual inspection of alternative span values. The early years’ cormorant curve used span = 0.3, required for algorithm constraints on the number of parameters fitted for a curve with many up/ down swings relative to the number of data points. We plotted census data points at month 9 of the calendar year (that is, the center month of triad ASO), which means these points do not fall directly on the vertical grid lines. The colored elements, upward spikes and downward “stalactites,” per-tain to the right- side axis showing ENSO- event severity and duration based on the ONI, with 12 monthly values per year, allowing finer gradations.

In a second round of statistical analysis, per capita growth rates for each species were plotted against selected ONI variables as follows. In an earlier analysis of El Niño’s im-pact on penguin populations, Vargas et al. (2006, 110) compared population growth rates with the “mean normalized sea- surface temperature (SST) anomalies for the pe-riod December– April that preceded each penguin count.” But El Niños and La Niñas are variable both in onset and duration, such that SST measures averaged over 5 months may not always accurately reflect the full El Niño “challenge” to the organisms. In this study, we explored two different measures based on SST anomalies. First was the max-imum ONI value from the 12- month triads up to and including the (assumed) September census each year. The rationale was that “ONI max” would measure that year’s most se-rious El Niño challenge to the organisms (downplaying any La Niña benefit during that year). The second was an aggregate measure, suggested by Dr. Gale, that we call “cONI”

9 Dr. Gale put to good use the R contributed packages, “ggplot2” (Wickham 2009) for statistical graphics and “dplyr” (Wickham et al. 2017) for data manipulation in this project.


30 Appendix E

for “composite ONI.” The cONI values were calculated as follows (capital letters refer to months of the year; for example, O = October):

(1) A “census year” was defined as the interval from month- triad SON (i.e., September- October- November) of calendar year x to ASO of calendar year x + 1, for the 29 years for which we were able to calculate one or both per capita rates of popula-tion change from the penguin and cormorant data.

(2) Each census year was categorized as an El Niño year, a neutral year, or a La Niña year according to whether the corresponding ENSO event (by the five consecutive month- triads rule) fell anywhere within the interval SON to the following ASO.10

(3) For each of 12 El Niño years, the value for cONI was defined as the upper quartile of ONI for that year. For each of eight neutral years, the value for cONI was the me-dian ONI for that year. And for each of nine La Niña years, the cONI was defined as the lower quartile of ONI for that year.11

Using median and quartiles in a composite measure for each 12 month- triad census year has two advantages. First, these are common nonparametric summary statistics that are resistant to outliers. Second, it does not downplay La Niña months nor neutral months of these years, providing a single measure with better symmetry for capturing the organisms’ experience in a 12- month period. We chose to use the cONI summary statistic rather than maximum ONI because of these features, as well as the fact that for our census years, it succeeded in a complete ordering of the years by their ENSO event- type (with one exception), whereas the maximum ONI statistic did not do nearly as well, even in the warm ENSO years.

In Figure E3, the LOESS curve was fitted to penguin points with span = 0.9. The gray 95% pointwise confidence band around the LOESS curve represents uncertainty of the fitted curve. In Figure 8.8, the LOESS curve was fitted to cormorant data with span = 0.9. Both smooth curves are displayed in Figure 8.8 to allow visual comparison of general features without cluttering the plot with too many symbols (circles and triangles).

I am very grateful to Dr. Gale for her patient, ever- thoughtful help with the Chapter 8 analysis.

10 Two exceptions were allowed: 1977– 1978 and 2006– 2007 were allowed an additional month- triad at the start in order to meet the five consecutive month- triads rule for a weak El Niño event in both years. 11 The quartiles, following the default definition in R, and median are three statistics that divide the (ordered) 12 month- triad ONI values of a given census year into four classes, each containing three values. The highest three ONI values are greater than or equal to the upper quartile. Six ONI values are greater than or equal to the median, and six are less than or equal to the median. The lowest three ONI values are less than or equal to the lower quartile.


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APPENDIX A Some Common Misconceptions About Galápagos