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Biological effects of El Niño on Galapagos penguin


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Long-term monitoring of physical and biological parameters is essential for understanding the effects of El Niño on bird populations, particularly for small or declining populations. We examined the biological effects of El Niño activity from 1965 to 2004 using instrumental sea-surface temperatures from the Galápagos Islands and 20 years of census counts of the Galápagos penguin. Between 1965 and 2004, nine El Niño events were recorded of which two were strong and seven were weak. The two strong El Niño events of 1982–1983 and 1997–1998 were followed by crashes of 77% and 65% of the penguin population, respectively. The evidence suggests that the increased frequency of weak El Niño events limits population recovery. The 2004 penguin population is estimated to be at less than 50% of that prior to the strong 1982–1983 El Niño event. We discuss the biological effects of increased El Niño intensity and frequency within the context of a 6000-year record of El Niño influence and in the light of increasing anthropogenic threats operating after 1535, when the Archipelago was discovered by Europeans.
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Biological effects of El Nin
˜o on the Gala
´pagos penguin
F. Herna
´n Vargas
, Scott Harrison
, Solanda Rea
, David W. Macdonald
Wildlife Conservation Research Unit, University of Oxford, Department of Zoology, South Parks Road, Oxford OX1 3PS, UK
Charles Darwin Research Station, Isla Santa Cruz, Gala
´pagos, Ecuador
Article history:
Received 24 May 2005
Available online 13 September 2005
El Nin
Long-term monitoring of physical and biological parameters is essential for understanding
the effects of El Nin
˜o on bird populations, particularly for small or declining populations.
We examined the biological effects of El Nin
˜o activity from 1965 to 2004 using instrumental
sea-surface temperatures from the Gala
´pagos Islands and 20 years of census counts of the
´pagos penguin. Between 1965 and 2004, nine El Nin
˜o events were recorded of which
two were strong and seven were weak. The two strong El Nin
˜o events of 1982–1983 and
1997–1998 were followed by crashes of 77% and 65% of the penguin population, respec-
tively. The evidence suggests that the increased frequency of weak El Nin
˜o events limits
population recovery. The 2004 penguin population is estimated to be at less than 50% of
that prior to the strong 1982–1983 El Nin
˜o event. We discuss the biological effects of
increased El Nin
˜o intensity and frequency within the context of a 6000-year record of El
˜o influence and in the light of increasing anthropogenic threats operating after 1535,
when the Archipelago was discovered by Europeans.
Ó2005 Elsevier Ltd. All rights reserved.
1. Introduction
The Gala
´pagos penguin (Spheniscus mendiculus) is an endan-
gered species by virtue of its restricted range and fluctuating
population size (BirdLife International, 2000). Approximately,
95% of the population of Gala
´pagos penguins is distributed
primarily along the westernmost islands of Fernandina
(0°220000 S, 91°3102000W) and Isabela (0°2503000S, 91°70W); this dis-
tribution coincides with the major upwelling zones and the
most productive waters of the archipelago (Boersma, 1977,
1978). The remaining 5% of the population lives in small pop-
ulations inhabiting the islands of Floreana (1°170000 S,
90°260000 W), Santiago (0°1503000S, 90°43 03000 W), and Bartolome
(0°1605100 S, 90°3204800W). Birds nest opportunistically through-
out the year if conditions permit although peaks in egg laying
occur in April–May (Vargas, unpubl. data) and in August–Sep-
tember (Boersma, 1977). Based on capture-mark-resight
methods (Vargas et al., 2005), the population size of the Gala
pagos penguin in 2004 was estimated at 1500 individuals (Var-
gas and Wiedenfeld, 2004).
Phylogenetic evidence suggests that the Spheniscus penguin
genus diverged from other penguin species between 100,000
and 800,000 years ago (Akst et al., 2002; Grant et al., 1994), and
subsequent association of S. mendiculus with the Gala
means that historic El Nin
˜o episodes are likely to have shaped
specific breeding and survival strategies in this species for
thousands of years. Lake sediment deposits provide evidence
that El Nin
˜o activity has influenced the climate of the Gala
gos Islands for at least the last 6000 years (Riedinger et al.,
2002) with it likely affecting the Gala
´pagos penguin (Boersma,
1998a; Valle and Coulter, 1987; Vargas, 1999), as it does other
seabirds, through a cascade of events (Chavez et al., 1999) that
lead to changes in the food web and predator–prey relation-
ships (Boersma, 1977). Of all the penguin species, only the Gala
pagos penguin lives on the equator and is able to do so because
of the cold oceanic upwelling along the equator and the
0006-3207/$ - see front matter Ó2005 Elsevier Ltd. All rights reserved.
*Corresponding author: Fax: +44 0 1865 393100.
E-mail addresses: (F.H. Vargas), (D.W. Macdonald).
available at
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Equatorial Under Current, also known as the Cromwell current
(Boersma, 1977, 1978). As the Equatorial Under Current hits the
western edge of the Gala
´pagos Archipelago, cold, nutrient-rich
water is forced to the surface (Houvenaghel, 1984) and provides
the shallow-diving Gala
´pagos penguin (Mills, 2000) with access
to its primary prey species.
El Nin
˜o events affect the biodiversity of the Gala
´pagos Is-
lands through dramatic changes to the environmental condi-
tions of the Islands. During El Nin
˜o, the Equatorial Under
Current weakens, the surface water warms, macronutrients
are reduced, primary production decreases (Chavez et al.,
1999), and fish numbers diminish; data from commercial fish-
eries indicated that the catch of mullets from the Gala
during the 1997–1998 El Nin
˜o event was half that of the com-
mercial catch in 1999 when there was no El Nin
˜o event
(Nicolaides and Murillo, 2001). Similarly, the catch of sardines
along the coast of mainland Ecuador during the 1998 El Nin
year was the lowest of the last two decades (Ja
´come and Osp-
ina, 1999).
Recently, the frequency and severity of El Nin
˜o events ap-
pear to have increased and this is a concern for the conserva-
tion of endangered seabird species. El Nin
˜o events now occur
2–7 times more frequently than they did 7000–15,000 years
ago (Riedinger et al., 2002; Rodbell et al., 1999). Climate mod-
els suggest that most of the warming observed during the last
50 years is attributable to human activities (Karl and Tren-
berth, 2003) with an increased El Nin
˜o pulse in the last three
decades (Trenberth and Hoar, 1996, 1997). The 1982–1983 and
1997–1998 El Nin
˜o events were the strongest recorded in the
last century (Chavez et al., 1999) and had severe biological ef-
fects (Barber and Chavez, 1983; Hays, 1986; Valle et al., 1987).
Sea-surface temperatures and precipitation data collected
from the Gala
´pagos between 1965 and 1999 indicate that
1983 and 1998 were the hottest and wettest years on the Gala
pagos Islands (Snell and Rea, 1999).
Here, we evaluate the effect of ENSO (El Nin
˜o Southern
Oscillation) on the population dynamics of the penguin and
determine the likely effects of climate change on the conser-
vation of Gala
´pagos penguins. Standard demographic param-
eters are inordinately difficult to obtain for this species
because the penguins are in small groups widely scattered
along the difficult terrain of the archipelago. However, we
present analysis from two long-running data sets: (1) the
number of adult and juvenile penguins recorded since 1970
and (2) the daily sea temperatures logged in the Gala
since 1965.
2. Materials and methods
We examined the biological effects of El Nin
˜o using census
data of the Gala
´pagos penguin and instrumental sea-surface
temperature data from the Gala
´pagos Islands.
2.1. Penguin data
We conducted complete census counts each year as part of a
joint effort of the Charles Darwin Research Station (CDRS)
and the Gala
´pagos National Park Service (GNPS). Censuses
attempted to count all penguins using methods described
elsewhere (Boersma, 1974, 1977; Mills and Vargas, 1997). Sam-
pling bias was minimized by standardizing dates, duration of
the census, time of day, number of observers, field equip-
ment, survey zones, travel speed, and types of data collected.
The 10-day census occurred in late August and early Septem-
ber across the range of the Gala
´pagos penguin. We counted
penguins between 06:00 and 18:00 using a small dinghy to ap-
proach the coast as closely as possible. The birds were classi-
fied as adults, juveniles, and penguins of unknown age
(whose age could not be determined when birds were swim-
ming). Fledged juvenile birds, with juvenile plumage as aged
by Boersma (1977), were used as an index of reproduction
per year. For our statistical analysis, we assumed no migra-
tion and equal detectability of birds across all years (including
years of El Nin
˜o events). All known nesting areas were
checked to determine the extent of nesting activity. Here,
we present data on the combined total number of adult and
juvenile penguins.
2.2. Sea surface temperature
Sea surface temperature is a good indicator of El Nin
˜o events
(Trenberth and Stepaniak, 2001), so we used SST data col-
lected between 1965 and 2004 at the meteorological station lo-
cated at the CDRS (00°440200S, 90°1802400 W) on Santa Cruz
Island. Sea surface temperature were recorded at 06:00,
12:00, and 18:00 with a hand held thermometer in a bucket
of water pulled from the sea surface (Snell and Rea, 1999).
We calculated normalized SST anomalies for the period
1970–2004 relative to the base period of 1965–1979 from the
same data set. The base period was selected as it was consid-
ered representative and not biased by the warming and El
˜o events after 1979 (Trenberth, 1997; Trenberth and Hoar,
We determined El Nin
˜o events by identifying periods dur-
ing which the five-month running mean of SST anomalies
was above 0.5 °C for at least six consecutive months. This
definition follows the protocols of the Japan Meteorological
Agency (J.M.A.) and Trenberth (1997) with adjustment for
instrumental sea-surface temperature from the Gala
Islands. These calculations also enabled us to determine
the duration, frequency, and intensity of warm El Nin
˜o and
cold La Nin
˜a events. La Nin
˜a events were determined by
identifying periods during which the 5-month running
means of SST was below 0.5 °C for at least six consecutive
The El Nin
˜o events were classified as strong or weak
depending on the magnitude of the positive anomalies. We
considered anomalies between 0.5 and 2 °C as weak El Nin
and anomalies >2 °C as strong El Nin
˜o events. Despite some
differences in measurements of magnitude (intensity), our
frequency of ENSO (El Nin
˜o Southern Oscillation) events from
the Gala
´pagos is in most cases in agreement with the consen-
sus (ENSO) lists ( and
the Multivariate ENSO index (
ENSO/enso.mei_index.html). The main difference is that the
1972–1973 event, classified as a strong El Nin
˜o by the consen-
sus list, appears only as a weak El Nin
˜o event in the Gala
108 BIOLOGICAL CONSERVATION 127 (2006) 107114
3. Results
Analysis of SST indicates two strong (1982–1983 and 1997–
1998) and seven weak (1965–1966, 1968–1969, 1972–1973,
1976, 1986–1987, 1991–1992 and 1993) El Nin
˜o episodes in the
´pagos during the study period (Fig. 1). The two strong El
˜o events, in addition to showing anomalies greater than
2°C, also lasted for 17 and 18 months, respectively. The aver-
age duration of the weak episodes was 11.4 months (±3.4 SD,
range 6–16). The 1982–1983 and 1997–1998 strong El Nin
events were associated with reductions in the penguin popu-
lation of 77% and 65%, respectively, and the frequent, weak El
˜o events coincided with years when recovery in the pen-
guin population faltered (Fig. 1). The change in penguin num-
bers was significantly and strongly correlated with mean
normalised SST anomalies (Fig. 2). This model (F
1, 15
= 71.1,
p< 0.001, b
= 0.81) predicts that strong El Nin
˜o events,
characterized by a rise in SST anomalies >2 °C above baseline
temperature, result in population crashes greater than 50%
(Fig. 2). In contrast, La Nin
˜a events, defined as a drop in SST
anomalies to 0.5 °C or lower below baseline temperatures,
are associated with periods of recovery in the population of
´pagos penguins (Fig. 2).
Fig. 1 illustrates that in the years of strong El Nin
˜o, the cen-
sus revealed fewer adults and juveniles than in other years
suggesting an association between El Nin
˜o, reduced fledgling
success (measured as the number of juveniles) and adult sur-
vival. Counts during weak El Nin
˜o events showed a low recov-
ery rate of the population indicating poor reproduction and
recruitment. The censuses also indicated an uncharacteristi-
cally low recovery rate of the penguin population between
1983 and 1997 coincident with a high frequency of weak Nin
events between the two strong events (Fig. 1).
During the 2004 census, we counted 858 penguins.
Although this represents nearly a doubling of the numbers
(444) after the last strong 1997–1998 El Nin
˜o event, the 2004
penguin numbers are less than half of numbers in the 1970s.
4. Discussion
4.1. Increased frequency and intensity of El Nin˜o
The CDRS SST data show that between 1965 and 1981 there
were no strong El Nin
˜o events in the Gala
´pagos that were
comparable to those of the 1980s and 1990s. We assert that
during these earlier years, the oceanographic conditions pro-
duced resources sufficient to support the high numbers of
penguins that we recorded in the first three counts of the
1970s and early 1980s (Fig. 1). In fact, recent investigations
suggest that a decrease of 25% in oceanic upwelling around
the equator after 1970 may have led to an increase of 0.8 °C
in SST (McPhaden and Zhang, 2002), probably reducing food
resources in Gala
´pagos. After 1980, the large fluctuations
and the slow recovery of the penguin population were proba-
bly linked to the increasing intensity and frequency of both
strong and weak El Nin
˜o events and the associated unproduc-
tive oceans.
Historically (before 1980), we presume that the penguin
population would recover in years following an El Nin
˜o, or
during cold La Nin
˜a events, with the associated abundance
of food. Our census data indicate that population recovery
during La Nin
˜a events have been only moderate (Fig. 2) and
have failed to restore the numbers typical of the period prior
to the 1980s (Fig. 1).
The modern pattern of more frequent and intense El Nin
episodes, including some events that are extreme by histori-
Fig. 1 – Sea-surface temperature (SST) anomalies from the Charles Darwin Research Station, Isla Santa Cruz, Gala
Ecuador. We calculated the normalized temperature anomalies (red and blue areas) by comparing the 5-month running mean
for SST of each month to the baseline SST from 1965 to 1979. SST anomalies that remain above 0.5 °C or below 0.5 °C
(beyond grey striped area) for at least six consecutive months define El Nin
˜o(n= 9) or La Nin
˜a(n= 9), respectively. The positive
temperature anomalies that exceeded 2 °C (dashed line) indicate strong El Nin
˜o events. Black bars are total number of
penguins. (For interpretation of the references to color in this figure legend, is referred to the web version of this paper.)
BIOLOGICAL CONSERVATION 127 (2006) 107114 109
cal standards (1982–1983, 1997–1998), has cumulative effects
that diminishes the capacity of the penguin populations to re-
cover from previous El Nin
˜o events before the next event oc-
curs. This cycle leads to long-term reductions in penguin
4.2. Strong El Nin˜ o events and population crashes
Our analysis indicates that strong El Nin
˜o events are cata-
strophic for the Gala
´pagos penguin causing declines greater
than 50% in the population of adult and juvenile birds (Fig. 2).
Starvation is the likely cause of this elevated mortality. Sim-
ilar mortality in seabirds, due to starvation, has been docu-
mented in productive ecosystems, such as those of the
Bengala Current during severe El Nin
˜o events. (La Cock, 1986).
The severity of strong El Nin
˜o, measured as duration and extent
of SST anomalies, explains this drastic effect on the Gala
penguin. Only 29 juveniles werecounted in the two censuses of
1984 following the 1982–1983 El Nin
˜o event (Valle and Coulter,
1987). In September 1997, the effects of El Nin
˜o (initiated in
March 1997) on the penguin population were still imperceptible
(Fig. 1), and we counted 1284 penguins in the Archipelago of
which 17% were juveniles. The 1997–1998 El Nin
˜o ended in July
1998. By the time of the census of September 1998, no nests or
juveniles were recorded, and only 444 adults were observed.
These two strong warm events occurred when they would have
had the maximum impact on breeding success during two con-
secutive breeding seasons (1982–1983 and 1997–1998).
Although penguins can breed year round, the onset of a
strong El Nin
˜o events coinciding with the critical period of
pre-breeding food acquisition could have detrimental effects
on the population. Since one known preferred breeding time
is from April–May, it could have been that the two strong El
˜o events that started in May 1982 and March 1997 were
particularly detrimental to penguins because of the lack of
available food.
The high annual adult survival in penguins in general
(Crawford et al., 1999; Weimerskirch et al., 1992) would tend
to make their population trends extremely sensitive to small
changes in annual survival (Ratcliffe et al., 2002). Conse-
quently, the estimated low adult survival values of 0.23–0.35
for the Gala
´pagos penguin during strong El Nin
˜o events, in
addition to the direct impact on the dynamics of the breeding
population, could also reduce the penguin life expectancy
(Croxall et al., 2002) and affect the overall population trend
in the manner described in this paper. Therefore, we consider
adult mortality to be the main effect of El Nin
˜o on the Gala
gos penguin.
4.3. Weak El Nin˜ o events and slow recovery rate of
penguin population
Weak El Nin
˜o events appear to affect only reproduction and
not adult survival because no population crashes were re-
corded during weak El Nin
˜o events. During the weak 1972–
1973 El Nin
˜o, Boersma (1998b) recorded only one surviving
chick from 92 nests. This suggests that penguins do lay eggs
during weak El Nin
˜o events, but we deduce that the food sup-
ply could be insufficient to achieve the survival and recruit-
ment of fledglings. The cumulative effects of weak El Nin
events on reproduction provide a plausible explanation for
the low recovery rate of the penguin population between
1983 and 1997 (Fig. 1). In fact, some authors have identified
the period between 1990 and 1995 as the longest El Nin
record (Trenberth and Hoar, 1996). Poor recruitment rates
associated to post-fledgling mortality during repetitive weak
Fig. 2 – Percent change in penguin numbers in relation to the mean normalized sea-surface temperature (SST) anomalies for
the period December–April that preceded each penguin count. We calculated changes in the penguin population for counts
that were not more than 3 years apart (n= 17) (F
1, 15
= 71.1, p< 0.001, b
= 0.81). We also tested the relationship without the 2
strong El Nin
˜o events in 1983 and 1998 to determine that the relationship remained significant without these extreme values
1, 13
= 10.2, p= 0.007, b
= 0.40). Dotted lines are 95% confidence limits. (For interpretation of the references to color in this
figure legend, is referred to the web version of this paper.)
110 BIOLOGICAL CONSERVATION 127 (2006) 107114
El Nin
˜os are also expected to have a lag effect on population
4.4. The mechanisms of El Nin˜ o events
Sinclair and Krebs (2002) state that food supply is the primary
factor determining the growth of animal populations. Fur-
thermore, there is accumulating evidence that changes in
the availability of food limits the production and survival of
the young, and that these changes are often driven by the
weather (White, 2004). At present, little is known about the
diet of the Gala
´pagos penguin. There are only opportunistic
observations of penguins foraging close to the shore that indi-
cate that prey species such as sardines (Sardinops sagax), piqu-
itingas (Lile stolifera), and mullets (Mugil sp.) are likely of
primary importance to the penguin diet (Mills, 2000; Vargas,
unpubl. data). If these schooling fish species migrate away
from the Gala
´pagos archipelago during El Nin
˜o events, the
penguin will not have access to prey. The Gala
´pagos penguin
will be constrained to the coastal areas by its inability to tra-
vel long distances (see Crawford and Shelton, 1978). In fact,
research on foraging behaviour suggests that feeding is exclu-
sively taking place in upwelling waters less than 2 km from
the coast where penguins perform dives of not more than
50 m (Mills, 2000; Steinfurth et al., unpubl. data).
The inability of the penguin populations to recover may
not be attributed solely to the time available between succes-
sive periods of impoverished food resources. The slow recov-
ery after El Nin
˜o events suggests that other factors might also
be at play. Boersma (1998b) noted higher mortality of females
than of males during strong El Nin
˜o events that lead to an
unbalanced sex ratio among survivors. The effect of such an
imbalance on the mating system of the penguins is unknown,
but a higher male:female ratio could dampen the recovery of
the population once released from the constraints of food
shortage. Flooding associated with El Nin
˜o could lead to nest
failure and desertion. In 1982–1983, over 2700 mm of rain was
recorded at Academy Bay (Santa Cruz) where the annual aver-
age (1965–2003) was only 500 mm. Flooding may be a particu-
lar problem for Gala
´pagos penguins as has been documented
for the Humboldt (Paredes and Zavalaga, 2001) and African
penguins (Wilson, 1985). Kelvin waves (eastward propagating
waves caused by fluctuations in wind speed at the ocean sur-
face at the Equator) in a strong El Nin
˜o create higher than nor-
mal sea levels around the Gala
´pagos, (Fig. 3., ftp:// and are expected
to increase risks of flooding. Most Gala
´pagos penguin nests
are usually sited less than 2 m above sea level (Vargas, unpubl.
data). In May 2004, a swell (wave) at Isla Mariela Mediana
(0°3503100 S, 91°5019.500 W) caused the loss of four nests with
eggs and chicks (two chicks were drowned in one of these
nests, Vargas, unpubl. data).
It is still unknown how the moult affects penguin survival
and breeding success during warm El Nin
˜o and cold La Nin
events. Some unanswered questions are whether penguins
are able to moult during El Nin
˜o or if penguins are capable
of moulting more than once in a year of La Nin
˜a when food
conditions would be favourable for laying multiple clutches.
Moulting requires energy and results in high thermoregula-
tion costs (Payne, 1972). Accordingly, the survival strategy of
this species of penguins would require that the penguins: (1)
build up energy reserves at sea, (2) moult on land, (3) return
to the sea to build up energy reserves again, and (4) begin
their breeding cycle. Preliminary data and incidental observa-
tions on the Gala
´pagos penguin suggest that, when not
moulting, this species is primarily at sea during the day and
on land at night (Boersma, 1977).
4.5. Implications for conservation
The data that we present here on the effects of El Nin
˜o on the
´pagos penguin is important to conservation biology be-
cause this species is endemic, rare, and, as we reveal, appar-
ently declining. We have demonstrated that the decline of the
´pagos penguin is associated with a change in climate that
is, at least, partly attributable to global human activity
(Houghton et al., 2001; Timmermann et al., 1999). Therefore,
the Gala
´pagos penguin is predicted to be at higher risk in
the 21st century as temperatures and precipitation will very
likely continue to rise as the ENSO shifts towards more warm-
ing events (Easterling et al., 2000; Houghton et al., 2001).
The fact that the Gala
´pagos penguin has survived for mil-
lennia in the face of El Nin
˜o (perhaps even stronger that those
of 1982–1983 and 1997–1998) is no cause for complacency as
other conditions have now changed. Before 1535, the Gala
gos Islands were uninhabited by people. Whereas currently,
nearly 27,000 humans reside there and about 100,000 tourists
visit annually (Boersma et al., 2005). There are several human-
caused effects that can lead to further reductions of post-El
˜o populations of the Gala
´pagos Penguin. The commercial
fishery compete with penguins for the sardines and mullets,
particularly during El Nin
˜o events when fish populations are
reduced, and penguins become entangled in gillnets (Stein-
furth, pers. com., see Darby and Dawson, 2000). Furthermore,
mosquitoes (Culex quinquefasciatus) that arrived on the Gala
pagos in the 1980s (Peck et al., 1998) because of human ac-
tions benefit from the warm and wet conditions of El Nin
The C. quinquefasciatus mosquitoes represent a potential
new threat for Gala
´pagos penguin (Miller et al., 2001) because
C. quinquefasciatus are vectors for avian malaria (Fonseca
et al., 1998), and penguins in the genus Spheniscus are highly
susceptible to avian malaria (Fix et al., 1988; Graczyk et al.,
1995). There is also concern about the potential arrival to
´pagos of the mosquito-born West Nile virus (Wikelski
et al., 2004) that can infect penguins (Travis et al., submitted).
The threats outlined alone or in combination (see Huyser
et al., 2000) may be exacerbated by the low genetic diversity
of the Gala
´pagos penguin that could have arisen from the ef-
fects of population bottlenecks imposed by El Nin
˜o episodes
and coupled with the effects of increased human activity
(Akst et al., 2002).
In a population viability analysis (PVA) workshop in Febru-
ary 2005, researchers estimated that under the current El
˜o scenario, based on the frequency and intensity of El
˜o events described here, the Gala
´pagos penguin has a
30% probability of extinction within the next century (CBSG,
2005; Vargas et al., in preparation). The likelihood of extinc-
tion increases when other catastrophic factors such as
disease outbreaks, oil spills, or predation by introduced pre-
dators are added into the simulations (CBSG, 2005; Travis
BIOLOGICAL CONSERVATION 127 (2006) 107114 111
et al., submitted). The Gala
´pagos penguin would be especially
at higher risk of extinction after strong El Nin
˜o events when
the population would be at lower levels.
Of course, direct management of the global human activi-
ties that probably underlie the increased frequency and sever-
ity of El Nin
˜o is beyond the scope of local strategies. However,
our results reveal that the situation of the Gala
´pagos penguin
is more fragile than previously realized and greater attention
should be paid to curtailing human activities that are increas-
ingly affecting this species.
4.6. Future perspectives and conservation
The diet of the Gala
´pagos penguin is virtually unknown. Con-
servation efforts will benefit from determination of seasonal
variation in diet. The distribution and abundance of prey spe-
cies could be better linked to changes in sea temperature,
underwater topography, and nutrient levels.
The population dynamics of the Gala
´pagos penguin living
in a climatically variable and unpredictable environment still
needs further study. Information on the age of first breeding,
longevity, annual breeding success and survival rates, recruit-
ment of juveniles, natal philopatry, and movements during
ENSO episodes is crucial for the conservation of this endan-
gered species.
Climatologists and wildlife managers should collaborate to
conserve the Gala
´pagos penguin. Climate models that suc-
cessfully predict El Nin
˜o events one or two years in advance
(see Chen et al., 2004) are of fundamental importance so that
timely and effective actions could be undertaken by wildlife
managers prior to extreme El Nin
˜o episodes.
Conservation actions should focus at reducing mortality of
adult birds, which could compensate, at least partially, for the
mortality losses during strong El Nin
˜o events. Reducing direct
and indirect anthropogenic-induced threats to the population
will enhance adult survival. Predation by exotic mammals,
entanglement in fishing nets, oil spills, and outbreaks of dis-
eases should be prevented (see CBSG, 2005, PVA report for
descriptions of research and management recommenda-
tions). Therefore, here we recommend the following priority
specific conservation actions:
1. Control feral cats (Felis catus) on Isabela. In early 2005, cats
were reported preying on adult penguins at Caleta Iguana,
Southern Isabela (Steinfurth, unpubl. data) Cats could also
prey on eggs and chicks in the nest.
2. Prohibit the use fishing nets within foraging ranges of pen-
guins. Fishing nets deployed for mullet and shark are
known to cause deaths by entanglement.
3. Prevent arrival of introduced vectors and diseases. Efforts
should be aimed at preventing the arrival of vectors (e.g.,
mosquitoes) and diseases, such as the West Nile virus
and avian malaria to which penguins are known to be
highly susceptible.
We are very grateful to P.D. Boersma for her invaluable exper-
tise on the Gala
´pagos penguin and critical evaluation of ear-
lier drafts of this manuscript. We thank K. Trenberth for
advice on SST analysis and on El Nin
˜o. P. Johnson helped with
statistics. M. Steinitz-Kannan, R. Wilson, E. Travis, and S. Bar-
low provided helpful comments. We are grateful to the staff of
the Charles Darwin Research Station (CDRS) and the Gala
gos National Parks Service (GNPS) for assistance with the
recording of meteorological data and for participating in
penguin counts. The GNPS granted permission to carry out
the work and provided logistical support. Financial support
was provided by D. Swarovski & Co., Seaworld, and the Dar-
Fig. 3 – Gala
´pagos sea level anomalies from tide gauge at (0°4500 S, 90°1900 W) Santa Cruz, Gala
´pagos (January 1980–December
2004). The sea level reached 20–35 cm higher than average during the two strong El Nin
˜o events of 1982–1983 and 1997–1998.
Sea level in December 1997 was slightly higher than the maximum observed during the 1982–1983 El Nin
˜o (figure based on
monthly data available at:
112 BIOLOGICAL CONSERVATION 127 (2006) 107114
win Initiative. Further support was provided by the Gala
Conservation Trust, the Whitley Laing Foundation, and the
Swiss Friends of Gala
Akst, E.P., Boersma, P.D., Fleischer, R.C., 2002. A comparison of
genetic diversity between the Gala
´pagos Penguin and the
Magellanic Penguin. Conservation Genetics 3, 375–383.
Barber, R.T., Chavez, F.P., 1983. Biological consequences of El Nin
Science 222, 1203–1210.
BirdLife International, 2000. Threatened Birds of the World. Lynx
Edicions and BirdLife International, Barcelona and Cambridge,
Boersma, P.D., 1974. The Gala
´pagos penguin: adaptations for life
in an unpredictable environment. PhD. Thesis, Ohio State
Boersma, P.D., 1977. An ecological and behavioral study of the
´pagos Penguin. Living Bird 15, 43–93.
Boersma, P.D., 1978. Breeding patterns of Gala
´pagos penguins as
an indicator of oceanographic conditions. Science 200,
Boersma, P.D., 1998a. Population trends of the Gala
´pagos penguin:
Impacts of El Nin
˜o and La Nin
˜a. Condor 100, 245–253.
Boersma, P.D., 1998b. The 1997–1998 El Nin
˜o: impacts on
penguins. Penguin Conservation (November), 10–11.
Boersma, P.D., Vargas, H., Merlen, G., 2005. Living laboratory in
peril. Science 308, 925.
CBSG, 2005. Gala
´pagos Penguin Population and Habitat Viability
Assessment: Draft Report. IUCN/SSC Conservation Breeding
Specialist Group, Apple Valley, MN.
Chavez, F.P., Strutton, P.G., Friederich, G.E., Feely, R.A., Feldman,
G.C., Foley, D.G., McPhaden, M.J., 1999. Biological and chemical
response of the equatorial pacific ocean to the 1997–1998 El
˜o. Science 286, 2126–2131.
Chen, D., Cane, M.A., Kaplan, A., Zebiak, S.E., Huang, D., 2004.
Predictability of El Nin
˜o over the past 148 years. Nature 428,
Crawford, R.J.M., Shannon, L.J., Whittington, P.A., 1999. Population
dynamics of the African Penguin Spheniscus demersus at
Robben Island, South Africa. Marine Ornithology 27,
Crawford, R.J.M., Shelton, P.A., 1978. Pelagic fish and seabird
interrelationships off the coasts of South West and South
Africa. Biological Conservation 14, 85–109.
Croxall, J.P., Trathan, P.N., Murphy, E.J., 2002. Environmental
change and antarctic seabird populations. Science, 1510–1514.
Darby, J.T., Dawson, S.M., 2000. Bycatch of yellow-eyed penguins
(Megadyptes antipodes) in gillnets in New Zealand waters
1979–1997. Biological Conservation 93, 327–332.
Easterling, D.R., Meehl, G.A., Parmesan, C., Changnon, S.A., Karl,
T.R., Mearns, L.O., 2000. Climate extremes: observations,
modeling, and impacts. Science 289, 2068–2074.
Fix, A.S., Waterhouse, C., Greiner, E.C., Stoskopf, M.K., 1988.
Plasmodium relictum as a cause of avian malaria in wild-caught
Magellanic Penguins Spheniscus magellanicus. Journal of
Wildlife Diseases 24, 610–619.
Fonseca, D.M., Atkinson, C.T., Fleischer, R.C., 1998. Microsatellite
primers for Culex pipiens quinquefasciatus, the vector of avian
malaria in Hawaii. Molecular Ecology 7, 1617–1619.
Graczyk, T.K., Brossy, J.J., Plos, A., Stoskopf, M.K., 1995. Avian
malaria seroprevalence in jackass penguins (Spheniscus
demersus) in South Africa. Journal of Parasitology 81,
Grant, S.W., Duffy, D.C., Leslie, R.W., 1994. Allozyme phylogeny of
Spheniscus penguins. Auk 111, 716–720.
Hays, C., 1986. Effects of the 1982–1983 El Nin
˜o on Humboldt
penguin colonies in Peru. Biological Conservation 36, 169–180.
Houghton, J., Ding, Y., Griggs, D., Noguer, M., van der Linden, P.,
Dai, X., Maskell, K., Johnson, C. (Eds.), 2001. Climate Change
2001: The Scientific Basis. Third Assessment Report of the
Intergovernmental Panel on Climate Change. Cambridge
University Press, Cambridge.
Houvenaghel, G.T., 1984. Oceanographic setting of the Gala
Islands. In: Perry, R. (Ed.), Key Environments – Gala
Pergamon Press, Oxford, pp. 43–54.
Huyser, O., Ryan, P.G., Cooper, J., 2000. Changes in population size,
habitat use and breeding biology of lesser sheathbills (Chionis
minor) at Marion Island: Impacts of cats, mice and climate
change? Biological Conservation 92, 299–310.
´come, R., Ospina, P., 1999. La Reserva Marina de Gala
´pagos. Un
˜o difı
´cil. In: Ospina, P., Mun
˜oz, E. (Eds.), Informe
´pagos 1998–1999. Fundacio
´n Natura-WWWF, Quito, pp.
Karl, T.R., Trenberth, K.E., 2003. Modern global climate change.
Science, 1719–1724.
La Cock, G.D., 1986. The Southern oscillation, environmental
anomalies, and mortality of two southern African Seabirds.
Climatic Change 8, 173–184.
McPhaden, M.J., Zhang, D., 2002. Slowdown of the meridional
overturning circulation in the upper Pacific Ocean. Nature 415,
Miller, G.D., Hofkin, B.V., Snell, H., Hahn, A., Miller, R.D., 2001.
Avian malaria and MarekÕs disease: potential threats to
´pagos penguins Spheniscus mendiculus. Marine Ornithology
29, 43–46.
Mills, K., Vargas, H., 1997. Current status, analysis of census
methodology, and conservation of the Gala
´pagos Penguin
(Spheniscus mendiculus). Noticias de Gala
´pagos 58, 8–15.
Mills, K.L., 2000. Diving behaviour of two Gala
´pagos Penguins
Spheniscus mendiculus. Marine Ornithology 28, 75–79.
Nicolaides, F., Murillo, J.C., 2001. Efectos de El Nin
˜o 1997–1998 y
Post Nin
˜o 1990 en la pesca del bacalao Mycteroperca olfax yla
lisa rabo negro (Mugil cephalus) de las Islas Gala
´pagos. In:
´, C., Ruiz, R.E., Valle, C. (Eds.), Informe Gala
2000–2001. Fundacio
´n Natura and WWF, Quito, pp. 104–109.
Paredes, R., Zavalaga, C.B., 2001. Nesting sites and nest types as
important factors for the conservation of Humboldt penguins
(Sphensicus humboldti). Biological Conservation 100,
Payne, R.B., 1972. Mechanisms and control of molt. In: Farner,
D.S., King, J.R., Parkes, K.C. (Eds.), Avian Biology. Academic
Press, New York, pp. 103–155.
Peck, S.B., Heraty, J., Landry, B., Sinclair, B.J., 1998. Introduced
insect fauna of an oceanic archipelago: the Gala
´pagos Islands,
Ecuador. American Entomologist 44, 218–237.
Ratcliffe, N., Catry, P., Hamer, K.C., Klomp, N.I., Furness, R.W.,
2002. The effect of age and year on the survival of breeding
adult Great Skuas Catharacta skua in Shetland. Ibis 144,
Riedinger, M.A., Steinitz-Kannan, M., Last, W.M., Brenner, M.,
2002. A similar 6100 C-14C yr record of El Nin
˜o activity from
the Gala
´pagos Islands. Journal of Paleolimnology 27, 1–7.
Rodbell, D.T., Seltzer, G.O., Anderson, D.M., Abbott, M.B., Enfield,
D.B., Newman, J.H., 1999. An asymptotically equal to 15,000-
Year Record of El Nin
˜o-Driven Alluviation in Southwestern
Ecuador. Science 283, 516–519.
Sinclair, A.R.E., Krebs, C.J., 2002. Complex numerical responses to
top-down and bottom-up processes in vertebrate populations.
Philosophical Transactions of the Royal Society of London
Biological Sciences 357, 1221–1231.
Snell, H., Rea, S., 1999. The 1997–98 El Nin
˜o in Gala
´pagos: can 34
years of data estimate 120 years of pattern? Noticias de
´pagos 60, 11–20.
BIOLOGICAL CONSERVATION 127 (2006) 107114 113
Timmermann, A., Oberhuber, J., Bacher, A., Esch, M., Latif, M.,
Roeckner, E., 1999. Increased El Nin
˜o frequency in a climate
model forced by future greenhouse warming. Nature 398,
Travis, E.K., Vargas, F.H., Merkel, J., Gottdenker, N., Jime
´tegui, G., Miller, E., Parker, P.G., submitted for publication.
Hematology, serum chemistry, and disease surveillance of the
´pagos penguin (Spheniscus mendiculus) in the Gala
Islands, Ecuador.
Trenberth, K.E., 1997. The Definition of El Nin
˜o. Bulletin-
American Meteorological Society 78, 2771–2778.
Trenberth, K.E., Hoar, T.J., 1996. The 1990–1995 El Nin
oscillation event: longest on record. Geophysical Research
Letters 23, 57–60.
Trenberth, K.E., Hoar, T.J., 1997. El Nin
˜o and climate change.
Geophysical Research Letters 24, 3057–3060.
Trenberth, K.E., Stepaniak, D.P., 2001. Indices of El Nin
˜o evolution.
Journal of Climate 14, 1697–1701.
Valle, C.A., Coulter, M.C., 1987. Present status of the flightless
Cormorant, Gala
´pagos Penguin and Greater Flamingo
populations in the Gala
´pagos Islands Ecuador after the
1982–1983 El Nin
˜o. Condor 89, 276–289.
Valle, C.A., Cruz, F., Cruz, J.B., Merlen, G., Coulter, M.C., 1987. The
impact of the 1982–1983 El Nin
˜o southern oscillation on
seabirds in the Gala
´pagos Islands, Ecuador. Journal of
Geophysical Research 92, 14437–14443.
Vargas, F.H., Johnson, P., Lacy, R., Crawford, R., Steinfurth, A.,
Macdonald, D.W. in preparation. Modelling the effect of El
˜o on the endangered Gala
´pagos penguin.
Vargas, F.H., Wiedenfeld, D., 2004. Summary Report: 2004 Penguin
and Cormorant Survey. University of Oxford and Charles
Darwin Foundation, Oxford.
Vargas, H., 1999. Ornithological notes from Gala
´pagos in 1998. In:
Ospina, P., Mun
˜oz, E. (Eds.), Gala
´pagos Report 1998–1999.
WWF- Fundacio
´n Natura, Quito, p. 72.
Vargas, H., Lougheed, C., Snell, H., 2005. Population size and
trends of the Gala
´pagos Penguin Spheniscus mendiculus.Ibis
147, 367–374.
Weimerskirch, H., Stahl, J.C., Jouventin, P., 1992. The breeding
biology and population dynamics of King Penguins Aptenodytes
patagonica on the Crozet Islands. Ibis 134, 107–117.
White, T.C.R., 2004. Limitation of populations by weather-driven
changes in food: a challenge to density-dependent regulation.
Oikos 105, 664–666.
Wikelski, M., Foufopoulos, J., Vargas, H., Snell, H., 2004.
´pagos birds and diseases: invasive pathogens as
threats for island species. Ecology and Society 9 (1), 5.
Available from: URL:
Wilson, R.P., 1985. Seasonality in diet and breeding success of the
Jackass Penguin Spheniscus demersus. Journal Fu
¨r Ornithologie
126, 53–62.
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... That is, the studies collected primary data on the Galapagos Islands and discussed the effects of climate change on endemic fauna, despite not being the central topic of the study. Nine additional studies were provided by the CDF [28,37,46,[53][54][55][56][57] . One more study that was published after February 8, 2020, was included in the review because of the relevant information provided, that is, the effects of climate change on the Galapagos sea lion [44] . ...
... Inshore birds, including the Galapagos penguin and flightless cormorants ( Phalacrocorax harrisi ), are amongst the most affected seabirds by ENSO [55] . Adult survival of the Galapagos penguin is reduced during ENSO years, with increased mortality during two strong ENSO of 1983 and 2004 of 77% and 65%, respectively [1,56,58,66] . In 1983, there was also a 50% population decline observed for flightless cormorants [55] . ...
... In addition to impacts on survival and population status, reproduction was negatively affected in Galapagos penguins, as they only breed when environmental conditions are favorable to them [1,55,56,58] . Vargas et al. [58] found that during the two strong ENSOs of 1983 and 1998, no fledglings were observed during the yearly census, while during weaker ENSO, reproduction decreased by 20% [58] . ...
The Galapagos Islands are one of the most productive marine ecosystems in the world. The convergence of four ocean currents and the isolation of these islands create a variety of ecosystems that host unique biodiversity. Many of the endemic species are particularly vulnerable to disturbances in their environment, as most of them are unable to migrate or adapt in response to changing climatic conditions. Due to climate change, there is an increase in extreme weather patterns (El Niño-Southern Oscillation [ENSO] and La Niña events) and climate variability. These affect the productivity of marine and terrestrial ecosystems on the Galapagos Islands and ultimately disrupt natural processes and ecosystem dynamics. Here we conduct a systematic review on the impact on the increase of extreme weather events (ENSO and La Niña events) and climate variability on the biodiversity of the Galapagos Islands. We demonstrate that the increase in the frequency of ENSO events poses a major threat to endemic marine biodiversity, while it has positive impacts on many terrestrial species due to increase rainfall and food availability. In contrast, La Niña provides sometimes positive conditions for marine species allowing them to recover, while for many terrestrial species La Niña years result in worse conditions causing adverse effects. Therefore, the increased frequency of ENSO and La Niña years under climate change poses significant threats to the Galapagos biodiversity. Also, increased climate variability (not related to ENSO and La Niña events) has adverse impacts on marine and terrestrial species, putting biodiversity under even more pressure. The results of our review are key to understand the far-reaching implications of climate change on the Galapagos Islands and can be used to understand impacts on other archipelagos worldwide, which are often areas with high levels of (endemic) biodiversity.
... En cuanto a la temporalidad de los eventos podemos observar que el año con más registros corresponde al año 2016, esto podría estar asociado, además de la interacción con la pesca, al Fenómeno de El niño (ENSO) que afectó entre los años 2015-2016en Chile (Becker 2016, algo similar aconteció en las costas de Perú cuando se produjo el fenómeno de El niño entre los años 1983-1984 con resultados de mortandades masivas reduciendo las poblaciones hasta en un 65% (Hays 1986), algo muy similar a lo sucedido en poblaciones de pingüino de las Galápagosdurante los eventos del niño de 1983-1984 y 1997-1998 que redujo la población en un 77% y 65 % respectivamente (Vargas et al. 2006).Por lo tanto el fenómeno de El Niño (ENSO) sería un gravitante factor a considerar. ...
... Es en este periodo en donde los adultos se preparan para la muda de plumas, por lo tanto requieren forrajear conseguir alimento durante largos periodos para sobrellevar las semanas sin alimento (De la Puente et al. 2013). FIGURA 6.-Total de eventos de varamiento para las especies de pingüinos distribuidos entre los meses del año. ...
Full-text available
La mortalidad masiva de animales siempre es una advertencia de que existe o ha existido una perturbación en el ecosistema. Los cadáveres son la principal fuente de información y las aves marinas, por sus singulares características, son especies claves a la hora de estudiar la salud de los ecosistemas que habitan. En este trabajo se recopilaron 852 datos de varamientos de seis especies de pingüinos entre los años 2009 y 2016 para las costas de Chile continental, cuyo objetivo es dar a conocer la problemática existente. Los resultados indican que el género Spheniscus es el grupo con más registro de varamientos (97,1 %), la región de Valparaíso (V Región) es la que presenta la mayor cantidad de eventos (n=267) y el año 2016 es el que ha presentado una mayor frecuencia de eventos (n=174). Con estos registros, es posible generar una base de datos que servirá en el futuro para estudiar los patrones espacio-temporales de varamientos para este importante grupo, lo que ayudará a optimizar el monitoreo de estas poblaciones para anticipar posibles eventos de varamiento.
... For example, an increased stress response was observed in Magellanic penguins when high rainfall caused nest flooding and decreased the reproductive success of the population (Walker et al., 2014). Similarly, two severe El Niño weather events were responsible for the considerable population decline of Galapagos penguins (Spheniscus mendiculus) by causing a shift in marine productivity and decreasing the availability of prey (Vargas et al., 2006). ...
... Following this storm event, hundreds of kororā were found wrecked on Auckland and Northland coastlines (Robson, 2018) and most of those necropsied by Massey University had empty stomachs (Massey University Auckland, 2018), indicating they were unable to find sufficient food. (Vargas et al., 2006). Severe weather events in South Australia have caused kororā to breed later (Chambers, 2004) and have caused flooding and other damage to kororā burrows, resulting in decreased fledging rate (Ross et al., 1996). ...
Full-text available
Using three study sites in the Hauraki Gulf, this study aimed to determine whether changes in foraging ecology and stress physiology were observed in kororā populations over time and space and whether these measurements could be used as indicators of marine ecosystem health. Kororā are inshore foragers and do not migrate following breeding, therefore they are reliant on local marine resources year-round and may act as a high-resolution marine indicator over a small spatial scale.
... Thirty-eight bird species showed a significant association with ENSO − (Table 1), including studies from Canada, the USA, Mexico, Jamaica, Costa Rica, Panama, Ecuador, Peru, Brazil, South Georgia, the UK, Spain, Seychelles, French Sub-Antarctic Islands, Australia, New Zealand, and Antarctica (Chastel, Weimerskirch & Jouventin, 1993;Lyver, Moller & Thompson, 1999;Sillett, Holmes & Sherry, 2000;Gaston & Smith, 2001;Ramos et al., 2002;Barbraud & Weimerskirch, 2003;Jenouvrier et al., 2005;Mazerolle et al., 2005;Chambers & Loyn, 2006;Forcada et al., 2006;Sedinger et al., 2006;Vargas et al., 2006Vargas et al., , 2007Lee, Nur & Sydeman, 2007;Balbontin et al., 2009;Devney, Short & Congdon, 2009;Norman & Chambers, 2010;Rolland et al., 2010;Wolf et al., 2010;Ancona et al., 2011;Baylis et al., 2012;Schmidt et al., 2014;Woehler et al., 2014;Wolfe, Ralph & Elizondo, 2015;Horswill et al., 2016;Townsend et al., 2016;Anderson et al., 2017;Sandvig et al., 2017;Barbraud et al., 2018;Velarde & Ezcurra, 2018;Woodworth et al., 2018;Jones & DuVal, 2019;McKechnie et al., 2020;Tavares et al., 2020;Cleeland et al., 2021;Smart, Smith & Riehl, 2021). These 38 bird species show the mean response (points) and 95% confidence intervals (solid lines). ...
Climate is a major extrinsic factor affecting the population dynamics of many organisms. The Broad-Scale Climate Hypothesis (BSCH) was proposed by Elton to explain the large-scale synchronous population cycles of animals, but the extent of support and whether it differs among taxa and geographical regions is unclear. We reviewed publications examining the relationship between the population dynamics of multiple taxa worldwide and the two most commonly used broad-scale climate indices, El Niño-Southern Oscillation (ENSO) and North Atlantic Oscillation (NAO). Our review and synthesis (based on 561 species from 221 papers) reveals that population changes of mammals , birds and insects are strongly affected by major oceanic shifts or irregular oceanic changes, particularly in ENSO-and NAO-influenced regions (Pacific and Atlantic, respectively), providing clear evidence supporting Elton's BSCH. Mammal and insect populations tended to increase during positive ENSO phases. Bird populations tended to increase in positive NAO phases. Some species showed dual associations with both positive and negative phases of the same climate index (ENSO or NAO). These findings indicate that some taxa or regions are more or less vulnerable to climate fluctuations and that some geographical areas show multiple weather effects related to ENSO or NAO phases. Beyond confirming that animal populations are influenced by broad-scale climate variation, we document extensive patterns of variation among taxa and observe that the direct biotic and abiotic mechanisms for these broad-scale climate factors affecting animal populations are very poorly understood. A practical implication of our research is that changes in ENSO or NAO can be used as early signals for pest management and wildlife conservation. We advocate integrative studies at both broad and local scales to unravel the omnipresent effects of climate on animal populations to help address the challenge of conserving biodiversity in this era of accelerated climate change.
... Species with narrow thermal ranges mostly belonged to the families Spheniscidae, Laridae, Alcidae and Phocidae and were mainly found in polar and tropical regions (Table 1, Figure 4). The associated vulnerability of these species to climate change has been demonstrated through studies on populations of the Galapagos penguin, Spheniscus mendiculus, the Guanay cormorant, Leucocarbo bougainvilliorum, and the Peruvian booby, Sula variegata, that have declined in response to increasing SST (Vargas et al. 2006;Barbraud et al. 2018). ...
Full-text available
Understanding climate change impacts on top predators is fundamental to marine biodiversity conservation, due to their increasingly threatened populations and their importance in marine ecosystems. We conducted a systematic review of the effects of climate change (prolonged, directional change) and climate variability on seabirds and marine mammals. We extracted data from 484 studies (4808 published studies were reviewed), comprising 2215 observations on demography, phenology, distribution, diet, behaviour, body condition and physiology. The likelihood of concluding that climate change had an impact increased with study duration. However, the temporal thresholds for the effects of climate change to be discernibly varied from 10 to 29 years depending on the species, the biological response and the oceanic study region. Species with narrow thermal ranges and relatively long generation times were more often reported to be affected by climate change. This provides an important framework for future assessments, with guidance on response- and region-specific temporal dimensions that need to be considered when reporting effects of climate change. Finally, we found that tropical regions and non-breeding life stages were poorly covered in the literature, a concern that should be addressed to enable a better understanding of the vulnerability of marine predators to climate change.
... Increases in the frequency of El Niño events are predicted to lead to decreased ocean productivity, altered food web dynamics, and shifts in species distributions (Walther et al. 2002;Hoegh-Guldberg and Bruno 2010;DiLorenzo and Miller 2017). Changes in the availability and distribution of fish species may impact the prey availability for top predators like seabirds, with consequences for their behavior, physiology, and demography (Vargas et al. 2006;Grémillet and Boulinier 2009;Oro 2014;Champagnon et al. 2018). Seabirds are currently the most threatened group of birds (Croxall et al. 2012) and conservation actions that anticipate the effects of climate change on their populations are required (Monahan and Fisichelli 2014). ...
Full-text available
The El Niño Southern Oscillation (ENSO) is a recurrent climatic pattern with important ecological consequences for seabirds due to its impacts on the abundance and distribution of food resources. We investigated the effects of ENSO phases on the foraging ecology of a marine top predator at Clarion Island in the Eastern Tropical Pacific using GPS and time-depth recorder data and regurgitates from incubating masked boobies (Sula dactylatra) during 3 consecutive years. Foraging locations were recorded in 2016 (El Niño, one female, three males), 2017 (neutral; six females, nine males), and 2018 (La Niña; eight females, ten males). Local sea surface temperature (SST) and chlorophyll-a concentration (CHL) within the birds’ foraging range were compared among the 3 years. Regurgitates were collected opportunistically from 25 and 31 incubating adults in 2017 and 2018, respectively. Average local CHL and SST were similar among years (mean SST 25 °C; mean CHL 0.10 and of 0.09 mg m−3 in January and March, respectively). Masked boobies travelled a maximum of 66 ± 34 km from the colony. The maximum trip duration was 7.7 ± 3.4 h and total distance travelled during a foraging trip was 164 ± 73 km, with no sex- or year-related differences. Masked boobies mainly caught flying fish, but their diet also included one squid and six other fish families. In contrast to previously reported changes in foraging ecology of seabirds, masked boobies at Clarion Island seemed to be unaffected during El Niño, because the local oceanography was relatively unperturbed by ENSO oscillations.
... SST readings during these events were between 25.0 o C and 28.6 o C for February and March 1973, 1976, 1983and 1998(Charles Darwin Foundation 2018. A global decadal increase of 0.19 o C in the period 1979-1998 (Vargas et al. 2007), in which two of the strongest El Niño events occurred in the archipelago, had great impacts on marine biodiversity (Trillmich & Limberger 1985, Nelson et al. 2004, Vargas et al. 2006 and may have affected the dispersal ability of species that actively or passively move through the archipelago. ...
Full-text available
A female Yellow-bellied Sea Snake Hydrophis platurus of 720 mm total length and 172 g was found dead at James Bay, Santiago Island in March 2018. Based on an analysis of this and other specimens of the species collected in the archipelago since 1970, we consider their probable origins as drifters on currents from coastal waters between Costa Rica and the Ecuadorian mainland. Identifiable gut contents of Galapagos specimens consisted of fish larvae. The new specimen is stored in the Vertebrate Collection of the Charles Darwin Research Station.
Mostly indirectly, but also through direct mechanisms, climate change is becoming an increasingly significant threat to seabird populations globally. Marine ecosystems and associated trophic linkages are being influenced by changing climatic conditions, while breeding colonies are being subjected to an increasing frequency of heat waves, storms, and unusual precipitation events. We provide an overview of the different responses of seabirds to climate change, including examples of distributional, phenological, demographic, and dietary changes that have been observed. Climate change is largely impacting predator-prey dynamics, and we elaborate on mechanisms and examples of how seabirds are being affected by changes in the distribution and biomass of their prey. Different life history stages vary in their vulnerability to climate change, and we discuss these different stages independently, highlighting the need for a stronger research focus on nonbreeding seabirds, both adults outside the breeding season and juveniles. We discuss factors such as life history traits and geographic distribution that influence vulnerabilities of different species to climate change before elaborating on challenges in understanding and predicting the influence of climate change on seabirds. Particularly noteworthy is the inconsistency between seabird species, even within the same regions, in terms of their responses to climate change. A better understanding of the intrinsic and extrinsic factors giving rise to species-specific vulnerabilities to climate change, and the interaction with other threats associated with biodiversity loss, is needed for improved seabird conservation management.
The endemic vertebrates of the Galápagos Islands evolved and adapted over thousands of years. In the last 500 years human activities have exerted great pressures on their populations, in some cases taking them to extinction. From the middle of the 20th century, protection and restoration of the species and habitats of Galápagos have been increasing, but the threats to the islands have also become more diverse because of globalization and ease of movement, with the potential for greater impacts. Of 120 endemic reptiles, birds and mammals (fish are excluded from his review and there are no endemic amphibians), seven are extinct and one extinct in the wild, with another 62 species in the highest categories of the IUCN Red List of Threatened Species (Critical Endangered, Endangered, Vulnerable). According to evidence in 95 sources, the principal threats affecting Galápagos vertebrates include human disturbance, and invasive species that compete with the endemics, predate them and destroy their habitats. The Galápagos National Park Directorate (GNPD) and Biosecurity Agency (GBA) are charged with controlling and preventing the introduction of such species, with scientific support from ONGs and Universities. However, there is a huge knowledge gap regarding the impacts of such threats on individual species, and much more research is needed for the better protection of vertebrate species and their habitats.
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The Galapagos Penguin Spheniscus mendiculus (GAPE), Flightless Cormorant Phalacrocorax harrisi (FLCO), and Waved Albatross Phoebastria irrorata (WAAL) are marine birds that are endemic to the Galapagos Islands. To provide health information for these three species, baseline data on several physiological parameters were collected non-invasively—from individuals and populations appearing to be healthy—during the course of physical examinations that were conducted from 2011–2019. Heart rate, respiratory rate, body temperature, and body condition (weight vs. morphometric measurements) were analyzed as a function of age and sex. Mean heart rate differed significantly between juveniles and adults in all three species. Respiratory rate and body temperature varied with species, age, and sex; body condition index of GAPE, FLCO, and WAAL showed that males are heavier than females. We briefly speculate on the ecological context of these patterns.
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The Galápagos Penguin (Spheniscus mendiculus) population probably has always been small and largely restricted to the islands of Fernandina and Isabela. Counts suggest the current population of Galápagos Penguins is likely between 4,250 and 8,500, half of what it was in the early 1970s. Population size has varied and declined probably because of substantial changes in oceanic conditions. Body condition as evidenced by weight is enhanced during cold surface water conditions, La Niña, and deteriorates when surface waters are warmed, El Niño, and under the most severe conditions, penguins starve. Analysis of a long-term data set from counts of the population suggests that the population has fluctuated, dropping precipitously after the 1982-1983 El Niño and has since then been recovering very slowly. This parallels the overall warming in the Pacific during the last 20 years associated with the more frequent El Niño and less frequent La Niña events. These trends suggest that long-term global climate warming is likely to threaten the Galápagos Penguin population particularly because the population is small and its distribution restricted. New threats from climatic warming and increasing human perturbations such as fishing, inadvertent discharge of petroleum products, and transport of potential predators and pathogens to islands increase the risk of extinction.
African Penguins Spheniscus demersus recolonized Robben Island in 1983 when about nine pairs bred at the island. By 1996, the colony had grown to about 3100 pairs. Adult survival was probably between 0.82 and 0.90 in 1993/94, but fell to 0.75 in 1994/95 when many birds at the island were oiled following the sinking of the Apollo Sea in June 1994. Some penguins initiated breeding when two years old, and all were assumed to be breeding at age five. The proportion of mature birds that bred in a year varied between about 0.70 and 1.00. During a breeding season, pairs laid their first clutches between January and August, mostly in February and March. The average clutch was 1.86 eggs. Of lost clutches 32% were replaced, whereas 23% of pairs losing broods relayed and 21% of pairs that successfully fledged chicks relayed. On only one occasion was the laying of a third clutch during a breeding season recorded, and this was unsuccessful. The mean number of chicks fledged per breeding pair varied between 0.32 and 0.59 per annum. Both fledging success and immigration of immature birds to the colony were significantly related to the spawner biomass of Cape Anchovy Engraulis capensis, the most important prey item of penguins at the island. Growth of the colony has been driven by immigration. Depending on the values assumed for survival of adults and first-year birds, 59-87% of new adults in the colony resulted from immigration. Several birds banded as chicks at Dassen and Dyer islands were recorded breeding at Robben Island.
Blood samples from Galapagos Penguins Spheniscus mendiculus were screened for avian malaria and the avian herpesvirus Marek's Disease Virus (MDV) by the polymerase chain reaction (PCR), using Plasmodium and MDV-specific primers, respectively. Malaria was considered as a potential threat to these seabirds, in light of the fact that Culex quinquefasciatus, a known mosquito vector of Plasmodium, has recently been recovered in the Galapagos Islands, and because penguins are considered to be especially susceptible to this disease. The screening for MDV was undertaken because of the recent Marek's Disease epizootic in Galapagos domestic poultry. No evidence of existing infection with either of these pathogens was detected. However, the impact of introduced malaria on endemic birds in island systems such as Hawaii, and the death of over 800 chickens in Galapagos due to Mark's Disease, underscores the need for continued monitoring of exotic disease agents and the need to consider them as threats to endangered wildlife.
The African Penguin Spheniscus demersus has decreased markedly in numbers through the 20th Century. In the first half of the century its eggs were harvested commercially, probably at a rate of 48% of total eggs produced. In 1910, the number of birds aged two or older at Dassen Island was estimated to be 1.45 million. This decreased to 0.22 million in 1956,0.14 million in 1967 and just 0.03 million in 1990 - a loss of 98%. A colony may take more than 50 years to recover from a catastrophic oiling event, even with rehabilitation. In the long term, low-level chronic oiling can have a greater impact than a once-off catastrophic event, especially if disturbance results in substantial losses of clutches. The actual disturbance caused in searching for and collecting oiled birds requires further research, and techniques need to be developed to minimize this disturbance. The proportion of first-year birds that survive is probably about 0.5.
All the oceanographic properties in the Galapagos are determined or influenced directly or indirectly by waters flowing with the undercurrent. The terrestrial environment is also dependent upon these marine influences, which are responsible for severe climatological and ecological conditions. The sharp isolation of the Galapagos Islands provided by the local upwellings and the selecting conditions they impose upon life are the leading factors promoting species isolation and endemism in this remarkable archipelago.-from Author