I POPULATION SIZE of BLUE-FOOTED BOOBIES IN

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POPULATION SIZE OF BLUE-FOOTED BOOBIES IN GALÁPAGOS: EVALUATION OF INDICATIONS OF POPULATION DECLINE

DAVID ANCHUNDIA

A Thesis Submitted to the Graduate Faculty of

WAKE FOREST UNIVERSITY GRADUATE SCHOOL OF ARTS AND SCIENCES

in Partial Fulfillment of the Requirements

for the Degree of

MASTER OF SCIENCE

Biology

May 2013

Winston-Salem, North Carolina

Approved By:

David J. Anderson, Ph.D., Advisor

Miles R. Silman, Ph.D., Chair

Todd M. Anderson, Ph.D.

DEDICATION

This work is dedicated to the memory of my loving mother Juana Isabel

Gonzalez. I thank her for all the support and the encouragement she gave me to study sciences. Also I thank my father Oswaldo Anchundia for his constant support during all this time. I will always appreciate all that they have done for me; this degree is dedicated to them.

David J. Anchundia Gonzalez

ACKNOWLEDGEMENT

I want to express my sincere gratitude to my advisor Prof. David John Anderson for all the advice, motivation, enthusiasm, and immense knowledge that he shared with me during my M. S. study and research. Also I thank my lab mates Jacquelyn Grace,

Felipe Estela, Emily Tompkins, and Terri Mannes for the help and guidance in my research. I want to thank the Prof. Miles Silman and Prof. Michael Anderson, who were part of my thesis committee, and the Professors of the Biology Department from Wake

Forest University who shared their knowledge with me. I would like to express my gratitude to: Prof. Kathryn Huyvaert from Colorado State University, who helped me in parts of the analysis and modeling parts of the project; Kyle Anderson from Idaho State

University, who helped with part of the GIS analysis; Professors Peter and Rosemary

Grant from Princeton University, who provided unpublished breeding and attendance data from Daphne Island; and Lisa Balance and Robert Pitman from the National Marine

Fisheries Service (La Jolla) for sharing unpublished at-sea distribution data.

I thank all the field assistants that helped me in the collection of the data, and also staff scientists and collaborators of Charles Darwin Research Station who helped me in the collection of the data for the population estimate. I want to thank the Galápagos

Conservancy and Galápagos Conservation Trust for the funding support of the project.

Finally I want to thank Wake Forest University and the Biology Department for giving me the opportunity to be part of this prestigious University.

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TABLE OF CONTENTS

List of Tables ...... vi

List of Figures ...... vii

Abstract ...... viii

Introduction ...... ix

CHAPTER 1. Population size of blue-footed boobies in Galápagos: evaluation of indications of population decline ...... 1

Abstract ...... 1

Introduction ...... 2

Methods ...... 5

Results ...... 13

Discussion ...... 19

Tables ...... 26

Figures...... 33

Literature Cited ...... 39

APPENDIX 1 ...... 43

APPENDIX 2 ...... 53

APPENDIX 3 ...... 59

CHAPTER 2. Implications of movement over the Perry Isthmus, Galápagos for seabird biogeography...... 62

Abstract ...... 62 iv

Introduction ...... 62

Methods ...... 63

Results ...... 64

Discussion ...... 65

Tables ...... 68

Figures...... 69

Literature Cited ...... 70

Curriculum Vitae ...... 71

LIST OF TABLES

CHAPTER 1.

Table 1. Schedule of visits and activities done at each colony ...... 26

Table 2. Number of blue-footed boobies counted during coastline surveys in 2011

(single observer, over 11 weeks) and 2012 (double observer, five teams, over three

consecutive days) ...... 27

Table 3. Breeding activity at colonies in 2011 and 2012 in relation to historical

maxima ...... 28

Table 4. Representation of prey items by weight in regurgitation samples ...... 29

Table 5. Log likelihood, AIC, and derivative values for models explaining variation in

breeding POTENTIAL (see Methods) ...... 31

Table 6. β values and their standard errors for predictors in the model set of ...... 32

CHAPTER 2.

Table 1. Schedule of visits and activities done at each colony ...... 68

LIST OF FIGURES

CHAPTER 1.

Figure 1. Location of focal and non-focal colonies, islands, and section scanned per

day during coastal survey of June 2012 ...... 33

Figure 2. Proportion of total grams of each fish in regurgitation samples ...... 34

Figure 3. Proportion of total number of fish items collected in regurgitations samples 35

Figure 4. Foraging sites of adults blue-footed boobies, identified from kernel analysis

of tracks from GPS tags ...... 36

Figure 5. Duration and number of trips for tagged individuals ...... 37

Figure 6. Distribution of juvenile blue-footed boobies in the Eastern Tropical Pacific

from ship-based survey, 1988-2006 ...... 38

CHAPTER 2.

Figure 1. Isabela Island and location of the Isthmus Perry ...... 69

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ABSTRACT

Census and survey data for blue-footed boobies (Sula nebouxii excisa) in

Galápagos, Ecuador from 2011-2012 indicated a population reduction, probably by more than 50%. Anthropogenic effects such as introduced predators are unlikely to explain this decline, because islands with and without such factors exhibited the same low breeding. The poor reproduction seems to be linked to scarcity of food. Previous studies indicated that sardine and herring (Clupeidae) support successful breeding, but these fish were mostly absent from the diet. Elsewhere in the eastern Pacific, sardines have decreased dramatically in abundance by natural processes in the last 15 years, as part of a well-documented and apparently natural cycle. This cyclic change in abundance provides an explanation for the recent demographic changes in blue-footed boobies in Galápagos.

Land barriers have been mentioned as one of the mechanisms that promote population differentiation in pelagic seabirds, at what scale does a land barrier restrict gene flow effectively? Genetic data indicate that the Isthmus of Panamá does restrict gene flow in boobies and other seabirds. I evaluated a smaller isthmus (the Perry

Isthmus) that could allow transit across Isabela Island, Galápagos. Daytime observations revealed crossings by > 48 blue-footed boobies and > 2 frigatebirds (Fregata spp.). If the

Isthmus of Panamá (width = 57 km, height = 26 m above sea level) is assumed to be an effective barrier to gene flow in boobies, but the Perry Isthmus (width = 12.5 km, height

23 m) is not, then these two features bracket the minimum dimension of historical and contemporary landforms that can interrupt gene flow in this group.

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INTRODUCTION

This work consists of two chapters related to seabirds from Galápagos Islands.

Chapter one focuses on the estimation of the population size of Galápagos blue-footed boobies (Sula nebouxii excisa) and demographic and ecological factors that may affect it.

Population size and evaluation of population decline are the main foci of the first chapter.

The second chapter tests an assumption of part of the first chapter (the frequency of movement of blue-footed boobies over land, and evaluates implications of movement over the Perry Isthmus, Galápagos for seabird biogeography.

Blue-footed boobies have a wide distribution on many separate sites on the eastern Pacific coast over more than 20,000 km2, but the blue-footed booby subspecies from Galápagos is present only in Galápagos. It is important to update the population number, to see if there is any decline, because several species in Galápagos are showing population reduction. Due to the lack of information on this subspecies in the last two decades, some information on Nazca boobies (Sula granti), which is well-studied in

Galápagos, was used to better interpret the potential factors affecting blue-footed boobies. The information provided in this thesis will help to increase our understanding of the life history of blue-footed booby. These results provide the first baseline for this species to compare with future data and qualitative comparison with past data. This information also can help us to understand food distribution for this species, and the timing and location of breeding.

Chapter two focuses on observations of pelagic seabirds flying over a large landmass. The work was done on the Perry Isthmus, the thinnest part of Isabela island.

There is not much literature about seabirds flying over land, and many of the

ix observations are anecdotal, describing observations of pelagic seabirds several kilometers inland. These sightings are attributed to natural disturbances, like storms or tropical cyclones, but information of flying deliberately over land barriers is not described.

Information about voluntary crossings of land is valuable to evaluate the counting method that I used in Chapter 1, and also to evaluate the role of land barriers in seabird biogeography.

CHAPTER 1.

Population size of blue-footed boobies in Galápagos: evaluation of indications of

population decline

ABSTRACT

Census and survey data for blue-footed boobies (Sula nebouxii excisa) in

Galápagos, Ecuador from 2011-2012 indicated a population reduction, probably by more than 50%. During the study breeding activity was nearly absent in all the colonies, with only three colonies showing any reproductive attempts, and the breeding population sizes were 1-11% of historical maxima. Anthropogenic effects such as introduced predators are unlikely to explain this decline, because islands with and without such factors exhibited the same low breeding. Comprehensive surveys of the coastline indicated that only 1.2% of the population was in juvenile plumage, indicating little successful reproduction for at least two years before the study. The poor reproduction seems to be linked to scarcity of food. Previous studies indicated that sardine and herring (Clupeidae) support successful breeding, but these fish were mostly absent from the diet, except in the central part of Galápagos, where most breeding attempts during this study occurred.

Elsewhere in the eastern Pacific, sardines have decreased dramatically in abundance by natural processes in the last 15 years, as part of a well-documented and apparently natural cycle. This cyclic change in abundance provides a straightforward explanation for the recent demographic changes in blue-footed boobies in Galápagos.

INTRODUCTION

Seabirds around the world experience the impact of natural phenomena and anthropogenic effects on population vital rates (Yorkston & Green 1997, Boersma 1998,

Tuck et al. 2001). For many species we lack appropriate information about population processes and size and about possible problems that could affect these variables because remote and sometimes ephemeral breeding locations make data collection difficult.

Many seabird populations are declining in size (Croxall et al. 2012), and frequent updates on population status may help managers to understand problems as they arise and separate natural effects from anthropogenic ones. In the Galápagos Islands, monitoring population size of some species of seabird and marine mammals has led some of them to be catalogued as endangered and critically endangered (Vargas et al. 2005, Alava &

Salazar 2006, Jiménez-Uzcátegui et al. 2006, Anderson et al. 2008). Other species are too poorly studied to allow similar evaluations; the blue-footed booby (Sula nebouxii;

Aves: Suliformes: Sulidae) is one such species.

The blue-footed booby is a medium-size seabird distributed in coastal areas of the eastern tropical Pacific, using Galápagos and islands and headlands on the west coast of

South and Central America and México to breed (Nelson 1978). Blue-footed boobies are one of the most striking seabirds of Galápagos, and one of the most famous. Despite their high profile, few studies have been done on this species. In recent years, a variety of people who have lived and worked in Galápagos for many years has suggested that the abundance of this species has decreased. El Niño–Southern Oscillation (ENSO) events have been linked to reproductive failure and adult mortality in some seabirds, and are known to cause blue-footed booby chick mortality, breeding failure, and colony

2 abandonment (Ricklefs et al. 1984). However, these anecdotal reports indicate that the size of the adult population does not vary with the ENSO cycle, and closely related species like Nazca (Sula granti) and red-footed boobies (Sula sula) show generally good breeding and attendance during non-ENSO years (pers. obs. on colonies 2011-2012).

The population size of blue-footed boobies has been documented poorly in

Galápagos; several reports have been issued but typically show only counts from one or a subset of all colonies (Appendix 1). Only Nelson in the 1960s estimated the population’s size across the archipelago, at more than 20,000 individuals (Nelson 1978). In the past,

34 regular breeding sites were known in Galápagos, with the largest persistent colonies on Daphne Major, North Seymour, Punta Cevallos, and Punta Suárez (Española), Punta

Vicente Roca (Isabela), and Cabo Douglas (Fernandina; Nelson 1978). In this study I evaluated the current population size, breeding activity, and diet of blue-footed boobies from these colonies to compare with past information.

Seabirds play an important role in marine ecosystems. They are sensitive to changes in food supply and they can be used as monitors for fish stocks (Furness et al.

1997). The published literature shows that blue-footed boobies forage mostly on fish in the families Clupeidae (sardines and herrings) and Engraulidae (anchovies) across their range (Anderson 1989, Mills 1998, Zavalaga et al. 2007, Weimerskirch et al. 2009, Cruz et al. 2012). The high energy density of these fish seems to facilitate breeding (Ricklefs

& Schew 1994, Müllers et al. 2009). In continental waters of the ETP the abundance and the diversity of these prey is higher than in the Galápagos Archipelago: three species of

Clupeidae and three of Engraulidae have been recorded in Galápagos compared to ten

Clupeidae and 12 Engraulidae in the Peruvian Upwelling (Froese & Pauly 2013).

However, while anchovies have been recorded in Galápagos, they are rare and observed sporadically (Grove & Lavenberg 1997). The industrial fishery for these families around the continental shelf is massive, while the Galápagos stocks support only a few artesenal dinghies. The population of continental blue-footed boobies seems to be stable and no concern has been expressed about a potential decline (D. J. Anchundia, pers. obs., C. B.

Zavalaga, pers. obs.). It is possible that the higher biomass and diversity of fish near the continent offer more opportunities to switch prey when preferred prey become scarce.

In previous work on breeding members of the Punta Cevallos (Española) population, Anderson (1989) observed that blue-footed boobies were highly specialized on Sardinops sagax, representing 94% of the items in the diet. Similarly, Sardinops sagax and Galápagos herring (Opisthonema berlangai) were common in diet samples from colonies of Seymour and Punta Pitt on San Cristóbal (Cruz et al. 2012). These clupeids are clearly important for Galápagos blue-footed boobies, and they also appear prominently in the diet of continental populations. The abundance of sardines around the continental shelf varies in a cyclic manner, with an approximate period of 25 years: when clupeid biomass is high, anchovy biomass is low, and vice versa (Chavez et al. 2003,

Alheit & Niquen, 2004, Bertrand et al. 2004). Thus, continental populations have the option of switching between clupeids and anchovies, depending on availability, while birds in Galápagos may not because sardines seem not to be replaced by anchovies in

Galápagos.

In this study I evaluated several hypotheses regarding population size and environmental factors influencing the blue-footed booby population in Galápagos: 1) the population of adults is smaller than in the past; 2) breeding activity is less frequent than

4 in the past; 3) low availability of prey, and clupeids in particular, influences breeding parameters such as colony attendance, breeding attempts, egg and clutch size, breeding success, and foraging trip lengths and destinations.

METHODS

Population size

I intended to use capture-mark-resight (CMR) methods to estimate the sizes of the breeding and non-breeding components of the blue-footed booby population, sex ratio, annual adult survival, and movement between breeding colonies (McClintock 2011). To this end, 879 adults were marked with two leg bands (one numbered stainless steel band and one field-readable plastic band) at five important historical colonies (Fig. 1). The majority of the birds were marked at the beginning of the study, in May 2011. In retrospect, the large number of birds available for banding on this occasion was an anomaly, and attendance was dramatically lower in later visits to these colonies. I resighted only 238 banded birds in these colonies during five resight sessions (i.e., resight probability averaged 5.5% per session) conducted at 3-4 month intervals until January

2013, due principally to low attendance and secondarily to some loss of plastic bands, rendering the CMR approach unworkable.

I used two surveys of the entire coastline of the islands south of the equator

(including all of Isabela) as an alternative measure of population size. Blue-footed boobies seldom visit the tropical, less productive waters (Houvenaghel 1978, Feldman

1986, Hayes & Williams 1989) around the five islands north of the Equator (Genovesa,

Marchena, Pinta, Darwin, and Wolf), both historically (Nelson 1978, Harris 1982) and

5 during this study (D. J. Anderson, pers. obs.); this fact justifies the exclusion of these sites from the “survey range” comprising 1100 km of coastline of 14 islands and 20 islets.

In the first survey, I made daytime counts in piecemeal fashion, covering the entire survey range in a boat at 1-8 m/s between June 3 and August 7, 2011, with a single observer (DAG) using a binocular 20-100 m from the coast. Each blue-footed booby perched on land or flying against the direction of the boat’s movement was recorded, with adult or juvenile status, latitude and longitude measured by a hand-held GPS unit, and time of day.

In the second survey, on 1-3 June 2012, I used an independent double observer technique to estimate population size (Nichols et al. 2000). With this method a primary and a secondary observer counted birds independently, with the secondary observer recording only birds missed by the primary, allowing estimation of detection probability.

Because almost no birds were breeding at the time of the survey, and I reasoned that non- breeders would spend much of their time resting on sea cliffs, justifying the choice of a boat-based coastal survey. Our group’s previous experience with this species supports this assumption, and during the survey we recorded birds sighted on the open ocean when the boats moved between islands as an additional test of the assumption. During both surveys observers gave special attention to detecting new colonies. Pairs of observers travelled on a boat moving 2-8 m/s 20-100 m from the coast, each using a binocular to detect birds on land and flying against the direction of the boat’s travel. In the single exception to this protocol, during the count in the northwest part of Santiago the boat moved > 1 km from the coast for 19 km due to hazardous navigation, so the birds on land and over water near the coast were missed. Birds sighted were recorded with GPS

6 location and binned into 30 min. travel intervals. Ten people participated in the survey: six observers from the Charles Darwin Research Station, two from Wake Forest

University Anderson Lab, and two external collaborators. To avoid counting a bird more than once, I tried to conduct the survey over the smallest time period possible to avoid movements of birds from one area of coastline to another. A limitation on the number of suitable boats available permitted a survey over three consecutive days, with 2-5 observer pairs working on a given day. All teams working on a given day counted in the same area of the survey range, with the areas chosen to minimize the possibility of birds moving between count areas during the survey (Fig. 1). On June 1, two observer pairs counted the western archipelago, reasoning that interchange between that region and rest of the archipelago was rare because few birds cross the Perry Isthmus in the middle of

Isabela each day (Chapter 2). On June 2, five observer pairs counted eastern Isabela and the eight islands and 15 islets in the central part of the survey range. On June 3, three observer pairs counted the relatively isolated islands and islets in the east, southeast, and south of the archipelago (Fig. 1).

The population estimator E[Ň] was obtained from the number of birds recorded by primary (n1) and secondary (n2; only birds not included in n1) observers during each

30 min interval (Seber 1982, Nichols et al. 2000). The population size is estimated as

2 E[Ň] = n1 /(n1-n2), Eq. 1

and the variance of E[Ň] as

2 2 4 V[Ň] = n1 n2 (n1+ n2)/(n1- n2) Eq. 2

Finally, the probability of detection is estimated as

[E]P = 1-[n2/( n1+1)] Eq. 3

Breeding

From May 2011-January 2013, I monitored breeding at four of the six historically largest breeding colonies (Daphne Major, Cabo Douglas on Fernandina, Punta Vicente

Roca on Isabela, and Seymour Norte), and one additional recently established colony

(Playa de los Perros on Santa Cruz; Fig. 1) at 3-4 month intervals. Because the breeding cycle requires 42 d. of incubation, ~100 d. of nestling rearing, and at least 28 d. of post- fledging feeding at the nest (Nelson 1978, Harris 1982), a reproductive cycle probably could not be completed without being recorded. I visited each of these five “focal colonies” at night, when attendance is highest, recording the number of adults present

(birds in juvenile plumage were never present), band numbers if visible, and the number of active nests with eggs and the number with nestlings. The fifth regularly large and active colony, Punta Suárez on Española, and three others were selected as “non-focal colonies”, and were visited three or four times each, and breeding was monitored when possible during these visits, with time of day varying (Table 1). The sixth historically large and active colony, Punta Cevallos on Española, was known to be essentially unattended through our group’s other research activities there. An additional, apparently newly established, non-focal colony on Baltra was discovered in the second year of study, and entered the study in August 2012.

If food constraint explains why birds are not breeding, this may be reflected in the energy of the female’s investment in the production of eggs. For example, female Nazca boobies lay a smaller second egg, and a smaller average clutch size, when food

8 conditions are poor (Anderson 1990). In June 2012 I measured the length and breadth of

46 eggs from the Playa de los Perros (Santa Cruz) colony with calipers (0.1 mm precision) and calculated egg volume as V = πLB2/6 (Preston 1974), where L is the length and B the breadth. I compared them with data collected during years of high attendance and successful breeding from Punta Cevallos (136 eggs in 1984 and 69 eggs in 1985). I used a single factor ANOVA and a Tukey–Kramer post-hoc test to evaluate the significance of differences. The clutch sizes from these years were compared using a chi square-test.

Diet

I attempted to collect diet samples during every visit to a focal or non-focal colony, but the irregular attendance in some colonies sometimes prevented sampling.

Only adults were sampled during late afternoon or at night, shortly after birds have arrived from daytime foraging trips. The diet samples were collected by both induced regurgitation and spontaneous regurgitation. For induced regurgitation the bird was captured in the colony and its head was enclosed in a cloth weighing bag, with the head of the bird oriented downward so gravity makes regurgitation easier. The bird was released after 30 secs. and any regurgitated prey were identified (or photographed and identified later), weighed, and measured for fork length. Any spontaneous regurgitation by a bird not in the hand was treated similarly. When possible, regurgitated prey were re- fed to the bird.

Movements

To identify foraging sites, SIMA® GPS tags were deployed only on nesting birds at their nests in the focal colonies. A total of 34 GPS units (on 20 females and 14 males) were deployed in: May and August 2011; May, August, and December 2012; and January

2013 (Appendix 2 provides details by bird). At Playa de los Perros 25 units (on 15 females and 10 males) were deployed, at Daphne Major six units (on three females and three males), and at Cabo Douglas three units (on two females and one male). The tags were deployed at night and usually recovered during the following night. Previous radio tracking elsewhere in Galápagos showed that blue-footed boobies foraged only during daylight hours and usually completed a foraging trip and returned to the nest during one daylight period (Anderson & Ricklefs 1987), facilitating recovery of the tag. The tags were configured to record the bird’s position every 10 or 15 sec. and were attached to the underside of four tail feathers using water-resistant Tesa tape®. The movements and foraging locations were subjected to kernel density analysis using ArcGIS® 10.0. This analysis calculates the density of waypoints recorded for the birds. This program’s

“generate near table” tool was used to determine the proportion of locations within 200 m of a coastline. Quantum-GIS® 1.8.0 was used to represent some maps.

Model development and data analysis

My collaborator Kathryn Huyvaert (Colorado State University) led the modeling exercise. Logistic regression was used to evaluate the associations between the binary response variable, breeding potential (POTENTIAL; the response was “yes” or “no”) and metrics of blue-footed booby foraging. Breeding potential was scored “yes” for a given colony on a given visit if the estimated number of potential breeding pairs exceeded 5%

10 of the historical maximum number of nests for that colony. The sex ratio of birds present was estimated from counts of birds attending colonies at night, by checking the size of the sexually dimorphic iris (Nelson 1978). Not all birds were sufficiently visible to identify sex, and the proportion assigned sex varied from 65-100%. The sex ratio was multiplied by the total number of adults present and the absolute number of the members of the limiting sex was identified. The number of the limiting sex was multiplied by two to estimate the number of individuals that could be paired to breed. In many cases, the adults were present but had not laid eggs; we considered them to be demonstrating

“breeding potential” by attending the colony. I used two metrics of blue-footed booby foraging: PERCAP, the per capita number of grams of clupeid fish recorded from regurgitations with weight > 0, and PROPENSITY, a measure of the propensity of birds to regurgitate when handled, calculated as the proportion of birds that did regurgitate after capture and confinement in a weighing bag for 30 secs.

A model selection process included a set of 13 models, including an intercept- only model, models incorporating the foraging metrics PERCAP and PROPENSITY, and single, additive, or interactive effects of these with other covariates that, a priori, I considered might explain additional variation in POTENTIAL. ISLAND was included as a covariate because the identity of the different islands may reflect variation in habitat or other ecological variability that influences the potential for blue-footed boobies to breed.

The temporal covariate VISIT was included, given the variability in food availability and other factors related to breeding potential that might vary over time; VISIT was coded

“1” for the June 2011 colony visits (Table 1), “2” for the August 2011 visits, etc. VISIT was not treated as a repeated measure in this analysis because the low rate of recapture

11 suggest that the majority of birds sampled from one visit to the next were new birds that had not been previously captured and sampled. This is supported by the fact that I had few recaptures of banded birds. Data were analyzed using ProcLOGISTIC as implemented in SAS v. 9.3 (SAS Institute, Cary, NC).

Model selection and inference

An information-theoretic approach (Burnham and Anderson 2002, Anderson

2008) was used to select models and for inference. In particular, I used Akaike’s

Information Criterion with an adjustment for small sample sizes (AICc) to rank the models in the model set. Models with the lowest AICc were considered the best in the set given the data. Differences between the top model and other models in the set were also calculated (ΔAICc) as were Akaike weights (AICc weights), which are estimates of the probability that a given model is the best model in the set. We also report maximum re- scaled R2 values (SAS Institute 2008) as a description of the proportion of variation explained by each model

Dispersion and distribution of BFBOs in the Eastern Tropical Pacific

Blue-footed boobies display an easily recognized juvenile plumage until age 2-3 years (Nelson 1978). Infrequent observation of blue-footed boobies in juvenile plumage could indicate low breeding success over the previous 2-3 years, or temporary emigration of juveniles from the range of the adults. To find out whether juvenile blue-footed boobies travel long distances after they fledge, I used data from ship-based surveys across the ETP between 1988-2006 (L. Ballance and R. Pitman, unpub. data).

RESULTS

Population size

In the 2011 coast survey, 7379 individuals were counted (Table 2), of which two

(0.03% of the total count) were in juvenile plumage. That survey was conducted over an

11 week period by a single observer, with significant potential for missing or double- counting individuals. In the 2012 coast survey, the probability of detection by primary observers was high (0.97), yielding very small confidence limits around the estimate of population size (6433 + 4; Table 2). In 2012, 75 juveniles were observed, all away from breeding colonies, and represented only 1.1% of the birds sighted.

These estimates apply to the portion of the population visible during daylight from boats within 100 m of the coast, and exclude birds away from the coast. Four lines of evidence indicate that few birds were outside the visual range of observers on the survey boats: 1) birds with GPS tags spent most of their foraging time within 200 m of an island’s coast (see below), well within visual range; 2) during boat travel between islands during the 2012 survey blue-footed boobies were sighted at a rate of only 2 birds/30 minutes compared to an average of 48 birds/30 minutes on the coast; 3) ~85% of birds sighted during the 2012 survey were resting on land, and not on the move; and 4) >90% of the birds seen flying during the 2012 survey were moving parallel to the coast, rather than to or from the open ocean.

Breeding

Breeding activity was much lower than historical maximum figures, with most monitored colonies containing <6% of the historical maximum (Table 3, Appendix 3).

Summing across all monitored sites, the largest number of simultaneous nests observed

(155) represents 310 breeding birds, only 4.8% of the population size estimate of 6433.

Two previously unknown breeding colonies were identified during the study, on Baltra with approximately 49 nesting (Table 3), and on the south coast of Fernandina west of

Punta Mangle, with approximately 75 adults present and an unknown number of nests.

The formerly large colony at Punta Cevallos on Española (489 nests in 1994; Townsend et al. 2002) was not monitored as part of this study, but was checked frequently as part of our ongoing research there; no more than three nests were ever present there during this study.

Most breeding attempts in which at least one egg was laid failed without producing a nestling: on visits after one in which nest with eggs were recorded, few or no nestlings or fledglings (either living or dead) were found, although incubating adults may have been present (possibly on new clutches). In the focal colonies in 2011, the total number of fledglings was 26 (nine at Playa de los Perros, nine at Cabo Douglas, and eight at Seymour), and in 2012, 59 offspring fledged (18 at Playa de los Perros, 12 at Seymour,

24 at Baltra, one at Daphne, and five at Punta Suárez; Appendix 3). December and

January were the only months in the two-year study in which I observed large offspring and fledglings, with the exception of the newly established Baltra colony, in which 24 fledglings were present in August 2012.

Clutch sizes in 2012 did not differ from those in 1984 and 1985: two eggs was the most common clutch size in all three years (χ2 = 4.28, df = 4, p > 0.05). The mean volume of eggs differed across years (X 1984 = 57.8 cc., X 1985 = 58.1 cc., X 2012 = 63.7 cc.),

F2,248 = 11.97, p < 0.001). A Tukey–Kramer post-hoc test indicated that egg volumes in

2012 were larger in volume than eggs from previous years (p < 0.001).

Diet

A total of 218 regurgitations were collected from eight colonies. Clupeids were the most common item in the samples, representing 80.2% of all items and 50.4% of the total weight (Figs. 2,3). The fork length of the fish ranged from 3 cm to 35 cm, with a mean of 6.8 cm (S.D. = 3.2).

The colonies that I visited fell into three clusters based on oceanographic habitat: the western colonies of Fernandina and Punta Vicente Roca, adjacent to the productive upwelling of the Equatorial Countercurrent with much lower sea surface temperature

(SST) than elsewhere in the archipelago (Ruiz & Wolf 2011); the central colonies of

Daphne Major, Seymour, and Santa Cruz, adjacent to a complex merging of currents and a mosaic of SST and productivity (Witman et al. 2010); and the southeastern colonies on

San Cristóbal, Española, and Floreana, in a generally less complex and less productive marine habitat. The diet composition in these regions varied, with clupeids much more common and occurring more regularly in the central cluster during this study (Table 4).

However, clupeids were collected at least once in all the colonies except on San Cristóbal and Española (Table 4).

Predictors of Breeding

Three of the 13 models were omitted from the final model set because these models had too few representatives for data combinations that included ISLAND such

15 that no maximum likelihood estimate could be derived. Of the final model set (Table 5), the intercept-only (model 10) had the highest AICc value, identifying it as the worst performing model given the data. It had a ΔAICc of 6.698 and a relative AICc weight of only 0.008, indicating that at least one of the predictors in better performing models provided meaningful information about variation in breeding potential. Examining the relative weights of each model (Table 5), models 1 and 2 have similar relative weights of

0.217 and 0.207, and those of models 3-6 are very similar to one another (0.101–0.128).

Model 7 displays a notable discontinuity, with a relative weight of only 0.059. I considered the likelihood of models 2-6 given the data to be sufficiently high to be considered informative (Burnham and Anderson 2002).

PERCAP (per capita grams of clupeids in regurgitations) appeared in three of the top six models and PROPENSITY (propensity to regurgitate anything) appeared in four of the top six models, but only as additive or interactive effects with each other or with

VISIT, suggesting interdependence in their predictive abilities (Table 5). However, the predictive values of PERCAP and PROPENSITY are highly questionable, because the

95% confidence intervals of each parameter’s β values includes zero in every instance

(Table 6). The β values associated with VISIT in the top six models were all negative, indicating that the probability of breeding declined with time, and the 95% confidence intervals did not include zero in any case.

Movements

Most of the tagged birds did not travel far from the coast; 81.9% of the GPS points during foraging trips were within 200 m of an island coastline. However, foraging

16 birds did not cross land except to fly directly from their nests to the water and back.

Many of the foraging sites identified by kernel analysis were within 200 m of an island coast (X = 44.54.x m [S.D. = 53.5]; Fig. 4). Birds at sea travelled up to 68 km (median =

11.2 km) from their breeding colony, on trips that ranged in duration from 0.4-18.1 hrs

(median = 2.3 hrs).

Birds from Playa de los Perros foraged at a variety of sites, including coastal spots like the Canal de Itabaca between Santa Cruz and Baltra and the coast of Santa Fé, and more pelagic locations to the south of the breeding colony. In contrast, most of the birds from Daphne Major foraged close to the coasts of nearby Santa Cruz, Seymour, Baltra, and Daphne Minor (Fig. 4). The three birds from Cabo Douglas all foraged within 2.1 -

4.7 km of the colony and within sight of the coast in shallower water to the east of the colony and not in much deeper water to the west, north, and south (Fig. 4).

Of the 879 birds banded in breeding colonies, 238 were resighted during later night visits to colonies. Four of these resights placed the bird in a different breeding colony from the banding site. One female banded on Playa de los Perros was resighted one year later on Seymour; one male banded on Playa de los Perros was resighted one year later at Punta Suárez, with a mate but no nest; one male banded on Daphne Major was resighted one year later on Seymour performing mate-attraction sky-points (Nelson

1978); and one female banded on Cabo Douglas was resighted three months later on

Seymour.

Distribution of BFBOs in the Eastern Tropical Pacific In December 2010, six months prior to the start of this study, I visited the Playa de los Perros colony and observed 225 fledglings, suggesting good breeding conditions at that time for this colony. However, in the coast survey done in June 2011, I observed

17 only two juveniles in the whole archipelago, and in the coast survey of 2012 I observed only 75. In the 1980s and early 1990s, when breeding conditions appeared to be better, birds in juvenile plumage were seen regularly resting on sea cliffs and flying along the coast throughout Galápagos (D. Anderson, pers. obs.). It is not clear whether most of the

225 juveniles moved outside my survey range or died before the surveys. It is important to determine where these birds in juvenile plumage live, because if they are outside the survey range during this life-history stage, their absence during the surveys may not indicate breeding failure.

The ship-based surveys across the ETP between 1988-2006 show many juveniles near the large breeding colonies on the northwest coast of South America, mostly near La

Plata Island (Ecuador), Lobos de Tierra Island (Perú), and the Gulf of California (Fig. 6).

It seems that juveniles stay close to land, and perhaps their natal colonies. I visited Isla

Santa Clara, in the Gulf of Guayaquil, site of a blue-footed booby colony of 6,000-14,000 individuals (Alava & Haase 2011), in July 2012, and I found hundreds of juveniles within

0.1–0.35 km. of the colony. It seems they stay near the island, which suggests they stay close to their colonies. In Galápagos, few individuals were recorded (77 total 2011-

2012). The lack of information for Galápagos blue-footed booby juveniles leaves uncertainty in interpretation, but following the behavior of the Santa Clara birds it is likely that the young from Galápagos stay close to their colonies.

DISCUSSION

My results indicate that the Galápagos population of blue-footed boobies is approximately 6433, plus an unknown but probably minor fraction of the population at

18 sea and out of visual range, representing a decrease of more than 50% from the only other estimate, from the 1960s. Questions can be raised about the methodology used for both estimates. Little information is available regarding the first estimate, and we do not know the technique used. Nelson (1978, p. 515) provided this estimate, first reviewing early counts from some islands and then apparently summarizing unpublished data and impressions from his own year in Galápagos (mostly in 1964) on a few islands and also from the more extensive experience of others, such as M. P. Harris, in the 1960s: “the total Galápagos [sic] population must exceed 10 000 pairs and could be substantially more…”. Without further clarification of methods and measurement error, little more can be said about this estimate except that it was made by careful scientists and probably represents at least 20,000 birds.

Regarding the second estimate, it is based almost exclusively on counts of birds resting on the coast or coastal waters, or flying within sight of the coast. The detection probability of this method was high for birds within sight of the boat, and several lines of evidence indicate that the proportion of birds missed at sea was low: most birds sighted were on land; most birds sighted flying were moving parallel to the coast; GPS tracking places most flying time within 200 m of some coast; counts while travelling between islands suggested that only 4.8% of birds were out of visual range of boats surveying the coast region; and little breeding was occurring at the time of the survey, so few to no birds were at nest sites not visible from the water. The population estimates done in 2011 and 2012 were similar, increasing confidence in the accuracy of the 2012 estimate.

Taking the 1960s estimate and my new estimate at their face values, a trend of a population decline is indicated, with the current population approximately 35% the size

19 of the 1960s population. Acknowledging significant uncertainty in the actual values, especially for the 1960s estimate, my conclusion is that the population has declined in size by at least 50% since the 1960s.

Birth, death, immigration, and emigration are the demographic processes affecting population size. Considering breeding, a very small proportion of the estimated population size (a maximum of 4.8%) even attempted to nest at formerly important colonies, and most of those attempts were unsuccessful. When fledglings were produced, they apparently died soon after becoming independent because almost no birds in juvenile plumage were seen in the two coastal surveys of the entire population.

Attendance at the former colonies in the whole archipelago during the two-year study was very low compared to historical attendance, including historical maxima (Table 3). I searched for potential new colonies during the two surveys, and found only one small colony on Fernandina. Another colony was discovered a month after the 2012 survey, on

Baltra, but both colonies are small compared with the size of past colonies. The small numbers of juveniles observed during the two censuses suggest this age group is essentially absent, probably due to the very low frequency of breeding attempts; blue- footed boobies have juvenile plumage until age 2-3 years, so this absence implies poor reproduction since at least 2009. The absence of this age class means that adults that die will not be replaced by young individuals, suggesting that the population size will continue to shrink until at least 2015. I am not able to estimate adult survival because the frequency of band resight was too low to be informative, but I assume that roughly 10% of adults die each year, based on data from a Mexican population of blue-footed boobies

(Oro et al. 2010).

Time series data from Punta Cevallos (Española) and from Daphne Major

(Appendix 3) suggest that the population decline began during the 1997-98 ENSO event.

Since 1997 the formerly large and regularly active blue-footed booby colony at Punta

Cevallos has been virtually vacant, and on Daphne Major few adults currently attend in a small part of the main crater, while in the past the main crater and a side crater was covered by up to 1600 blue-footed boobies at times. Now vegetation covers much of the past breeding site. Neither of these islands supports a possible introduced predator, and no evidence of the effects of disease have been noted among breeders or non-breeders at either site. These two colonies are in separate oceanographic habitat regions of the archipelago, but exhibit similar breeding histories, suggesting the possibility that breeding has been poor across the archipelago since 1997 and depends little on spatial habitat variation. If so, then the age structure of the current population must be strongly biased toward elderly individuals; if blue-footed boobies show actuarial senescence, as

Nazca boobies do (Apanius and Anderson 2003) in addition to reproductive senescence

(Velando et al. 2007), then the birth and death processes leading to smaller population size can be expected to accelerate.

Emigration and immigration may add or subtract individuals from the blue-footed booby population, but these processes seem unlikely to be important in this species.

Adults studied with electronic tags foraged within 100 km of land but rest at night on land (Nelson 1978, Anderson and Ricklefs 1987, this study), limiting their ability to move widely on the open ocean or transfer to the continental shelf of the Americas.

Similarly, temporary movement of juveniles away from Galápagos is not indicated by ship-based surveys, which instead show concentrations of juveniles near breeding

21 colonies (Fig. 7). Finally, the genetic differentiation of the Galápagos population (Taylor et al. 2011), considered a subspecies (S. n. excisa), from the continental subspecies S. n. nebouxii; (Nelson 1978) implies little movement between Galápagos and the Americas.

Breeding and survival are apparently the most important demographic effects on population size in this system. Why are the birds not breeding, perhaps since 1997?

Evaluation of scarcity of food as a cause of poor breeding provided mixed results.

Past data from Punta Cevallos showed that blue-footed boobies forage mostly on sardines, similar to Nazca boobies (Anderson 1989), until 1997. High abundance of sardine may was good indicator for raise nestlings and more accessible food for juveniles.

After 1997, sardines disappeared from the Nazca booby diet, but Nazca boobies continued breeding by switching to other prey (D. J. Anderson, unpub. data). In contrast, blue-footed boobies abandoned this colony (Appendix 3). Breeding also declined to virtually none on Daphne at approximately this same time (Appendix 3), and we suspect that the late 1990s was the beginning of a period of poor breeding throughout the archipelago, based on the impressions of scientists and others with long experience in

Galápagos. Data from Galápagos sea lions (Zalophus wollebaeki) suggest that sardine have become less available throughout the archipelago on approximately the same schedule as that of Punta Cevallos: they foraged mostly on sardines during the 1980s

(Dellinger & Trillmich 1997), and more recently (2008 - 2009) sardines are not present in their diet at all (Páez-Rosas & Aurioles-Gamboa 2010). Diet samples taken during this study suggest that the central archipelago has a more regular availability of sardines currently than the other regions, and on these islands is where more current breeding attempts are observed.

The logistic model identified informative models that contain food-related parameters, but the β values associated with the parameters could not be distinguished from zero (Table 6). The model evaluated the predictive ability of current diet characteristics to explain current breeding motivation. For several reasons, interpretation of the modelling must be done with caution: diet samples were taken on one or two days per four months, and this coarse-grain sampling may be unduly influenced by day-to-day variation in prey availability; the breeding parameter used a criterion of 5% of the historical maximum, which may be too lax to indicate breeding motivation reliably; and most significantly, important information associated with Island is not available, because models with island did not converge.

I offer an alternative interpretation of food availability and breeding: that clupeid availability is critical for recently independent young, and not necessarily for egg- formation and parental care. Under this hypothesis, parents should initiate breeding when the probability is high of clupeid availability five months in the future. When parents time reproduction in this way, their offspring can avoid the typically high mortality of recently independent juveniles by foraging on quality prey. When blue-footed boobies did attempt to breed during this study, their clutch sizes were similar to those from the

1980s, and egg volumes were actually larger, indicating favorable current conditions.

However, few birds attempted to breed, and I suggest that this is because parents were assessing the variable clupeid availability as insufficient to support independent juveniles. Before 1997, sardines were available consistently in space and time. Under this hypothesis, current diet characteristics are not expected to predict breeding

23 motivation well, and our model did not, if those characteristics vary over time, which they did during this study (Table 4).

Information regarding sardine abundance from the Peruvian Upwelling, east of

Galápagos, shows that the sardine population there has declined almost to absence, on the same schedule as that which I infer for Galápagos. Fishery capture declined from thousands of tons in the 1990s to 0 tons since 2002, with anchovies showing a corresponding increase (FAO, Instituto Nacional de Pesca Ecuador 2013). Sardines cycle between high and low abundance with a period of 25 years in the Pacific, linked to the

Pacific Decadal Oscillation (PDO; Chavez et al. 2003). The decline of sardines in the

ETP started in the mid 1990s, matching the decline in breeding on two colonies in

Galápagos (Appendix 3). Decline of sardines seems to not affect blue-footed boobies on the continental coast because they can switch to another high energy fish like anchovies

(Zavalaga et al. 2007), which highly abundant in the Peruvian upwelling system but not in Galápagos. I suggest that Galápagos populations of clupeid cycle in abundance on the same schedule, and for the same reasons, as continental populations. Information about fish populations in Galápagos is poor, making it difficult to compare past and present population. Some fishermen have the perception that the bait fish (including clupeids) are not abundant like they were in the past. If sardine is not abundant like in the past other animals may be showing problems similar to those of blue-footed boobies.

Introduced species have been one of the major threats for native or endemic species (Vitousek et al. 1997). In the last decades, several species have been introduced to Galápagos, affecting the fauna and flora of the archipelago. Some have speculated that the increase in cats (Felis catus) may be affecting the breeding cycle of blue-footed

24 boobies, with cats acting as a predator. However, there are islands on which cats are not present (Española, Daphne Major, Seymour, and Fernandina) and the same pattern of not breeding happens. Punta Vicente Roca historically has had a large presence of cats, and an eradication program has been conducted without success. Despite this, blue-footed boobies kept breeding until the late 1990s, which may imply that cats are not the main problem. Also one of the largest and most regular current colonies is on the island with more species introduced in Galápagos with a constant presence of cats, therefore I discard that this hypothesis. Of course, predation could happen in the islands where the cats were introduced and could enhance the breeding failure, but cats cannot account for the archipelago-wide failure.

Diseases can be another explanation of poor breeding, but I did not do any work related to this. However, during the two years and all the visits to the colonies I did not observe any apparently sick bird. Four carcasses were found on two colonies, but cause of the deaths were unknown, because the carcasses were there for long time. Avian malaria is present in Galápagos and it affects several species, mostly Passeriformes, and has not been registered that it affects sulids. Blue-footed boobies are known to have some parasites, including two endoparasites (a nematode (Contracecum sp.) and a trematode (Renicola sp.)), which they may contract from their prey. Studies of brown pelicans (Pelecanus occidentalis) show these gastrointestinal parasites had low virulence in and probably play a secondary role in population fluctuations (Greve et al.

1986).

TABLES

Dec Dec 2011/ 2012/ May Jun Aug Jan May Jun Aug Jan Colony site 2011 2011 2011 2012 2012 2012 2012 2013

FOCAL COLONIES

Playa de los Perros MN C MN MN MN C MN MN -Santa Cruz

Daphne Major MN C MN MN MN C MN MN

Cabo Douglas MN C MN MN MN C MN MN - Fernandina

Pta. Vicente Roca MN C MN MN MN C MN MN -Isabela

Seymour Norte C MN MN MN C MN MN

NON-FOCAL COLONIES

Punta Cormorant, M ,C M M ,C D D D Cuevas -Floreana

Punta Pitt M ,C M M ,C M D N D N -San Cristóbal

Punta Suárez MN MD,C MN - Española

Table 1. Schedule of visits and activities done on each colony. MN: monitoring breeding, presence of banded adults, diet sampling, at night; MD: monitoring breeding, presence of banded adults, diet sampling, at day; C: count of adults at day during coastal count across survey range.

June–July 2011 June 2012

Island # birds observed # birds observed

Isabela 4651 2320

Fernandina 426 630

Santiago 422 919

Rábida 35 16

Pinzón 93 73

Daphne Major 41 77

Daphne Minor Not visited 100

Seymour 57 132

Baltra Not visited 157

Santa Cruz 554 1025

Santa Fé 624 117

Floreana 239 393

San Cristóbal 237 413

Española Not visited 165

Total 7379 6495

Table 2. Number of blue-footed boobies counted during coastline surveys in 2011

(single observer, over 11 weeks) and 2012 (double observer, five teams, over three consecutive days; see text).

Historical maximum Maximum # Maximum # Colony site # nests nests in 2011 nests in 2012 Daphne Major 836 4 (<1%) 4 (<1%) Seymour Norte 965 16 (2%) 62 (6%) Playa de los Perros No data 73 62 Santa Cruz Cabo Douglas 1467 1 (<1%) 1 (<1%) Fernandina Punta Vicente Roca 1800 67 (4%) 0 Isabela P. Cormorant & Cuevas 134 3 (2%) 6 (4%) Floreana Punta Pitt No data 2 3 San Cristóbal Punta Suárez 256 29 (11%) 11 (4%) Española La millonaria New No data 49 Baltra colony

Table 3. Breeding activity at colonies in 2011 and 2012 in relation to historical maxima.

otal otal

“

Underline

at that site that at

. The most important prey species for each by year are identified identified are box. a with each for species The . by most prey important year

s with few regurgitations and items. For each colony, “11” = 2011 and and 2011 2012. “11” = “12”= colony, each For items. and regurgitations with s few

vertically

samplingsession

is the total grams of fish collected during that during grams collected total the is fish of year

and sum 100 to and

Table 4. Representation of prey items by weight in regurgitation samples. Numbers in the chart represent percentage of of percentage in samples. by represent items chart the in weight Representation 4. Numbers prey regurgitation Table of grams represents grams” 30

Log likelihood, AIC, and derivative values for models explaining variation in breeding POTENTIAL (see Methods). (see POTENTIAL explaining models breeding in values derivative for variation and likelihood, AIC, Log

5. Table

” and “Effect SE” refer to the the to refer SE” and “Effect ”

Table 6. β values and their standard errors for predictors in the model set of Table 4. “Effect “Effect 4. Table of set model predictors the in for errors their standard and values β 6. Table first predictor in the model (i.e., for VISIT in the top model). Underlined β values are those whose 95% confidence interval 95%VISIT β top model the in whose those the in for confidence are (i.e., Underlined predictor values model). first zero. includes

FIGURES

Figure 1. Location of focal and non-focal colonies, islands and section scanned per day during coastal survey of June 2012.

Figure 2. Proportion of total grams of each fish on the all regurgitations.

Figure 3. Proportion of total number of fish items collected in the regurgitations.

Figure 4. Foraging sites of adult blue-footed boobies, identified from kernel analysis of tracks from GPS tags. Top left: birds from Playa de los Perros colony. Top right: birds from Cabo Douglas colony with arrows indicating kernels. Bottom: birds from Daphne

Major colony.

Figure 5. Duration and number of trips for individuals tagged.

Figure 6. Distribution of juvenile blue-footed boobies in the eastern tropical Pacific from ship- based surveys, 1988-2006. Data source, L. Balance and R. Pitman: Southwest Fisheries Science

Center (L Jolla, CA).

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APPENDIX 1

Field reports by scientist that work in Galápagos, sporadic data collected on breeding and attendance of blue-footed boobies from the 1960s until 1980s.

Little formal work has been done on blue-footed boobies in the past, but field reports submitted by scientists during field visits in the 1960s until 1980s, archived in the

Charles Darwin Research Station library, helped to determine the attendance and breeding of blue-footed boobies in historical colonies. The reports were completed by scientists visiting sites for various purposes; many of them were not expert in seabird biology, and some describe the information broadly while others give more detail. The information was obtained from the archive of the library of the Charles Darwin Research

Station in Galápagos by David J. Anderson in 1987. This valuable information was important to compare with past blue-footed activities and current. The tables presented go in spatial geographic order, starting from the western colonies and ending with southeastern colonies.

Additional data for Daphne Island were provided by P. R. Grant and B. R. Grant, and by David J. Anderson.

Isabela Island Colony Tagus Cove

Date #Nest Juveniles Comments 22-Aug-1974 200 Tourist trail suspended, there were many birds covering the trail Sep/Oct -974 200 The nest were deserted, linked to explosions in Beagle Crater, and earthquake in South American mainland 14-Jun-1977 ~800 adults congregation no nest 1/4 of the nest had chicks, 577 adults in the 14-Jul-1977 60 colony May/Jun-1977 No birds observed, colony abandoned 28-Jul-1980 29 28 Half of the nests had chicks 21-Jul-1981 10 pairs

Colony Punta Vicente Roca Jan/Feb-1978 Chicks of all sizes 25-Oct-1978 Many birds courting, some with large young 25-Jun-1979 1335 Mostly incubators, hawk attacked male, and he abandoned the egg and the hawk ate the egg 8-Apr-1980 951 pairs, courting and laying eggs 14/15-May-1980 Abundant chicks, some with event 4 chicks 14-May-1980 Cats bothering nesting birds 20-Aug-1980 No nesting, few observed 20-Nov-1980 Large number of birds nesting 22/31-Jul 1981 1500 pairs Jan-1983 604 529 Most of the nests had small and medium chicks Sep-1984 355 270 All the nests had large chicks Insignificant chick mortality compared to 17-Jan-1985 Seymour and Daphne 17-Jan-1985 1834 15/16-May-1985 1000 Areas abandoned, probably due to plant growth Sep-1985 155 619 All the nest had chicks

Colony Beagle Crater 21-Jul-81 1000 pairs

Colony Caleta Iguana 21-Jul-81 300 pairs

Colony Marielas islets 21-Jul-81 50 pairs

Colony Punta Moreno Aug/Sep-1976 15

Colony Tortuga island 26-Jul-75 47

Fernandina Island Colony Cabo Douglas Date #Nest Juveniles Comments 22/31-Jul-1981 ~2000 pairs 9-Oct-1981 1 mile colony long, it was not observed before 1978 16/25-Oct-1982 Many juveniles flying, high mortality of them 10-Jul-1984 Many chicks and juveniles 24-Feb-1985 Many 100s in all stages 21-Sep-1985 1487 1575 Around 70% of the nests had small, medium, and large chick, > 1600 adults were courting 20-Feb-1987 150 dead chicks, absence of adults

Daphne Island

Date #Nest Juveniles Comments 27-May-1964 156 10-Jan-1970 425 25 479 dead chicks 10-Apr-1970 465 215 11-Dec-1973 16 adults Several 4-Aug-1974 dozen 18-Aug-1974 55 27-Dec-1974 30 100 birds dead 27-Dec-1974 100 dead young birds, 30 eggs deserted Feb/Aug-1975 450 15-Jul-1975 291 662 pairs Jun/July-1975 36 37 dead chicks, water warm; feeding infrequent, siblicide increased, later water became cold siblicide decreased 11-Aug-1975 19 372 112 pairs, 92 chicks dead 11-Oct-1975 143 pairs 76 dead chicks and juveniles 21-Nov-1975 21 98 pairs, 92 dead chicks and juveniles 3/24-Jan-1976 350- 400 4-Mar-1976 325 9-Jan-1977 104 1 May/June-1977 60 577 adults, most of them displaying 12-May-1977 400 adults 12-Jun-1977 580 adults 14-Jun-1977 800 adults 17-Jun-1977 60 18/26-Oct-1977 Chicks all stages 23-Dec-1977 201 128 adults 25-Dec-1978 350 15-Nov-1978 164 381 92 dead chicks 12-Dec-1978 54 448 Most of the nests had chicks Jan-1979 250 dead fledglings 22-Jan-1979 51 half chicks, half eggs 27-Apr-1979 411 1/10 nests had chicks 26-May-1979 677 1/4 nests had chicks 25-Jun-1979 1355 1% of the nests had chicks 19-Sep-1979 18 177 13-Apr-1980 602 8 60 % of the nests had chicks 5-Aug-1980 29 28 107 adults

28-Apr-1981 628 79 60% of the nests had chicks small and large 4-Jul-1981 Many small, few large chicks Feb/April 1982 620 Before El Nino 1982 17-Aug-1983 104 adults 1-Aug-1984 165 239 adults 1-Mar-1985 400-500 courting adults 13-Feb-1986 335 21-Nov-1986 178 12-Jan-1987 44 150 All nests had chicks 7-Jan-1988 78 78 pairs Jan/May 1989 450 9-Nov-1989 Many dead juveniles; very hot 9-Jan-1990 131 28-Jan-1990 160 adults 20-Jan-1991 100 179 adults 10-Mar-1991 1 100 dead chicks 27-Feb-1992 35 adults 2-Mar-1993 1 12-Jan-1994 55 adults 25-Dec-1995 41 23-Jan-1996 55 29 July 1996 141 696 Main crater: 50 nests w/ eggs or hatchlings, 40 nests w/ downy chicks, 589 fledglings or near-fledglings; upper crater: 6 nests w/ eggs or hatchlings, 1 nest w/ a downy chick, 107 fledglings or near-fledglings; Outside crater (only 5 of these were not on the Plateau): 44 nests Mar-1997 21 22 adults 10-Feb-1998 110 12-Dec-1998 Empty Feb-1999 159 adults 18-Feb-2000 9 31 adults Feb-2002 2 Empty Feb-2003 Empty Feb/Mar-2004 Empty 23-Feb-2006 5 15-Feb-2007 4 Mar-2007 109 adults 22-Feb-2008 7 18-Mar-2009 40 adults

Seymour Island

Date # Nest Juveniles Comments 4/9-March-1975 30 20 pairs Feb/Aug 1975 160 11/14-July-1975 17 28 pairs Oct-1975 10 9 7/21-Nov-1975 13 12 3 pairs 24-Jun-1976 8 9 pairs 24-Jun-1976 9 9 pairs 14-19-Aug-1976 Mostly eggs and small chicks 20-Sep-1979 22 23/24-Jan-1981 Relatively little breeding 4-Jun-1982 Many eggs, few chicks 12/14-Jun-1984 Majority pairs forming May/Jun-1985 826 14/17-Aug-1985 Many juveniles, many dead chicks 18-Sep-1985 Many chicks 4/10-Feb-1986 Abundant chicks and eggs 17-Nov-1986 205 half with eggs, others with chicks Jan/May 1989 989

Floreana Island and Islets

Colony Champion Islet Date #Nest Juveniles Comments 2/5-Oct-1976 Many nesting Feb/Mar-1977 2 Sept/Oct-1977 112 19-Sep-1979 Mostly juveniles 30-Mar-1980 Mostly eggs and courting 14-May-1980 Mostly advanced chicks, birds with two chicks but some with three and four 6/23-Aug-1980 182 122 All the nests had medium and large chicks 20-Nov-1980 Large number of nests 23-Jan-1980 Relatively few breeders 3-Jul-1981 Few small young 14-Aug-1985 Mostly juveniles, low number dead chicks 18-Sep-1985 Little nest initiation since June. Many dead chicks

Eastern Plateau Floreana Jan/June-1982 240 Jul/Dec-1982 172 Jan/Jun-1983 0 Jan/June-1984 334 Jul/Dec-1984 504 Jul-Dec-1985 127 Jan/Jun-1986 350 Jul/Dec-1986 205 Punta Cormorant 1-Nov-1982 134 21-Sep-1984 65 19-Nov-1986 33 Lowest breeding in five years 20-Feb-1987 Empty colony

Gardner Island 21-Jan-1976 Abundant nesting

Española Island

Colony Punta Suárez Date Nest Juveniles Comments 19/20-Dec-1974 Few eggs 24-Feb-1975 All nests abandoned, small chicks drowned after two days of rain 24/25-Aug-1976 4 60 courting 22-Aug-1977 Eggs and small chicks 18-Dec-1977 246 19-May-1978 12 250 courting Nov/Dec-1978 Few nests 11-Dec-1978 112 23 30-Jan-1979 77 58 42 dead chicks 24-Feb-1979 42 2/3 of nesting had chicks 13-Apr-1979 25 courting 12/17-Nov-1979 76 77 60 pairs May/Jun-1981 Many mostly large young 8/23-July-1984 Large number of chicks, all stages Nov/Dec-1984 Large number of chicks, all stages 4/14-March-1985 Large number at all stages, mainly courting 9-Feb-1986 335 100 dead chicks

Colony Punta Cevallos Oct/Nov-1974 Many nesting 22/26-Oct-1976 Large number adults displaying, some with eggs

1000

800

600

400

200

# nests on Daphne Major Daphne # nests on

0 75 80 85 90 95 00 05 09 Year

Breeding history on Daphne Major, based on unpublished data of P. R. Grant, B. R. Grant, and D. J. Anderson

APPENDIX 2

Additional information from GPS tags on blue-footed boobies in the colonies of Playa de

los Perros (Santa Cruz), Daphne Major and Cabo Douglas (Fernandina), deployed

between May 2011 and January 2013

Playa de los Perros (Santa Cruz)

Twenty-five GPS tags were deployed at Playa de los Perros, but three did not move from the nest. Many birds from this colony visited Punta Nuñez (S 0.7449° W

90.2712°) and a location close to Cerro Gallina (S 0.7709° W 90.4050°) on the south coast of Santa Cruz. Most of the trips were during the day, and at night the birds moved to land, probably to rest. Some birds moved during the night to Punta Nuñez, possibly following human disturbance, and some spent the night there. Probably the constant transit of people through the colony (fisherman) disturbed them, making some birds find an alternative site for the night. It is possible that these sites will be chosen in the future as breeding sites. Two other individuals visited the northwest side of Santa Fe (S 0.7992°

W 90.0723°). They moved actively at both terrestrial and marine locations, apparently foraging. One individual spent the night on Santa Fe; for the other, the battery ran out and its location at night is unknown. This area had a large congregation of blue-footed boobies (~500 adults) and Nazca boobies (~200) during the survey in June 2011, and I thought it might have been a breeding site, but no nests have been observed here.

Daphne Major

Six GPSs were deployed in Daphne Major. Most of the birds from this colony moved to the coast of Santa Cruz, Baltra, and Gordon Rocks. They foraged in areas of

53 shallower and productive waters, perhaps in small upwelling zones that are common near these two sites (Witman et al 2003, Witman et al 2010).

Cabo Douglas (Fernandina)

Three GPS were deployed at Cabo Douglas. All three foraged very close to the colony, and during my visits there I observed many birds foraging close to the shore within sight of the breeding colony.

GPS deployedtags de at Playa los Perros (Santa Cru

aphneMajor

deployed at D

GPS tags GPStags

(Fernandina) Douglas Cabo deployed at GPStags

APPENDIX 3

Additional information about breeding and success in visited colonies.

Breeding success (production of fledglings) has been observed three years in row on 28 December 2010, 27 December 2011, and from 27 December 2012 until 10 January

2013 at Playa de lo Perros, with similar results from other colonies that have been monitored only over two years (28 December 2011 until 8 January 2012, and 28

December 2012 until 9 January 2013). This suggests that eggs laid in August and

September are more likely to produce a fledgling than are eggs laid at other times of year.

Many eggs laid in May during two years apparently failed, because no fledglings were found in the colonies in August; however, some large chicks were observed on 14-23

August 2012. Probably many of these large chicks fledged between the August and

December visits, because I found few or no carcasses at the colony in December.

Attendance was lowest during December and January in both years. During my visit to

Playa de los Perros in March 2012 I found only a few individuals resting on rocks close to the shore without apparent intention to breed. I speculate that blue footed boobies prefer to breed during from May to December during the cold season. If blue-footed boobies congregate only during that time, then their breeding may have some seasonality.

Below I provide data on adult attendance, breeding initiation, and breeding success of each colony during the visits in 2011 and 2012.

2 large chicks large 2

; ;

1 large chick large 1

; ;

arge chick arge

1 1

; ;

2 large chicks large 2

; ;

8 large chicks large 8

29 large chicks; large 29

2 2

15 large chicks; large 15

CHAPTER 2.

Implications of movement over the Perry Isthmus, Galápagos for seabird biogeography

ABSTRACT

Land barriers have been mentioned as one of the mechanisms that promote population differentiation in pelagic seabirds, and the literature indeed contains few records of pelagic seabirds flying over land for most species. However, even infrequent crossings of land barriers may permit enough gene flow to influence differentiation, provoking a question: at what scale does a land barrier restrict gene flow effectively?

Genetic data indicate that the Isthmus of Panamá does restrict gene flow in boobies and some other seabirds. I evaluated a smaller isthmus (the Perry Isthmus) that could allow transit across Isabela Island, Galápagos, a potential north-south barrier to movement.

Daytime observations over 3.5 days in June 2012 revealed crossings by > 48 blue-footed boobies (Sula nebouxii) and > 2 frigatebirds (Fregata spp.). If the Isthmus of Panamá

(width = 57 km, height = 26 m above sea level) is assumed to be an effective barrier to gene flow in boobies, but the Perry Isthmus (width = 12.5 km, height 23 m) is not, then these two features bracket the minimum dimension of historical and contemporary landforms that can interrupt gene flow in this group.

INTRODUCTION

Volant seabirds are highly mobile animals able to fly hundreds or thousands of kilometers per day on most days of their lives (Prince et al. 1992). Despite this extreme vagility, the modest interruption of the ocean surface imposed by the Isthmus of Panamá

62 appears to have been an effective barrier to gene flow, and by implication, movement, for some taxa (terns: Avise et al. 2000; boobies: Steeves et al. 2003). The minimum width of the Isthmus of Panamá (57 km) is a trivial distance compared to normal daily travel for these species. The route of least elevational climb to cross the isthmus would require birds to clear Gatun Lake, at an elevation of 26 m above sea level (Johnson & Austin

2008), a minor challenge for a plunge-diving booby that regularly reaches more than 30 m above the surface (Anderson & Ricklefs 1987).

Here I address the general issue of landforms restricting movement of seabirds, exploiting a smaller variant of the Isthmus of Panamá. Isabela Island, Galápagos presents a significant north-south barrier to seabirds unable or unwilling to cross land along its

135 km length. The north and south lobes of the island join at the Perry Isthmus (Fig. 1), a land bridge whose width (12.5 km) and elevation at the lowest crest (23 m) make it a less challenging transit than the Isthmus of Panamá. Significant numbers of blue-footed boobies (Sula nebouxii) and frigatebirds (Fregata minor and F. magnificens) forage on the two sides of the Perry Isthmus (pers. obs.). Movement among some of these foraging sites would be much easier across the Perry Isthmus than around Isabela by water. I tested the hypothesis that the Perry Isthmus presents an effective barrier to movement of pelagic seabird species, by observing movements of free-living birds across the Perry

Isthmus over a 3.5 day period.

METHODS

Seabird movements were observed from Cerro Iguana (N 0.625178°, W

90.975286°), a hill within the valley forming the isthmus, on 12-15 June 2012. From this

63 hill the entire width of the isthmus was clearly visible. Birds passing through the low point of the valley at 23m elevation above sea level were seen easily from Cerro Iguana

(elevation 68 m above sea level), and atmospheric conditions were clear on all days of observation. An 8X binocular and 60X spotting scope were used to identify and count all seabirds observed crossing the isthmus; noting their conservation interest in Galápagos, we also recorded sightings of greater flamingos (Phoenicopterus ruber) and brown pelicans (Pelecanus occidentalis). We used a GPS, compass, and direct observations to determine the heading of each individual visually. Two observers scanned for seabirds continuously and recorded counts and identifications independently. Observations between observers were identical except in one case (Table 1). Frigatebirds (Fregata minor and F. magnificens) were identified to genus only due to the difficulty of species identification of males. The birds were counted when they passed in front of Cerro

Iguana. In all cases, birds that we sighted over the isthmus passed from one coast to the other in a direct path. The altitude of passing birds was estimated visually by comparing the vertical position of the bird to the altitude of the observer (68 m) and the altitude of land under the bird.

RESULTS

We counted 48-50 blue-footed boobies and two frigatebirds crossing the Perry

Isthmus (Table 1). Numbers of birds flying over the isthmus varied by day and the timing of transits did not peak during early morning or late afternoon, contrary to my expectation. Most of the birds were seen crossing during late morning and early afternoon, and many were observed flying over land during the hottest time of the day.

Blue-footed boobies at sea alternate level flapping flight with gliding (Nelson

1978), but over the Perry Isthmus they flapped their wings constantly and appeared to be moving faster than when flying over water. In contrast, frigatebirds never flapped their wings during crossing. All crossing blue-footed boobies passed in groups at low altitude, while frigates were seen alone and flying at high altitude (~80-90 m above the ground).

Two additional frigatebirds were observed flying behind our location >100 m high, moving from north to south, but they were not counted because they did not cross Isabela on the east-west axis.

DISCUSSION

Here I evaluated and compared a smaller isthmus (Perry Isthmus), and the

Isthmus of Panamá, to see which is the minimum dimension that this group of birds can breach. The extent to which pelagic birds fly over land has been questioned by many seabird biologists. My data indicate that some seabirds do cross land barriers. Potential benefits of an overland route include taking a shortcut or flying to inland waters.

Crossing over the 12.5 km isthmus may allow seabirds to avoid an energetically-costly flight around the island (>200 km).

Blue-footed boobies probably see water on the other site of the Perry Isthmus from a minimum altitude of 35-40 m over sea level, and to reach this altitude is not a challenge for them. Frigatebirds probably can see the whole width of the Perry Isthmus in detail, due to their high altitude flight. Neither species seems to be limited by the visual barrier of the Perry Isthmus. If a pelagic seabird wants to cross the Isthmus of

Panamá through the canal, they have to reach more than 26 meters to get to Gatun Lake.

To see water across the isthmus incorporating the locations of lower elevations of the isthmus, the birds have to reach an altitude of ~ 180 m. Boobies do not achieve this height normally when over water, although they do climb to significant heights to reach nesting spots on Galápagos islands like Gardner and Wolf islands (~90 m) and inside the crater on Daphne Major (65-70 m), and up to 300 m to nesting sites on Malpelo, another rocky island (F. Estela, unpub. data) Thus, the limitation on travel over land is apparently not on flying ability, and may be on visual attraction to the water on the other side.

There are several records of pelagic birds found inland, but most are attributed to extreme climate phenomena, with a handful of exceptions. The frequency of records of blue-footed boobies; brown boobies (Sula leucogaster), Laysan albatross (Phoebastria immutabilis) and magnificent frigatebirds (Fregata magnificens) on the Salton Sea, CA,

USA and surrounding areas (123 km from the closest coast), and the lack of association of some observations with any climate phenomena suggest that some birds can flight deliberately to this location (Patten et al. 1997; Dunn & Unitt 1977). In addition some frigatebirds are frequently observed taking a bath in the fresh water lake El Junco on Isla

San Cristóbal, Galápagos at 660 m above sea level and 4.5 km from the nearest coast

(Thornton 1971). Maybe the capability of pelagic birds to fly over land has been underestimated, and more effort is needed to document the extent to which seabirds incorporate overland travel into their routes.

Pelagic birds probably cross land barriers, but maybe the occurrence is low, and maybe the reason is because land represents a strange ecosystem, where they cannot find food or it may be difficult to take off (Friesen et al. 2007), or there may be strong

66 selection due to land-based predators such as hawks and eagles. For example, some

Nazca boobies (S. granti) from Malpelo Island land immediately or move away from land when they see a peregrine falcon (Falco peregrinus) flying (F. Estela, pers. comm.).

Perhaps the land is not the real obstacle, and there are others factors that prevent crossing over. The implications of large physical barriers to gene flow are unclear, and maybe small landforms like isthmuses or peninsulas are not barriers for highly mobile animals.

15 June 2012 in Galápagos was at June 15 Galápagos in 2012

. Civil twilight on 12 on Civil . twilight

TABLES

nd 1823h, respectively 1823h, nd

Difference count of observed birds between the two the between birds observed of observers count Difference

Table 1. Birds observed crossing the Isthmus Perry, Isabela Island, Galápagos in June Galápagos the 2012. Island, observed Perry, Isabela crossing Birds 1. Isthmus Table a 0534h *

FIGURES

Figure 1. Isabela Island and location of the Isthmus Perry. Topographic isoclines indicate 150 m increments in altitude above sea level.

LITERATURE CITED

ANDERSON, D. J. & RICKLEFS, R. E. 1987. Radio-tracking masked and blue-footed boobies (Sula spp.) in the Galápagos Islands. National Geographic Research 3: 152-162.

AVISE, J. C., NELSON, W., BOWEN, B. W. & WALKER, D. 2000. Phylogeography of colonially nesting seabirds, with special reference to global matrilineal patterns in the sooty tern (Sterna fuscata). Molecular Ecology 9: 1783–1792.

DUNN, J. & UNITT, P. 1977. A Laysan albatross in interior southern California. Western Birds 8: 27-28.

FRIESEN, V. L., BURG, T. M. & McCoy, D. 2007. Mechanisms of population differentiation in seabirds. Molecular Ecology 16: 1765-1785.

JOHNSON, J. & AUSTIN, M. A. 2008. A Process Modelling Framework for Formal Validation of Panamá Canal System Operations. Eighteenth Annual International Symposium of The International Council on Systems Engineering, Utrecht, The Netherlands.

NELSON, J. B. 1978. The Sulidae. Oxford University Press, Oxford.

PATTEM, M. A. & MINNICH, R. A. 1997. Procellariiformes occurrence at the Salton Sea and Sonoran Desert. The Southwestern Naturalist 42: 302-311.

PRINCE, P. A., WOOD, A. G., BARTON, T. & CROXALL, J. P. 1992. Satellite tracking of wandering albatrosses (Diomedea exulans) in the South Atlantic. Antarctic Science 4: 31-36.

STEEVES, T .E., ANDERSON, D. J. & FRIESEN, V. L. 2005. The Isthmus of Panamá: a major physical barrier to gene ﬂow in a highly mobile pantropical seabird. Evolutionary Biology 18: 1000-1008.

STEEVES, T. E., ANDERSON, D. J., McNALLY, H., KIM, M. H. & FRIESEN, V. L. 2003. Phylogeography of Sula: the role of physical barriers to gene ﬂow in the diversiﬁcation of tropical seabirds. Journal of Avian Biology 34: 217-223.

THORNTON, I. 1971. A Natural History of the Galápagos. The Natural History Press. New York

CURRICULUM VITAE David J Anchundia

Nationality: Ecuadorian Profession: Biologist E-mail: [email protected]; [email protected] Phone: (336)671-7043 ++(593)993031330

EDUCATION

2013 M.S., Biology, Wake Forest University, Winston‐Salem, NC. 2008 B.S., Biology University of Guayaquil, Ecuador.

WORK EXPERIENCE

 Currently working on the project; Population size of Galápagos blue-footed booby, from May 2011 to present, Wake Forest University.

 Staff Member, Charles Darwin Foundation. Critically endangered Mangrove Finch Project; February 2010 to March 2011.

 Eradication project of introduced species on the islands Rabida, Bainbridge, Beagle and Sombrero Chino in Galápagos, and hawk mitigation. Galápagos National Park, Charles Darwin Foundation, Island Conservation and the University of Minnesota Raptor Center. November 2010 to April 2011

PAST PROJECT COORDINATOR

 Author of the manual guide, toxics plants and potential dangerous animals for quarry workers Holcin Company Guayas-Ecuador July-September 2007.

 Biomass of a lizard (Microlophus occipitalis) in secondary growth forest in Cerro Blanco Protected Forest May-December 2007.

 Organizing member of the Second Bi-national Congress of biology students in Ecuador and Peru January 21-24, 2004.

PROJECT ASSISTANT

 Evolutionary and behavioral ecology team, particular interest in evolution of reproductive life histories of Nazca Boobies (Sula granti), Wake Forest University October-November 2010.

 Feeding ecology of Galápagos Hawk on Santiago Island; University of Missouri, Charles Darwin Foundation and Galápagos National Park, March-September 2010.

 Ontogeny of diving Behavior of Galápagos sea lion; University of Bielefeld Germany, Charles Darwin Foundation and Galápagos National Park, September- November 2008 and March-Nov 2009.

 Status of six colonies of seabirds on La Plata Island, (Sula sula, Sula nebouxii, Sula granti, Fregata magnificens, Phaethon aethereus, Phoebastria irrorata). Equilibrio Azul Foundation, Machalilla National Park, Ecuador July-September 2009.

 Census of birds in Puerto Hondo Mangrove and mountain range Chongon Colonche, Ecuador, September-December 2007.

 Capture of dipterous (Tabanus sp) and coleopterus-beetle (Cicindela sp) for the entomology collection of University of Guayaquil at Sumaco National Park, Amazon Ecuador November 10-14, 2006

 Naturalist guide & Bird watching guide at Cerro Blanco Protected Forest- Ecuador, 2004 to present.

VOLUNTEER

 Cerro Blanco Protected forest, August - December 2007

 Guide at the San Martin Zoo, April 3 - May 2 2006 in Baños Ecuador.

 Identification of species of fungi and frogs in the community Quichua Sinchi- Runa, Amazon of Ecuador, March-April 2005 March-April 2006

SEMINARS, AWARDS, COURSES AND PROGRAMS ATTENDED

 Southeastern Ecology and Evolution Conference at the University of Central Florida March 2013.

 Best graduate poster in Southeastern Ecology and Evolution Conference at the University of Central

 Digital processing of satellite imagery and management ENVI 4.5 software; analysis of geographic information system GIS Arcgis 9.2, August and October 2010.

 InterExchange Work and travel program Destin FL USA. February-June 2008.

 Theory-Practical “IV curso taller Binacional Peruano-Ecuatoriano y III curso Iberoamericano “Introduction to the Paleontology of vertebrates”. August 20-29, 2007, Piura- Peru.

 Top ten best undergrad student 2003 to 2007 University of Guayaquil, Natural Science Department.

 Theory-Practical “Methods for the Conservation of neotropical amphibians focused in Andean ecosystems. July 17- 27, 2007.

 Theory course “conserving wild fauna in captivity” By the municipality of Guayaquil. October, 2007.

 Seminar “basic principles of conservation” By the Scientific Station Pedro Franco Davila (Jauneche). June 3, 2007

 Theory-Practical “Conservation and Mangroves handling” El Guabo-Ecuador. August 20-21, 2005.

 Participation XXVIII Ecuadorian Days of Biology. November 25-27, 2004.

 Theory-Practical “First Aid” in the Red Cross of Guayaquil. May 24 to June 19, 2004.

 Theory-Practical “VIII course of environmental interpretation “Bosque Protector Cerro Blanco" By Pro-Bosque foundation. March 18-28, 2004.

LANGUAGES

Spanish Native language English Proficient French Medium Level