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Jiménez-Uzcátegui: Foraging ecology of Galápagos seabirds 5
Marine Ornithology 47: 5–10 (2019)
USING REFERENTIAL VALUES OF
δ
13C AND
δ
15N TO INFER THE
FORAGING ECOLOGY OF GALÁPAGOS SEABIRDS
GUSTAVO JIMÉNEZ-UZCÁTEGUI1, LEANDRO VACA2, JAVIER COTÍN1, CAROLINA GARCÍA1, ALBA COSTALES1, CHRISTIAN
SEVILLA3 & DIEGO PÁEZ-ROSAS2,3*
1Charles Darwin Research Station, Puerto Ayora, Galápagos, Ecuador
2Universidad San Francisco de Quito and Galápagos Science Center, Islas Galápagos, Ecuador *(dpaez@usfq.edu.ec)
3Dirección del Parque Nacional Galápagos, Islas Galápagos, Ecuador
Received 02 June 2018, accepted 23 August 2018
SUMMARY
JIMÉNEZ-UZCÁTEGUI, G., VACA, L., COTÍN, J. ET AL. 2019. Using referential values of
δ
13C and
δ
15N to infer the foraging ecology of
Galápagos seabirds. Marine Ornithology 47: 5–10.
The Galápagos Penguin Spheniscus mendiculus, Flightless Cormorant Phalacrocorax harrisi, and Waved Albatross Phoebastria irrorata
are endemic to Islas Galápagos. They are known to feed on different prey (including crustaceans, cephalopods, and/or several species of
epipelagic and benthic fish), in accordance with different foraging strategies. In this work, we used stable-isotope analysis of carbon and
nitrogen to corroborate available information on habitat use (
δ
13C) and trophic position (
δ
15N). Feather samples from the three species were
collected in six different areas prior to the 2011 and 2012 breeding seasons. Results showed differences in foraging strategies between
Galápagos Penguins and the other two species (
δ
13C and
δ
15N, P < 0.01). The Flightless Cormorant and Waved Albatross showed similar
proportions of
δ
13C (P = 0.07), but they occupied different trophic levels (
δ
15N, P < 0.01). Isotopic signatures in Galápagos Penguins
reflected differences based on their breeding areas (
δ
13C and
δ
15N, P < 0.01), which were subject to different environmental conditions. This
information could be used to evaluate future ecological conditions among the feeding areas of these species.
Key words: marine birds, Islas Galápagos, isotopic values, foraging strategies, trophic level
INTRODUCTION
The Galápagos Penguin Spheniscus mendiculus (GAPE), Flightless
Cormorant Phalacrocorax harrisi (FLCO), and Waved Albatross
Phoebastria irrorata (WAAL) are endemic marine birds of Ecuador,
breeding in Islas Galápagos (Harris 1973b). More than 90% of
GAPEs and the entire population of FLCOs occur on the western
islands of the archipelago (islas Isabela and Fernandina), while
99.9% of the WAAL breeding population occurs in the eastern
region, on Isla Española (Snow 1966, Harris 1973b). The remaining
GAPEs are found on islas Floreana and Santiago (Wiedenfeld &
Jiménez-Uzcátegui 2008), and a few pairs of WAALs are found
on Isla La Plata, which is located a few kilometers off the coast of
Ecuador (Harris 1973a, Awkerman et al. 2014).
The foraging activities of GAPEs and FLCOs are restricted to the
western bioregion of the archipelago (Edgar et al. 2004); both
species are coastal predators and probably use different foraging
strategies (Snow 1966, Boersma et al. 2013). GAPEs forage up to
23.5km from their nesting area and usually feed at depths of up
to 6 m (Steinfurth et al. 2008) in the upwelling system of Bahía
Elizabeth. The GAPE is considered to be a generalist predator
because its diet includes several species of epipelagic fish and
cephalopods (Vargas et al. 2006, Boersma et al. 2013), among
which the larvae or juveniles of anchovies Engraulis spp. and
sardines Sardinops spp. stand out (Steinfurth unpubl. data). FLCOs
forage up to 5 km from their nests at depths of up to 6 m (Vargas
2006). The FLCO is seen as a benthic predator because it consumes
such prey as crustaceans, octopus, and benthic fish (Snow 1966,
Valle 1994). The WAAL is considered to be a pelagic predator
because it consumes squid and pelagic fish mainly outside the
Galápagos Marine Reserve on the Peruvian and Ecuadorian coasts
(Fernández et al. 2001, Awkerman et al. 2014), but occasionally in
Bahía Elizabeth at Isabela Island (Jiménez-Uzcátegui unpubl. data).
There are currently several techniques used to study the feeding
behavior of marine predators. Among these, stable-isotope analysis
for carbon (
δ
13C) and nitrogen (
δ
15N) provides information on
the food assimilated by a consumer (DeNiro & Epstein 1978,
1981). Knowing the isotopic niche makes it possible to infer
an individual’s habitat type (using
δ
13C) or trophic level and
breadth (using
δ
15N) (Boecklen et al. 2011, Kim et al. 2012).
The isotopic signatures of a predator’s tissues can thus be used as
natural chemical tracers of ecological processes, allowing us to
identify energy flows and to characterize the sources of primary
production that support its food web (Newsome et al. 2007,
Martínez del Río et al. 2008). In marine organisms,
δ
13C values
reflect the type of habitat (coastal/oceanic or pelagic/benthic)
used by their prey (Hobson & Welch 1992). Differences in
δ
13C
are determined by physicochemical and biological factors that
influence the taxonomic composition of phytoplankton and the
concentration of dissolved CO2 in primary consumers (Goericke
& Fry 1994, France 1995). Nitrogen isotopes, on the other hand,
are strongly fractionated from prey to predator, resulting in
δ
15N
enrichment at higher trophic levels (Post 2002).
Inert tissues, such as feathers, retain their isotopic information once
grown and therefore capture mid- and long-term dietary changes
(Cherel et al. 2000, Jaeger et al. 2009). Since feather keratin is
metabolically inert after protein synthesis, the isotopic composition
5
6 Jiménez-Uzcátegui: Foraging ecology of Galápagos seabirds
Marine Ornithology 47: 5–10 (2019)
of feathers reflects diet before moult (Hobson & Clark 1992,
Bearhop et al. 2002). For this reason, isotopic analysis of feathers
has become a powerful method to investigate the foraging ecology
of adult seabirds (Cherel et al. 2002, Quillfeldt et al. 2005). Several
studies on seabird feathers have focused on wing feathers (primaries
and secondaries), but the ethics of sampling wing feathers from live
birds is questionable because of the resulting impairment on flying
(Weimerskirch et al. 1995, Cherel et al. 2008). Since body feathers
are more readily obtained from live animals, they provide an
alternative to the use of wing feathers (Bearhop et al. 2000, Norris
et al. 2007). Body feather moult in GAPEs, FLCOs, and WAALs
occurs weeks before the onset of breeding and at an interval of
about six months (Boersma 1976, Harris 1993b, Valle 1994).
Therefore, the isotopic information from body feather tissue would
be limited to the few months before the breeding season (Becker et
al. 2007, Jaeger et al. 2009).
Despite the increasing use of stable isotopes to monitor the trophic
ecology of seabirds over recent years, only a few researchers have
used this technique on Galápagos marine birds (Lee-Cruz et al.
2012, Awkerman et al. 2014) and none have focused on using
the isotope data to infer or validate the trophic habits of GAPEs
and FLCOs. Our main goal was to test the use of body feathers
from adult seabirds to provide another perspective on the trophic
behavior and feeding strategies of GAPEs, FLCOs, and WAALs in
Islas Galápagos. By better understanding the role of these predators
in the food web, we can establish baseline knowledge that will
contribute to the management and conservation of these species.
METHODS
Study area
The Islas Galápagos are in the eastern Pacific Ocean along the
Equator, approximately 960km west from the continental coast. In
total, six sampling areas were selected. GAPEs were sampled on
Isla Isabela at Caleta Iguana (00°58.6′S, 091°26.7′W) and Puerto
Pajas (00°45.3′S, 091°22.5′W), as well as on Islotes Las Marielas
(00°35.8′S, 091°05.4′W). FLCO populations were sampled on Isla
Fernandina at Playa Escondida (00°15.7′S, 091°28.1′W) and on Isla
Isabela at Punta Albemarle (00°09.2′N, 091°22.0′W). WAALs were
sampled on Isla Española at Punta Suárez (01°22.3′S, 089°44.4′W)
(Fig.1).
Sampling
In 2011 and 2012 we captured 170 adult females (79GAPEs,
61 FLCOs, and 30 WAALs) in August (one month before the
breeding season), as part of an ongoing Marine Birds Project
conducted by the Charles Darwin Foundation and the Galápagos
National Park. We banded every bird and collected biological
samples and clinical data from each. Body feathers were
collected near the tail for GAPEs but near the wings for FLCOs
and WAALs. Feathers were collected using a common non-
destructive sampling protocol (Burger 1993) and were kept in a
paper envelope with all pertinent information (e.g., species, date,
location, and identification number).
Laboratory analysis
Each feather sample was rinsed with deionized water to remove
residues that might interfere with the isotopic signature. The
samples were then desiccated in an oven at 80°C for 24h, and
lipids were extracted following the Microwave Assisted Extraction
protocol (Delazar et al. 2012), using 25 mL of chloroform/methanol
(1:1 v/v). This process was applied to eliminate any bias that may
be introduced by lipids in the tissues, which could negatively skew
the
δ
13C isotopic signature (Post et al. 2007). After lipid extraction,
the samples were air-dried, cut into small pieces, and ground to a
very fine powder using an agate mortar. A subsample of this powder
(~1mg) was sealed in a tin capsule.
Isotope values were measured under continuous-flow conditions in
a mass spectrometer (20–20 PDZ Europe, Sercon Ltd., Cheshire,
UK) at the Stable Isotope Facility at the University of California,
Davis. The results are presented as delta values per mil (‰) using
the following equation:
δ
15N or
δ
13C=((Rsample / Rstandard) − 1) * 1000‰
where Rsample and Rstandard are the values of 15N/14N or 13C/12C,
respectively (DeNiro & Epstein 1978).
Fig.1. Breeding colony locations for Galápagos Penguins (GAPE),
Flightless Cormorants (FLCO), and Waved Albatross (WAAL),
sampled in 2011 and 2012.
Fig. 2. Values of
δ
13C and
δ
15N (expressed in ‰; mean ± SD)
in feather samples from Galápagos Penguin (GAPE), Flightless
Cormorant (FLCO), and Waved Albatross (WAAL). The sample size
for each species is shown in the parentheses beside the species code.
Jiménez-Uzcátegui: Foraging ecology of Galápagos seabirds 7
Marine Ornithology 47: 5–10 (2019)
The standards used were atmospheric nitrogen (N2) for
δ
15N and
Pee Dee Belemnite for
δ
13C. The results were calibrated using
international standards (ammonium sulfate for
δ
15N and sucrose for
δ
13C), which generated a standard deviation between the isotopic
measurement trials of<0.3‰ for
δ
15N and<0.2‰ for
δ
13C.
Data analysis
Statistical tests were performed with Minitab, version 15 (Minitab
Inc.) and Statistica 8.0. Data were tested for normality and
homoscedasticity using the Shapiro–Wilk and Levene tests,
respectively. The statistical significance of differences in
δ
13C and
δ
15N values were determined using parametric or non-parametric
tests and are reported when P<0.05. The graphics were created
using SigmaPlot, version 11 (Systat Software, Inc.). Values are
reported as mean±standard deviation (SD).
RESULTS
Isotopic difference among species
Respectively, the mean estimated
δ
13C and
δ
15N values were
−17.7‰ ± 1.2‰ and 12.7‰ ± 1.2‰ for GAPE feathers;
−14.2‰ ± 1.4‰ and 13.7‰ ± 0.8‰ for FLCO feathers; and
−14.5‰±0.9‰ and 16.6‰±1.3‰ for WAAL feathers (Fig.2).
The C/N ratios of the samples ranged from 2.8 to 3.2 and were
thus within the theoretical range established for the assimilation
of protein from a predator’s diet (McConnaughey & McRoy 1979)
(Table1). The
δ
13C and
δ
15N values were significantly different
among species (Kruskal–Wallis test, P = 0.01 and P < 0.01,
respectively):
δ
13C values for GAPEs differed from those for
FLCOs and WAALs, while
δ
15N values differed among all species
(multiple comparisons of median ranks, P<0.01; Fig.2).
Isotopic difference among breeding areas
The mean
δ
13C and
δ
15N values for GAPEs and FLCOs are shown
by breeding areas and seasons in Table1. The
δ
13C and
δ
15N values
for GAPEs were significantly different between breeding areas
(ANOVA: F=2.76 and P=0.01 for
δ
13C; F=2.90 and P=0.01
for
δ
15N). There were significant differences in
δ
13C values for all
populations, and the
δ
15N values at Caleta Iguana differed from the
other two sites (Tukey multiple comparisons, P<0.01; Fig.3a). In
contrast, there were no significant differences between
δ
13C and
δ
15N values in the FLCO breeding areas (paired t-test, P=0.83 and
0.55, respectively; Fig.3b).
Fig. 3. Values of
δ
13C and
δ
15N (expressed in ‰; mean ± SD) in feathers of A) Galápagos Penguins sampled in three breeding areas: Caleta
Iguana, Puerto Pajas (Isla Isabela), and Islotes Las Marielas; and B) Flightless Cormorants sampled in two breeding areas: Punta Albemarle
(Isla Isabela) and Playa Escondida (Isla Fernandina).
TABLE 1
Isotope values (
δ
13C and
δ
15N) and C/N ratio (mean ± SD in ‰) in feather samples of Galápagos Penguin (GAPE),
Flightless Cormorant (FLCO), and Waved Albatross (WAAL), categorized by breeding area and year
Species Site Year n
δ
13C (‰)
δ
15N (‰) C/N mass ratio
GAPE
Caleta Iguana 2011 18 −18.09 ± 0.65 12.35 ± 0.72 2.87 ± 0.03
2012 12 −18.80 ± 0.91 11.61 ± 0.84 2.83 ± 0.14
Puerto Pajas 2011 10 −17.72 ± 1.11 13.02 ± 0.73 3.20 ± 0.04
2012 11 −18.03 ± 0.36 13.05 ± 0.99 3.20 ± 0.02
Las Marielas 2011 18 −16.90 ± 0.84 13.49 ± 1.06 3.18 ± 0.02
2012 10 −16.39 ± 0.91 13.01 ± 1.29 3.15 ± 0.03
FLCO
Playa Escondida 2011 13 −14.81 ± 1.71 13.33 ± 0.90 3.09 ± 0.06
2012 19 −13.84 ± 0.98 13.94 ± 0.65 3.19 ± 0.04
Punta Albemarle 2011 19 −14.24 ± 1.40 13.82 ± 0.80 3.20 ± 0.02
2012 10 −13.87 ± 1.07 13.81 ± 0.89 3.17 ± 0.02
WAAL Punta Suárez 2012 30 −14.57 ± 0.99 16.69 ± 1.39 3.18 ± 0.02
8 Jiménez-Uzcátegui: Foraging ecology of Galápagos seabirds
Marine Ornithology 47: 5–10 (2019)
Between 2011 and 2012, the GAPE populations did not show
significant differences in
δ
13C and
δ
15N (Mann–Whitney U-test: Las
Marielas, P=0.15 and 0.27, respectively; Puerto Pajas, P=0.67 and
0.52, respectively; Caleta Iguana, P=0.07 and 0.08, respectively).
These differences between years were not apparent in FLCO
populations (paired t-test: Punta Albemarle: P = 0.50 and 0.97,
respectively; Playa Escondida, P=0.24 and 0.61, respectively).
DISCUSSION
Given that stable-isotope analysis is influenced by organic matter
sources (
δ
13C) and by prey type and trophic level (
δ
15N), our
results indicate that there is trophic segregation among GAPE
and FLCO populations. Displacement patterns were identified
in both species with the help of satellite tags (Vargas 2006,
Steinfurth et al. 2008), and the variation in
δ
13C and
δ
15N values
between species supports the hypothesis that GAPEs and FLCOs
feed in different ocean areas around the Galápagos. This, in turn,
influences trophic level.
Some of the advantages of using feathers for trophic research
include the ability to gather long-term information (i.e., over a span
of months) and the possibility of monitoring feeding behavior in
pre-breeding stages (Cherel et al. 2000, Jaeger et al. 2009). Thus,
the appropriate use of GAPE, FLCO, and WAAL body feathers
is crucial, because these species retain these feathers for at least
five months, then moult weeks before the breeding season (Harris
1973a, Boersma 1976, Valle 1994). Inaccuracies in isotopic niche
estimates may be debated; however, we detected feeding-strategy
patterns for all species that were consistent with those previously
reported by groups using regurgitations from adult females to
determine diet in different areas of the archipelago (Snow 1966,
Fernández et al. 2001, Boersma et al. 2013).
The
δ
13C values for FLCOs were more positive than those for
GAPEs, indicating the use of separate environments. Due to
differences in carbon sources (benthic–macroalgae vs. pelagic–
phytoplankton), food webs in inshore and benthic ecosystems
show a stronger enrichment of
δ
13C than those in pelagic
ecosystems (Goericke & Fry 1994, France 1995). Therefore, the
δ
13C signature we observed in GAPEs indicates a consistently
pelagic foraging strategy. In contrast, FLCOs have a more inshore
foraging strategy, which limits their diet to prey associated with
rocky bottoms (Snow 1966, Valle 1994). However, Steinfurth et
al. (2008) mention that, in many instances, GAPEs feed near and
parallel to the coast; this pattern does not coincide with the few
available diet studies, which suggest that cephalopods and larval
or juvenile anchovies and sardines are their main prey (Boersma
et al. 2013, Steinfurth unpubl. data). The
δ
15N values for FLCOs
were higher than those for GAPEs over the entire study period.
This is consistent with the preferred foraging zones among
cormorants and penguins in Islas Galápagos (Valle 1994, Vargas
2006). The diet of GAPEs, which feed mostly in oceanic waters,
is mainly composed of prey from the lower trophic levels (filter
fish and squids; Boersma et al. 2013, Steinfurth unpubl. data), as
opposed to that of FLCOs, which feed mainly near of the coast
and consume prey from the higher trophic levels (benthic fish and
octopus; Valle 1994).
Although WAALs are not a diving bird, they exhibited 13C-enriched
values, as did the FLCOs. This result suggests that WAALs would
be foraging in highly productive areas, such as the coast of Peru,
where elevated primary productivity is associated with upwelling
in the Humboldt Current System (Banks 2002); this corroborates
the pelagic-predator strategy reported for this species (Fernández
et al. 2001, Awkerman et al. 2014). WAALs are primarily
teuthophagous, but they also feed on epipelagic fish (Harris
1973a). This is reflected in their nocturnal feeding behavior, in
which they take mesopelagic prey, that surface at night (e.g., squid;
Harris 1973a). The high
δ
15N values in WAALs relative to other
species could indicate that they are feeding on prey of a higher
trophic level or that they are consuming similar prey (i.e., filter
fish and squid) in areas of greater nitrification, such as the coasts
of Peru and Ecuador (Farrell et al. 1995). The
δ
15N fractionation
depends on temporal variation in the number of nitrate sources
and on the nitrate consumption rate in the upper ocean (Maslin &
Swann 2006). Higher
δ
15N values in coastal–benthic species may
be influenced by a combination of factors, including the presence
of marine plants that use ammonium and nitrate enriched in 15N
(Macko & Estep 1984) or a higher food web complexity that may
include several trophic levels (DeNiro & Epstein 1981). This
scenario could apply to the isotopic differences in
δ
15N that we
observed between GAPEs and WAALs, although the two species
consume a large variety of small pelagic fish that are in a similar
trophic position (Harris 1973a, Boersma et al. 2013).
The isotopic differences found in GAPEs between breeding areas
showed that individuals from Caleta Iguana feed further away from
the coast than individuals from Las Marielas. Satellite telemetry
data from GAPEs at Las Marielas show a coastal behavior (i.e.,
with few feeding trips and few deep dives in front of the islets)
towards the Canal Elizabeth at Isla Isabela (Steinfurth et al. 2008).
Because the population of Caleta Iguana is farther away from the
area of greater productivity (Bahía Elizabeth, where there is greater
availability of prey; Ruíz & Wolff 2011), it would be forced to
travel long distances to find food (Vargas et al. 2006, Steinfurth et
al. 2008). This may be one of the reasons why there is a constant
population of GAPEs in Las Marielas (Jiménez-Uzcátegui pers.
obs.). Spatial differences not observed in the FLCO populations
can be explained in two ways: (a) the FLCOs of distinct breeding
areas consume the same variety of prey species but in different
proportions, resulting in similar
δ
15N average values (Newsome et
al. 2007); or (b) the FLCOs of these sites feed on different prey, but
of a similar trophic level (Post 2002). This low degree of trophic
overlap was suggested by Valle (1994), who mentioned similarities
in both prey and potential feeding zones throughout their entire
distribution area. In this study, no temporal differences were
observed in GAPE or FLCO feeding strategies. This corroborates
other studies that mention that, during normal years, there are no
great variations in the primary productivity of the ecosystems where
these populations live (Banks 2002, Nims et al. 2008, Schaeffer et
al. 2008).
Our results show that the GAPEs, FLCOs, and WAALs follow
different trophic strategies and use different foraging habitats: the
δ
13C and
δ
15N values placed them in foraging zones and trophic
positions that coincide with previously published feeding strategies
and known prey types. Further research is required on these three
species to analyze their trophic variability and to establish their
roles in the different ecosystems. Our results also indicate that
stable-isotope analysis is a valuable tool to monitor the ecological
conditions of the feeding areas occupied by these endangered
species and to detect temporal/spatial changes associated with
climate variability or human impacts.
Jiménez-Uzcátegui: Foraging ecology of Galápagos seabirds 9
Marine Ornithology 47: 5–10 (2019)
ACKNOWLEDGEMENTS
We thank the Galápagos National Park and the Charles Darwin
Foundation for logistical support and for granting us permission to
collect the samples used in this study. We also thank the Universidad
San Francisco de Quito for financing the isotopic analyses and for
logistical support during the preparation of this manuscript. We
would like to thank our donors—the Galápagos Conservation Trust,
the Truell Charitable Foundation, the Penguin Fund of Japan, and
Mr. Seishi Sakamoto—for financial support during the planning and
preparation of this work. We are grateful to our collaborators; to the
75+ assistants and volunteers who helped with the research between
2009 and 2017; and to Franklin Gil, Manuel Masaquisa, Freddy
Villalva, Wilman Valle, Patricio Carrera, Ainoa Nieto, and Pelayo
Salinas de Leon. We thank Sarah Brooks for the English revision
and the Galápagos Science Center for providing the information-
processing and analysis facilities. Finally, we thank two anonymous
reviewers who helped immensely with improving our paper. This
publication is contribution number 2220 of the Charles Darwin
Foundation for the Galapagos Islands.
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