i

POPULATION SIZE OF BLUE-FOOTED BOOBIES IN GALÁPAGOS:

EVALUATION OF INDICATIONS OF POPULATION DECLINE

BY

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.

ii

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

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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Grant from Princeton University, who provided unpublished breeding and attendance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Fisheries Service (La Jolla) for sharing unpublished at-sea distribution data.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

v

Introduction ....................................................................................................................62

Methods ..........................................................................................................................63

Results ............................................................................................................................64

Discussion ......................................................................................................................65

Tables ..............................................................................................................................68

Figures............................................................................................................................69

Literature Cited ..............................................................................................................70

Curriculum Vitae ...............................................................................................................71

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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

vii

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

viii

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

x

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.

1

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.

2

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

3

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).

4

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

5

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

6

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

7

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

E[Ň] = n12/(n1-n2), Eq. 1

and the variance of E[Ň] as

V[Ň] = n12 n2

2(n1+ n2)/(n1- n2)

4 Eq. 2

Finally, the probability of detection is estimated as

8

[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

9

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

10

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%

11

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

12

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).

13

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).

14

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.),

15

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

16

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

17

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

18

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

19

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

20

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).

21

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

22

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.

23

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

24

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

25

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).

26

TABLES

Colony site

May

2011

Jun

2011

Aug

2011

Dec

2011/

Jan

2012

May

2012

Jun

2012

Aug

2012

Dec

2012/

Jan

2013

FOCAL COLONIES

Playa de los Perros

-Santa Cruz

MN C MN MN MN C MN MN

Daphne Major

MN C MN MN MN C MN MN

Cabo Douglas

- Fernandina

MN C MN MN MN C MN MN

Pta. Vicente Roca

-Isabela

MN C MN MN MN C MN MN

Seymour Norte C MN MN MN C MN MN

NON-FOCAL COLONIES

Punta Cormorant,

Cuevas

-Floreana

MD,C

MD

MD,C

Punta Pitt

-San Cristóbal

MD,C

MN

MD,C

MN

Punta Suárez

- Española

MN

MD,C

MN

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.

27

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).

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

28

Colony site

Historical

maximum

# nests

Maximum #

nests in 2011

Maximum #

nests in 2012

Daphne Major 836 4 (<1%) 4 (<1%)

Seymour Norte 965 16 (2%) 62 (6%)

Playa de los Perros

Santa Cruz

No data 73 62

Cabo Douglas

Fernandina

1467 1 (<1%) 1 (<1%)

Punta Vicente Roca

Isabela

1800 67 (4%) 0

P. Cormorant & Cuevas

Floreana

134 3 (2%) 6 (4%)

Punta Pitt

San Cristóbal

No data 2 3

Punta Suárez

Española

256 29 (11%) 11 (4%)

La millonaria

Baltra

New

colony

No data 49

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

maxima.

29

30

Tab

le 4

. R

epre

senta

tion o

f pre

y i

tem

s b

y w

eight

in r

egurg

itat

ion s

ample

s.

Num

ber

s in

the

char

t re

pre

sent

per

centa

ge

of

gra

ms

and s

um

to 1

00

ver

tica

lly. T

he

most

im

port

ant

pre

y s

pec

ies

for

each

by y

ear

are

iden

tifi

ed w

ith a

box

. U

nder

line

repre

sents

sam

pli

ng s

essi

ons with few

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

Tota

l

grams”

is

the

tota

l gra

ms

of

fish

coll

ecte

d d

uri

ng t

hat

yea

r at

that

sit

e.

31

Tab

le 5

. L

og l

ikel

ihood, A

IC,

and d

eriv

ativ

e val

ues

for

model

s ex

pla

inin

g v

aria

tion i

n b

reed

ing P

OT

EN

TIA

L (

see

Met

hods)

.

32

Table 6. β values and their standard errors for predictors in the model set of Table 4. “Effect β” and “Effect SE” refer to the

first predictor in the model (i.e., for VISIT in the top model). Underlined β values are those whose 95% confidence interval

incl

udes

zer

o.

33

FIGURES

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

during coastal survey of June 2012.

34

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

35

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

36

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.

37

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

38

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).

39

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43

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.

44

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

14-Jul-1977 60

1/4 of the nest had chicks, 577 adults in the

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

17-Jan-1985

Insignificant chick mortality compared to

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

45

Colony Marielas islets

21-Jul-81 50 pairs

Colony Punta Moreno

Aug/Sep-1976 15

Colony Tortuga island

26-Jul-75 47

46

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

47

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

4-Aug-1974

Several

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

48

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

49

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

50

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

51

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

52

Year

# n

ests

on D

aphne

Ma

jor

0

200

400

600

800

1000

75 80 85 90 95 00 05 09

Breeding history on Daphne Major, based on unpublished data of P. R. Grant, B. R.

Grant, and D. J. Anderson

53

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

54

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.

55

GP

S t

ags

dep

loyed

at

Pla

ya

de

los

Per

ros

(San

ta C

ruz)

56

57

GP

S t

ags

dep

loyed

at

Dap

hne

Maj

or

58

GP

S t

ags

dep

loyed

at

Cab

o D

ougla

s (F

ernan

din

a)

59

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.

60

1 2

lar

ge

chic

ks;

2 1

lar

ge

chic

k;

3 1

lar

ge

chic

k;

4 2

lar

ge

chic

ks

61

1 1

5 l

arge

chic

ks;

2 2

9 l

arge

chic

ks;

3 8

lar

ge

chic

ks;

42 l

arge

chic

ks

62

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

63

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

64

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.

65

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.

66

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

67

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.

68

TA

BL

ES

Tab

le 1

. B

irds

obse

rved

cro

ssin

g t

he

Isth

mus

Per

ry,

Isab

ela

Isla

nd, G

aláp

agos

in J

une

2012.

*D

iffe

rence

count

of

obse

rved

bir

ds

bet

wee

n t

he

two o

bse

rver

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FIGURES

Figure 1. Isabela Island and location of the Isthmus Perry. Topographic isoclines

indicate 150 m increments in altitude above sea level.

70

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

71

CURRICULUM VITAE

David J Anchundia

Nationality: Ecuadorian

Profession: Biologist

E-mail: anchdj11@wfu.edu; davidanchundia@gmail.com

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.

72

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.

73

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